Subscriber access provided by UNIV OF LOUISIANA
Critical Review
Sustainability analysis of microalgae production systems A review on resource with unexploited high-value reserves Arun K Vuppaladadiyam, Pepijn Prinsen, Abdul Raheem, Rafael Luque, and Ming Zhao Environ. Sci. Technol., Just Accepted Manuscript • DOI: 10.1021/acs.est.8b02876 • Publication Date (Web): 12 Nov 2018 Downloaded from http://pubs.acs.org on November 14, 2018
Just Accepted “Just Accepted” manuscripts have been peer-reviewed and accepted for publication. They are posted online prior to technical editing, formatting for publication and author proofing. The American Chemical Society provides “Just Accepted” as a service to the research community to expedite the dissemination of scientific material as soon as possible after acceptance. “Just Accepted” manuscripts appear in full in PDF format accompanied by an HTML abstract. “Just Accepted” manuscripts have been fully peer reviewed, but should not be considered the official version of record. They are citable by the Digital Object Identifier (DOI®). “Just Accepted” is an optional service offered to authors. Therefore, the “Just Accepted” Web site may not include all articles that will be published in the journal. After a manuscript is technically edited and formatted, it will be removed from the “Just Accepted” Web site and published as an ASAP article. Note that technical editing may introduce minor changes to the manuscript text and/or graphics which could affect content, and all legal disclaimers and ethical guidelines that apply to the journal pertain. ACS cannot be held responsible for errors or consequences arising from the use of information contained in these “Just Accepted” manuscripts.
is published by the American Chemical Society. 1155 Sixteenth Street N.W., Washington, DC 20036 Published by American Chemical Society. Copyright © American Chemical Society. However, no copyright claim is made to original U.S. Government works, or works produced by employees of any Commonwealth realm Crown government in the course of their duties.
Page 1 of 62
Environmental Science & Technology
1
Sustainability analysis of microalgae production
2
systems - A review on resource with
3
unexploited high-value reserves
4
Arun K. Vuppaladadiyam,‡a,b Pepijn Prinsen,‡c Abdul Raheem,‡a,b Rafael Luquec and
5
Ming Zhao,a,b,*
6 7
a
b
Key Laboratory for Solid Waste Management and Environment Safely, Ministry of
8 9 10
School of Environment, Tsinghua University, Beijing 100084 China.
Education, Beijing, 100084, China c
Departamento de Química Orgánica, Universidad de Córdoba, Campus de
Rabanales, Edificio Marie Curie (C-3), Ctra. Nnal. IV, Km 396, Córdoba, Spain.
11 12
KEYWORDS. Microalgae, biorefinery, sustainability, techno-economic assessment, life-
13
cycle analysis, socio-economic impact
14
ABSTRACT. Sustainability, at present, is a prominent aspect in the development of
15
production systems that aim to provide the future´s energy and material resources.
16
Microalgae are a promising feedstock, however, the sustainability of algae-based
ACS Paragon Plus Environment
1
Environmental Science & Technology
Page 2 of 62
17
production systems is still on debate. Commercial market volumes of algae derived
18
products are still narrow. The extraction and conversion of primary metabolites to
19
biofuels requires cultivation at large scales; cost-effective methods are therefore highly
20
desirable. This work presents a complete and up to date review on sustainability
21
analysis of various microalgae production scenarios, including techno-economic,
22
environmental and social impacts, both in large-scale plants for bioenergy production as
23
in medium-scale cultivars intended for the production of high added-value chemicals.
24
The results show that further efforts in algal based research should be directed to
25
improving the productivity, the development of multi product scenarios, a better
26
valorization of co-products, the integration with current industrial facilities to provide
27
sustainable nutrient resources from waste streams and the integration of renewable
28
technologies such as wind energy in algae cultivars.
29
Table of Contents
30 31 32
1. INTRODUCTION
33
The global population could reach and even exceed 9 billions by 2050.1 The
34
development of efficient conversion methods that use sustainable feedstocks to meet
ACS Paragon Plus Environment
2
Page 3 of 62
Environmental Science & Technology
35
the growing global energy demand and to reduce the use of fossil resources, is now an
36
imminent challenge for the research community. Around 87 % of the global CO2 emitted
37
by anthropogenic activities result from fossil resources, with coal, oil and natural gas
38
contributing 43, 36 and 20 %, respectively.2 In the EU, ca. 30 % of the total energy use
39
is spent in transport fuels.3 One way to convert CO2 and light energy into renewable
40
fuels, chemicals and energy is to store them in microalgae (biosequestration).
41
Microalgae can fix CO2 more efficiently than terrestrial plants (with biomass yields ca.
42
55 kg ha-1 year-1, twice as high) and do not directly compete with food crops for arable
43
land.4,5 Still, significant bottlenecks exist in the road towards sustainable commercial
44
microalgae derived production systems, due to techno-economic, environmental and
45
social constraints and challenges in their cultivation, harvesting and associated
46
downstream processes.
47
Recently, various reviews have been published in the field of sustainable microalgae
48
based production systems, including conversion to biofuels6-9 and high added-value
49
chemicals.10-12 Some of them focused on specific sustainability aspects such as the use
50
of industrial flue gas as CO2 source13 or wastewater (WW) as nutrient source,14-16 and
51
environmental applications.17,18 Some reviews deal with techno-economic assessment
52
(TEA) studies,19-21 others with life cycle analysis (LCA)22-24 and some with socio-
53
economic indicators.25 Rather few works evaluated the sustainability in all its
54
aspects.26,27 As progress is continuously being developed in various fields, including
55
metabolic engineering, cultivation, harvesting, extraction and conversion, these review
56
studies may help to clear out favorable routes towards sustainable industrial algal
57
production systems. The data available in the literature is hardly assesed in a
ACS Paragon Plus Environment
3
Environmental Science & Technology
Page 4 of 62
58
quantitative manner because they are rather dificult to compare due to differences in
59
model definitions, assumptions and boundaries and the high amount of biorefinery
60
scenarios and input parameters used.
61
The present work aims to evaluate the sustainability of different microalgae
62
biorefinery scenarios in a quantitative and up to date study based on techo-economic
63
assessment and life-cycle analysis. Key papers from the last seven years on TEA and
64
LCA studies were selected. Production costs of algal biomass, algal oil/biocrude and
65
algal biofuel were contrasted by comparing MAFBSP (minimum ash-free biomass
66
selling price) and MFSP (minimum fuel selling price) in various biorefinery scenarios
67
together with high impact variables (according to the sensitivity analysis if any).
68
MAFBSP and MFSP refer to prices to obtain a zero net present value (NPV) for a
69
specified internal rate of return after taxes, typically set at 10 % target). MAFBSP and
70
MFSP are accounting concepts, not real selling prices. Higher MAFBSP/MFSP means
71
that the (final) product needs to be sold at higher value for revenues and inflow cash
72
reaching breakeven level of the original capital investments. To correct these cost data
73
for the currency and inflation between different publication years, MAFBSP and MFSP
74
values are expressed in USD (2018), recalculated with the mean annual currency and
75
inflation rates (with respect to publication year). Next, important findings from the
76
literature are highlighted involving sensitivity, cost breakdown and market analysis,
77
which are important tools in TEA studies. In the section on LCA, net energy ratios
78
(NER), greenhouse gas (GHG) emissions and water footprints (WF) were compared for
79
the most prominent scenarios. All energy balances were expressed as NER values.
80
Data were also collected on algal biomass productivities using different wastewater
ACS Paragon Plus Environment
4
Page 5 of 62
Environmental Science & Technology
81
(WW) sources to evaluate their potential as nutrient source. In the last section, various
82
indicators of socio-economic impacts are highlighted. Finally, based on the main
83
conclusions, future prospects for algae-based research and commercial production
84
systems are summarized.
85
2. TECHNO-ECONOMIC ASSESSMENT (TEA)
86
Production systems must be techno-economically viable to be sustainable. This aspect
87
is currently still on debate in algae based biorefinery, due to the large uncertaincy in the
88
extrapolation of lab-scale data to large scale scenarios and depending on the data
89
available for every biorefinery scenario and the model boundary limits, giving raise to a
90
high degree of heterogeneity among the data.26-29
91
2.1.
92
An important part in the cost distribution is attributed to the algae biomass production
93
itself. This includes cultivation and harvesting. Figure 1 shows the biomass production
94
cost of various algal production systems including open raceway ponds (ORP) and
95
photobioreactors (PBR). The results show considerable variations in production costs
96
(MAFBSP), depending on the input parameters used and assumptions made in the TEA
97
scenarios. In some cases the production cost is competitive with the USA soybean
98
market price as the benchmark feedstock for competitiveness with first generation
99
biodiesel, whereas in other cases it largely exceeds it. The USA 2022 target price (entry
100
3) of 2.25 USD kg-1 may be a better reference to compare with.52 The large differences
101
in production costs are mainly the effect of varying biomass productivity, scale,
102
cultivation method and nutrient costs. The highest impact variable was the scale of
Algal biomass production
ACS Paragon Plus Environment
5
Environmental Science & Technology
Page 6 of 62
103 104
Figure 1. Minimum biomass selling price in TEA scenarios 1-7.
105
biomass production (1, 10, 100 and 400 ha in scenarios 1-2). But, the scale of economy
106
effect may be subjected to uncertainity, as real life data are rather scarce (instead they
ACS Paragon Plus Environment
6
Page 7 of 62
Environmental Science & Technology
107
are extrapolated from lab-scale or pilot scale data). The economy of scale effect in
108
algae production systems is limited by the modular character of the cultivation
109
systems.27,30
110
The cultivation method affects the cost considerably, as illustrated for ORP, tubular
111
(TPBR) and flat-plate (FPPBR) photobioreactors in scenario 1. Hoffmann compared
112
algal turf scrubbers (ATS, scenario 4a) with classic ORP cultivars (scenario 4b).33 ATS
113
systems are based on native cultures which dynamically adapt to changing conditions to
114
improve the culture stability and avoid crash events. The lipid content of ATS algal
115
biomass was however low (10 %) and they presented high ash content. Nevertheless,
116
the ATS cultivars produced algal biomass at 2620 USD ton-1, while ORP cultivars at
117
3460 USD ton-1, mainly due to the difference in cell density at harvesting (200 vs. 0.5 g
118
L-1, respectively). Rotating algal biofilm reactors (RABR, scenarios 5a-5e) are another
119
innovative cultivation method.34
120
The effect of zero cost nutrients is also noticeable (scenarios 2a and 2c vs. 2b and
121
2d). Some studies reported the use of WW as nutrient feed source and the supply of
122
CO2 from flue gas sources, but not all of them included the carbon credits associated
123
with the estimated storage and pump costs. Rezvani et al. studied the integration of
124
cultivars with different CO2 biosequestration methods (scenarios 6a-6j).35 The cultivation
125
method (ORP/PBR) and photosynthetic efficiency (PE) were also included as variables.
126
The effects were rather small and the production costs were low in all cases compared
127
with other studies, possibly due to the effect of other variables such as productivity, lipid
128
content and scale. The substantial lower cost also may have resulted from MAFBSP´s
ACS Paragon Plus Environment
7
Environmental Science & Technology
Page 8 of 62
129
definition; in this case it was calculated at an electricity price similar to that from a
130
conventional PP without CO2 capture and storage.
131
Important parameters in the selection of a suitable cultivar location include not only
132
the estimated PE and seasonal variations, but also governmental regulations and labour
133
costs as illustrated in scenarios 7a-7d. Ruiz et al. (2016) reported a tidous and realistic
134
analysis of ORP and PBR cultivars.27 They compared the capital and operational costs
135
on a 100 ha scale from current production facilities in several countries. They concluded
136
that FPPBR are the most cost-effective production system, with the best projections for
137
southern Spain (3.4 EUR kg-1).
138
2.2.
139
Algae harvesting (often followed by dewatering) is a bottleneck step, as it contributes
140
considerably in the overall biomass production cost.36,37 The energy consumed during
141
harvesting and dewatering can account up to 90 % of the total energy required for algal
142
biodiesel production.38 Typically, algae slurries ca. 1 wt% dry solids must be dewatered
143
to ca. 20 wt%. Centrifugation technologies work efficient but face large initial capital
144
investments. Figure S1 (see Supporting Information) shows the effect of the cell density
145
and lipid content on the energy use and the cultures size required to produce 1 L of
146
algal oil, showing that centrifugation should be considered more appropriate as a final
147
step in dewatering methods, especially at large scales.
Algae harvesting
148
Aggregation by flocculation and coagulation is one of the most cost-effective
149
harvesting technologies.39,40 Bioflocculation (BF) occurs at pH > 9, whereas chemical
150
flocculation techniques cover a broader pH range, employing cationic iron, aluminium
151
salts, lime, cellulose, polyacrylamide polymers, cationic starch or surfactants to alter the
ACS Paragon Plus Environment
8
Page 9 of 62
Environmental Science & Technology
152
physiochemical interaction between algae cell walls (negatively charged) and induce the
153
formation of aggregates. Around 95 % cell flocculation efficiency was achieved when
154
the pH of Nannochloropsis sp. cultures (107 cells mL-1) was adjusted to 10 by adding
155
Ca(OH)2.41 The corresponding harvesting cost was estimated as low as 7.5 USD ton-1
156
biomass and was further reduced to 3.5 USD ton-1 when the cell density reached 108
157
cells mL-1. When using chitosan flocculation (CHF) in a pre-concentration step, Xu et al.
158
found that up to 95 % of the energy required for harvesting via centrifugation can be
159
saved.42 Despite the promising results, chemical flocculation is not the best option from
160
an environmental point of view, especially when using aluminium salts.38 Chemical
161
flocculation technologies also face lower biomass recovery, typically 1-20 % lower
162
compared to other harvesting methods.43 In some cases, negative effects can be
163
observed in product quality.40 Harvesting microalgae via aqueous ammonia hardly
164
affected the metabolites content distribution. The liquid fraction may be re-used as
165
nutrient feed for algae cultivation.44 Aggregation induced by micro-organisms avoids the
166
use of chemical flocculants.45,46 However, relatively large inoculant sizes (30:1) were
167
needed and flocculation was rather slow. Powell and Hill accelerated the BF process
168
drastically and reduced the bacteria cell:algae cell ratio to 1:1.47
169
Direct filtration, cross-flow filtration or combinations with inverse osmosis were also
170
demonstrated to recover algae aggregates efficiently.48-50 NAABB researchers
171
assembled a thin porous nickel-alloy metal-sheet membrane in a cross-flow module for
172
dewatering microalgae cultures up to 24 % solids.51 Filter pore sizes need to be
173
carefully designed in function of the aggregation rate, as smaller cells (< 10 µm) are not
174
recovered and small pores lead to filter blocking. Recently, Global Algae Innovations
ACS Paragon Plus Environment
9
Environmental Science & Technology
Page 10 of 62
175
(Hawaii) developed an advanced membrane filtration system for combined harvesting
176
and dewatering without using flocculants, demonstrated at large scales (20 m3 h-1) with
177
an energy use ca. 0.04 kWh m-3 and 100 % harvest efficiency.28 Another elegant way to
178
facilitate membrane filtration is to ´pelletize´ microalgae in fungi-algae complexes (2-5
179
mm), though the process depended on glucose addition.52 Electrolytic flocculation
180
through release of metal ions from a sacrificial anode is another alternative.53 In 2009,
181
Originoil (USA) announced Live ExtractionTM, a technology which extracts oil from algae
182
on a frequent basis based on the balance of living and dead algae cells using
183
electromagnetic pulses.54
184
Despite the development of novel harvesting and dewatering technologies, only few
185
works evaluated their cost-effectiveness and in particular combinations of them. This is
186
important as probably not just one harvesting or dewatering technology may be the
187
most suitable candidate but rather a combination of them, depending on biomass
188
composition and downstream processes. Recently, Fasaei et al. (2018) described the
189
effect on the energy use and costs associated with sequential combinations of various
190
harvesting and dewatering operations,19 as illustrated in Figure S2. Low-energy
191
combinations were chemical flocculation, either cationic (CAF) or chitosan (CHF)
192
mediated, followed by centrifugation or pressure filtration. Different effects were
193
observed from the cell culture density and feed rate in ORP, TPBR and FPFBR. CAF
194
showed higher costs as higher flocculant dosage is required compared to CHF.
195
2.3.
196
For the production of lipid derived biofuels and chemicals, first oil or biocrude needs to
197
be extracted or produced from algal biomass. Figure 2 compares the outcome of recent
Algal oil/biocrude production
ACS Paragon Plus Environment
10
Page 11 of 62
Environmental Science & Technology
198 199
Figure 2. MFSP of algal lipid oil/biocrude in TEA scenarios 1-7.
ACS Paragon Plus Environment
11
Environmental Science & Technology
Page 12 of 62
200
TEA studies on the production cost of algal oil or biocrude, obtained either via dry or wet
201
solid extraction (DSE or WSE) or via hydrothermal liquefaction (HTL), respectively. The
202
MFSP varied typically between 2 and 7 USD L-1 oil, still considerably higher than fossil
203
derived crude oil and soya oil. Given the high amount of variables in algae strains,
204
cultivation and harvesting methods, conversion techniques and co-product valorizations,
205
it is no surprise that one finds considerable discrepancies in the results reported. Some
206
uncertainity contributors in the models are even not related to cultivation and refining
207
(e.g. market price, risk tolerance, capital finance, etc.). Beal et al. analysed an
208
interesting set of scenarios for hybrid PBR-ORP cultivars (Figure 2, scenarios 4a-4h)
209
with various combinations of harvesting, nutrient feeding, conversion pathways and co-
210
product valorizations based on 100 ha data obtained during 1 year in Texas and Hawaii
211
facilities.58 In the OpenAlgae process, lipid oil is produced via WSE and the solid is
212
valorized as animal feed. The Valicor process is similar to the OpenAlgae process, but
213
the residual aqueous stream is also converted to combined heat and power (CHP) via
214
catalytic hydrothermal gasification (CHG). In the HTL process, biocrude is produced and
215
both residual solids and aqueous streams are used for CHP. The advantage of
216
including solids is that their residues after CHG are recycled to decrease the chemical
217
nutrient requierements (at least for nitrogen). HTL is also the most favorable conversion
218
process from the energetic point of view, as the dewatering step is minimized. The U.S.
219
Department of Energy set the 2018 HTL productivity goal for algal biofuels at 3.8 L m-2
220
year-1 biocrude (33 g m-2 day-1 productiviy and 35 % conversion). Interestingly, the
221
lowest MFSP values were reached when considering wind energy to reduce the share
222
of grid electricity. In fact, the use of wind and solar energy has been considered in only
ACS Paragon Plus Environment
12
Page 13 of 62
Environmental Science & Technology
223
few TEA scensaios. Pearce et al. considered solar powered thermal processing (CSP,
224
scenario 5),59 using a 100 m parabolic trough integrated succesfully with a HTL reactor,
225
which works more efficiently compared to the classic set-up for parabolic troughs in grid
226
electricity generation, as the use of heat transfer fluids, counter current heat
227
exchangers, fluid transfer interconnectivity and electrical power control systems is
228
minimal. They reported a competitive biocrude production cost of 1.37 USD L-1.
229
2.4.
230
Once algal oil or biocrude is obtained, it can be converted to biofuels. Whereas
231
conversion to fatty acid methyl esters (FAME) is an already established route, more
232
recent research focused on the conversion to renewable diesel (RD) via hydrotreating
233
(HT). One motivation for this shift is that the distribution pattern of the fatty acid chain
234
length and insaturation degree in microalgae is not optimal compared to oleo-rich
235
crops,61 affecting the physico-chemical properties of FAME mixtures intented for
236
combustion use in vehicles. Other motivations for this shift include the high costs
237
associated with algal biomass drying:32 1) FAME production from wet algae slurries is
238
only possible via wet conversion technologies whereas RD is produced from wet algae
239
slurries via WSE or HTL, 2) promotion of lipid productivity is of primordial importance in
240
FAME production whereas in RD production proteins and carbohydrates also contribute
241
in the total fuel yield. Figure 3 shows the outcome of recent TEA studies on the
242
production of algal derived RD, produced either via WSE (scenarios 1 and 6) or via HTL
243
(scenarios 2-5 and 7-9). The MFSP results are in the range of competitiveness
244
compared to those of RD obtained via pyrolysis (scenario 10) and those of advanced
245
FAME production (integration with bioethanol production, either via fermentation of the
Algal biofuel production
ACS Paragon Plus Environment
13
Environmental Science & Technology
Page 14 of 62
246 247
Figure 3. MFSP of algal RD (scenarios 1-10) and FAME (scenario 11).
ACS Paragon Plus Environment
14
Page 15 of 62
Environmental Science & Technology
248
whole algae slurry (scenario 11a) or after solid-liquid separation (scenario 11b)). The
249
production costs of wood pyrolysis and Fischer-Tropsch corn derived RD are also
250
displayed for comparison,62 showing that micro-algae are currently less cost-
251
competitive. Lipid extracted algal biomass (LEA) in contrast, was valorized at much
252
lower cost by Ou et al. (30-140 USD ton-1),63 resulting in HTL derived RD at competitive
253
prices (scenarios 4a-4c). The oil was hydrotreated in a two-stage process at 200 and
254
400 °C resulting in RD containing 51 % cycloalkanes, as the LEA was enriched in
255
proteins and carbohydrates and depleted in fatty acids. The RD product composition,
256
important in view of application in combustion engines, is an aspect which is not
257
accounted for in most TEA studies. Zhu et al. (2015) compared fresh - and seawater
258
microalgae as feedstock for HTL biocrude production (scenarios 5a-5d), containing 4
259
and 16 wt% lipids (ash-free basis), and 8 and 22 wt% ashes, respectively.64 This
260
resulted in higher biocrude and RD yield for seawater algae (whereas more naphtha as
261
co-product was produced from freshwater algae). Seawater microalgae are appealing
262
for large scale biofuel production, as freshwater consumption can be reduced drastically
263
and fuel yields are generally higher, but their high ash content affects the overall
264
process economy. Hoffman compared RD produced from ATS and ORP cultivars
265
(scenarios 7a-7b).33 Although the algal biomass production cost was lower in the ATS
266
model (Figure 1, scenarios 4a-4b), this was not the case for the RD production cost,
267
mainly due to the high ash content and low lipid content. Juneja and Murthy presented a
268
TEA analysis of RD production via HTL using CO2 supply from a PP at 4.5 km distance
269
and WW from a facility located at 3 km distance (scenarios 9a-9g).14 The nitrogen
270
utilization degree (0.08-0.12 g L-1) from the WW had high impact on the MFSP of RD, in
ACS Paragon Plus Environment
15
Environmental Science & Technology
Page 16 of 62
271
the range of the effect of the lipid content (15-35 wt%), followed by the scale of the WW
272
facility, diesel yield and algae concentration at harvest.
273
The results in Figures 1-3 show, at least in equicomparable conditions, the
274
importance of reaching higher biomass productivities (g m2 day or g L-1 day-1). The
275
productivity as key parameter to attain feasible biorefinery scenarios was previously
276
highlighted as one of the main conclusions in various studies.56-58,61 Productivity
277
improvements require efforts in microalgae based biotechnology, e.g. via the
278
development of genetically modified species.28 Another strategy to increase the
279
productivity is the cultivation of microalgae in co-cultures, either with other algae
280
species or with fungi, yeasts or bacteria. Gomez et al. used genome-based metabolic
281
network modelling to demonstrate this in large scale open pond cultivars.67 First, they
282
modelled single algae and single oleaginous yeast cultivation in flue gas enriched
283
medium. Next, an algal-fungal ORP with a feed of cellulosic glucose and oleaginous
284
yeast was considered, which consumed glucose/xylose mixtures resulting from
285
lignocellulose hydrolysis waste. Co-cultures of algae and yeast produced FAME at
286
competitive prices, ca. 2.0 USD L-1 for pure cellulosic glucose and 1.4 USD L-1 for
287
lignocellulosic glucose/xylose, whereas the algae monoculture gave similar results only
288
at very short distances from the flue gas source. Oleaginous yeasts such as
289
Cryptococcus albidus, Rhodotorula glutinis and Yarrowia lipolytica are attractive for
290
biofuel production as they can convert lignocellulosic sugars into lipids, accumulating up
291
to 36-72 %.68 These cultivation systems could be applied in the vicinity of PP, but
292
optimization is required as most oleaginous yeasts are not extremophiles. The
293
importance of these findings is the fact that the introduction of yeast or fungi enables
ACS Paragon Plus Environment
16
Page 17 of 62
Environmental Science & Technology
294
lignocellulosic (waste) materials to be digested and to become metabolized by
295
microalgae, which are otherwise not available for assimilation in single algae cultures.
296
This cultivation strategy enables the partial transformation of these carbon sources into
297
algae fixed CO2 . At the same time, the yeast or fungi can benefit from the O2 produced
298
by algae and increase their lipid production. In addition, microbial communities are
299
better protected against microbial invasion.68
300
2.5
301
Cost breakdown analysis is often divided in fixed capital costs and operational costs, as
302
illustrated in Figure S3 for various algal biofuel production scenarios. Doshi et al. (2017)
303
analysed the financial investment for a 250 ha FAME production plant consisting of 175
304
ha ORP cultivars, fed with WW and CO2 refined from flue gas, supplemented by urea
305
and diammonium phosphate as fertilizers (based on nutrient availability in WW
306
medium).69 An important detail in the study was that the cost of flue gas refining was
307
assumed to be fully covered by the waste producers. Pond construction and installation
308
costs represented the highest capital investment (34 %), whereas the sum of
309
maintenance, supplies and insurance costs dominated (91 %) the total operational cost.
310
The present value depended on the revenues from FAME (1.50 USD L-1) as the main
311
product and glycerol (1.52 USD L-1), fertilizer (12.0 USD kg-1) and animal feed (12.0
312
USD kg-1) as the co-products. The results demonstrated that valorization of the LEA
313
residue was essential for the financial feasibility (NPV > 0). Maximizing FAME yields in
314
compromise with lower LEA yields for animal feed lead to a negative NPV. Batan et al.
315
reported the capital and operational costs for a PBR cultivar intended for RD production
316
via WSE followed by HT.60 Surprisingly, the harvesting costs were estimated much
Cost Breakdown Analysis
ACS Paragon Plus Environment
17
Environmental Science & Technology
Page 18 of 62
317
higher than those reported by Doshi et al (ORP),69 despite no use of flocculant was
318
reported and despite exhibiting higher biomass concentrations at harvest. Although
319
higher capital investment was required to purchase PBR, the installation cost and
320
working capital was considerably lower compared to ORP. Hoffman contrasted the cost
321
analysis of ATS against ORP cultivars intented for RD production via HTL and HT.33
322
The total capital investment was similar whereas the operational cost was drastically
323
lower for ATS cultivars, as it was assumed that all nutrients were provided from WW
324
streams (without credits for removing N and P) and that CO2 was provided by a nearby
325
source of flue gas. Flocculants were not required for dewatering of ATS cultures (algae
326
can be harvested at concentrations up to 200 g L-1) in contrast with ORP cultures
327
(harvested at 0.5 g L-1). Recently some hybrid PBR-ORP cultivars were analysed, in
328
which algal strains are inoculated in PBR followed by large scale growth in ORP.70 The
329
hybrid system showed attractive capital investment requirements. Capital costs of 269,
330
83 and 101 million USD year-1 for PBR, ORP and hybrid PBR-ORP, respectively (0.7-
331
108 dry ton year-1). The effects on the operational costs were similar.
332
2.6 Sensitivity Analysis
333
Sensitivity analysis is an important tool in TEA, as it indicates more clearly the fields that
334
must be improved in the road to commercial algae production systems. It shows how a
335
certain output value (MFSP, NPV, t-values, etc.) varies with a changing input parameter
336
in the calculation model (Excel, AspenPlus, FARM, etc.), including a baseline case, a
337
lower case and an upper limit case, in the form of probability curves, histograms, etc.
338
Bravo-Fritz et al. (2016) considered an interesting set of biorefinery scenarios and
339
compared them between Isochrysis sp. and Tetraselmis sp. cultivars at medium and
ACS Paragon Plus Environment
18
Page 19 of 62
Environmental Science & Technology
340
large scale sizes.70 All the scenarios (Figure S4) resulted in negative NPV, except for
341
protein extraction (albeit it had the worst energy balance evaluation). The most
342
promising scenarios included: a) drying + ball-milling + lipid/debris separation, b) WSE
343
and c) WSE + anaerobic digestion (AD). The effect on MFSP of the assessment context
344
(moderate, intermediate and optimistic) and the scale were actually more significant
345
than the biorefinery scenario itself. Only with Isochrysis sp. in the optimistic scenario
346
and at large scale competitive production costs (MFSP) were achieved ca. 1 USD L-1.
347
Here is the point where TEA results start to get speculative; data on larger scale are
348
required to confirm the data used from small scale. One succesful example of this was
349
reported by Wen et al. (2016) on the up-scaling of Chlorophyta cultivars from pilot scale
350
(0.01 m3 reactor) to outdoor (40 m3 ponds), in which both the biomass productivity and
351
lipid content remained stable.72
352
Whereas sensitivity analysis of single product scenarios (e.g. biodiesel) indicates that
353
higher lipid contents will lead to lower MFSP, the behavior is different in multi product
354
scenarios.69 Therefore, sensibility studies which evaluate on a NPV basis are more
355
appropiate, rather than evaluation of the production cost only (MFSP), because a better
356
valorization of residual process streams can improve the total revenue value.
357
Importantly, in a multi product scenario of biodiesel, glycerin, animal feed and fertilizer,
358
it was found that a lower biodiesel price was off set by sales of high-value feed and
359
fertilizer and hence the feasibility range based on realistic potential prices for
360
commercial diesel fuel was hardly affected. In other words, the key for biofuels to
361
become price competitive (not cost competitive) is a better valorization of the co-
ACS Paragon Plus Environment
19
Environmental Science & Technology
Page 20 of 62
362
products. This was also one of the main conclusions of a very recent review on
363
microalgae based biorefinery concepts.72
364
In sensitivity analysis, the input parameters are based on results from the literature
365
which in turn are based on past events or past interpretations of future outcomes. In this
366
sense, switch-value (SV) analysis is more appropiate to compare the financial
367
feasability of biorefinery scenarios in function of a certain input parameter. The
368
parameter values are calculated at which NPV values turn to zero. In other words, SV
369
values describe how close the parameter set for the baseline scenario corresponds with
370
NPV = 0 situations. Doshi et al. (2017) calculated for a multiproduct scenario (biodiesel,
371
glycerol, animal feed and fertilizer) SV values of 19.6 g m-2 day-1 (biomass growth rate),
372
40 % lipids (dry content), 11.8 USD kg-1 (both fertilizer and animal feed price), 41 % use
373
of biomass allocated for biodiesel production, 19.5 years (operation period) and 97 %
374
use of the LEA residue.69 In the sensitivity analysis, lipid contents higher than the
375
baseline case (40 %) resulted in negative NPV values, showing that further
376
improvements in lipid extraction and transesterification are still highly desired before
377
increasing the biomass proportion allocated for biodiesel. By improving the cost-
378
efficiency of these proceses with 20 % (via reduced capital investment and maintenance
379
costs), the pay-back period was reduced from 20 to 12.3 years. TEA clusters that
380
explore fast and efficient new scenarios based on novel product and technological
381
developments are highly desired, as recently addressed by an expanded biorefinery
382
superstructure proposed by Rizwan et al., including the processing of microalgae
383
residues and solvent recycling.73 The model (Figure S5) was developed for C. vulgaris,
384
but it can easily be extended to other species.
ACS Paragon Plus Environment
20
Page 21 of 62
Environmental Science & Technology
385
2.7.
386
Market analysis is an essential part of TEA analysis and should be thoroughly
387
conducted, as it defines the potential market niches, values and volumes. Microalgae
388
derived products find their market majorly in 4 sectors: (i) bio-energy and renewable
389
bulk chemicals, (ii) agricultural products (biopesticides and biofertilizers), (iii) animal
390
feed (supplements) and (iv) human use (food, nutraceuticals and cosmetics). Algal
391
biomass is considered as a suitable feedstock, but the reality is that industrial
392
applications are related to almost exclusively human consumption and animal feed.74 In
393
the bioenergy sector, the production of biofuels requires large scale algal biomass
394
production (ca. 107 tons year-1), which is way too far from the actual global production
395
volume (104 tons year-1). This production scenario also falls short compared to the
396
production required for agricultural (105 tons year-1) and animal feed (106 tons year-1)
397
and only meets the requirements for human applications (104 tons year-1). A market
398
analysis for different microalgae derived products is presented in Figure S6. To be
399
economically feasible NPV must be positive, but only products for human consumption
400
and animal feed have market values higher than the production cost. High added-value
401
products include animal feed products which are often protein enriched, while products
402
for human consumption are usually obtained from polyunsaturated fatty acids (PUFAs)
403
in lipid fractions and secondary metabolites (i.e. extractives). It is estimated that the
404
market value of carotenoids would reach 1000 million US$ by 2020. Commercially
405
produced astanxanthin from microlalgae has a market value of 15,000 USD kg-1.
406
2.8
Market analysis
High Added-Value Chemicals
ACS Paragon Plus Environment
21
Environmental Science & Technology
Page 22 of 62
407
Large scale cultivation plants for the production of biofuels (as described in sections
408
2.1-2.5) do not have the same cost distribution, revenue and profitability compared to
409
small-scale specilalized cultivars for the production of high added-value chemicals, as
410
illustrated in a comparison between algal FAME and β-carotene production plants
411
(Table S1). Although the market volumes of secondary metabolites are very low
412
compared to bulk chemicals and biofuels, their value is much higher, as illustrated in
413
Table S2 for astaxanthin, lutein, β-carotene and phycocyanins. Ruiz et al. designed
414
specific biorefinery process chains for the production of pigments in function of different
415
market scenarios (cosmetics, healthcare, food and natural/synthetic pigments), e.g. for
416
the production of omega-3 fatty acid and astaxanthin.27 Based on a realistic cost and
417
market analysis, the authors demonstrated a higher profitability for cosmetic and food
418
related products with better projections for the near future, compared to the production
419
of bulk chemicals and in particular biofuels. Other examples of commercial speciality
420
products from microalgae are PUFAs,75 natural (fluorescent) dyes76 and stable isotope
421
chemicals for research and pharmaceuticals.77 Biofuels in contrast have a relatively low
422
commercial value and need to be produced at large scale or need a better co-product
423
valorization to become cost and price competitive. These findings has partially moved
424
the
425
products.5,21,27,74,75 This shift has also been stimulated by the fall of oil prices.5
interest
in
algae
based
research
from
biofuels
to
high
added-value
426
Despite various improvements, the selective extraction of valuable compounds
427
remains a key challenge.27 The highest costs are attrituted to biomass drying and cell
428
disruption (e.g. bead-milling, 1 kWh kg-1 ~ 0.17 USD kg-1 for 95 % disruption). The use
429
of pulsed electric fields may drop the energy use to 0.06 kWh kg-1 for 70 % cell
ACS Paragon Plus Environment
22
Page 23 of 62
Environmental Science & Technology
430
disruption.78 A lot of energy is also put in solvent extraction and recovery. It was
431
estimated that the use of heat for biomass drying, lipid extraction and solvent recovery
432
reaches 0.21 USD kg-1. Supercritical fluids and switcheable solvent systems are
433
attractive alternatives to traditional solvents. Aqueous ammonia extraction, in similiarity
434
with the AFEX process,79 or anhydrous liquid ammonia,79,80 is also an option as
435
ammonia can be recycled efficiently. Ammonia residue streams could be recycled to the
436
algae nutrient feeding.44
437
3. ENVIRONMENTAL IMPACT
438
Most of the environmental impact studies related to microalgae biorefinery scenarios
439
are conducted and evaluated via Life Cycle Analysis (LCA) of carbon, energy, water
440
and nutrients. The most frequently used environmental sustainability indicators are net
441
energy ratio (NER), greenhouse gas (GHG) emissions and water footprint (WF). Similar
442
to the data from TEA studies, progress is highly desired in further collecting data from
443
pilot plants to estimate better productivity data for large scale plants, and to contrast
444
them with the current available data from large plants.81
445
3.1 Net Energy Ratio and Greenhouse Gas Emissions
446
GHG emissions produced during the life cycle of algal biofuels are reported as CO2
447
equivalents (g CO2eq) by combining CO2, CH4 and N2O emissions scaled by their global
448
warming potentials. NER indicates the ratio of energy demand (from cultivation to final
449
production stage) to energy content of the biofuel. Some works consider only the well to
450
pump cycle (WTP: feedstock terminal and retail station), while others also consider the
451
pump to wheels cycle (PTW: CO2, CH4 and N2O emissions associated with biofuel
ACS Paragon Plus Environment
23
Environmental Science & Technology
Page 24 of 62
452
combustion). Well to wheels (WTW, also ´cradle to grave´) results consider the entire
453
biofuel life cycle. Emission data on the combustion of biofuels in engines are still lacking
454
and often the value for low-sulfur diesel is used instead. A substantial amount of the
455
reports in literature used the GREET model (Greenhouse Gases Regulated Emissions
456
and Energy Use in Transportation). This model is updated regularly and can be
457
downloaded as an excel file.82 While most LCA studies on microalgae derived biofuel
458
production reported promising results, others did not.83-87 Clarens et al. (2010)
459
illustrated that life cycle impacts of algae cultivation are sensitive to several input
460
parameters, some of which are still overlooked.88 Collet et al. (2014) reported
461
recommendations for LCA studies on algal biofuels to harmonize results in order to
462
improve their validity.89 Improvements could be made in the life cycle inventory (LCI)
463
and the functional unit itself. At the LCI level, special attention should be paid to the
464
perimeter of the study (e.g. inclusion of infrastructures) and to the valorization of co-
465
products.
466
3.1.1 Algal Oil/Biocrude and FAME
467
Figure 4 shows the high impact scenario variables and the outcome of recent LCA
468
studies on the production of FAME (via transesterification of lipid oil), algal oil (via
469
DSE/WSE) and biocrude (via HTL). NER and GHG emissions for fossil derived low-
470
sulfur diesel are shown for comparison, as well as the GHG reduction thresholds for
471
2018 set by the European Directive on Renewable Energy in 2009.97 The general trend
472
for FAME showed a less favorable energy balance (higher NER) and higher GHG
473
emissions, with exception of some scenarios. Note that equal biomass productivities
474
and FAME yields can result in different NER and GHG emissions, depending on the
ACS Paragon Plus Environment
24
Page 25 of 62
Environmental Science & Technology
475 476
Figure 4. Net energy ratios (NER) and greenhouse gas (GHG) emissions associated with
477
the production of algal derived lipid oil (green), biocrude (blue) and FAME (red).
ACS Paragon Plus Environment
25
Environmental Science & Technology
Page 26 of 62
478
carbohydrate and protein contents (co-product valorization). An important part of the
479
energy and emission balance is related to drying requirements of algal biomass.
480
Whereas HTL requires minimal drying, DSE requires important amounts of energy. DSE
481
scenarios can be improved by integrating heat recovery with the drying process, as
482
illustrated by Zaimes and Khanna (2013) in scenarios 2a-2b, still the WSE method
483
showed better results (scenario 2c).91 Quinn et al.
484
(scenarios 3a-3d), despite having superior extraction performance compared to hexane,
485
was not as favorable as expected.92 This was mainly because it was supposed that CO2
486
extraction required dry conditions. Soh et al. (2014) conducted LCA studies based on
487
lab-scale (0.5 L) data from 2 freshwater (N. oleoabundans and C. sorokiniana) and 2
488
marine (N. oculata and T. suecica) microalgal species, both with nitrogen deprivation
489
and repletion (scenarios 4a-4h).93 Higher lipid productivity did not lead to lower NER
490
and lower GHG emissions in all cases, because AD also has favorable impacts on
491
these indicators (as drying is not required for AD). Still, considerable uncertainty exists
492
on this effect as the CH4 yields from LEA are poorly described in the literature.83
493
Ponnusamy et al. (2014) compared hexane extraction in near dry conditions with
494
subcritical water extraction, as a variant to HTL.94 The total energy requirements for
495
subcritical water extraction were estimated similar to those for hexane extraction and
496
recovery (33 MJ kg-1 FAME). For the base case (scenario 5a) they assumed 50 % heat
497
exchanger efficiency and 60 % in the optimized case (scenario 5b), whereas 85-90 %
498
was used in previous literature.
(2014)
showed that supercritical CO2
499
The use of external fossil energy is mainly governed by the electricity demand in the
500
cultivation stage for mixing, pumping and injecting gas and can vary widely with
ACS Paragon Plus Environment
26
Page 27 of 62
Environmental Science & Technology
501
considerable effects on both NER and GHG emissions.98,99 It was determined that in the
502
case of Nannochloropsis sp. ORP cultivars, a possible reduction of 70 % of the
503
electricity consumption at the cultivation stage would reduce the GHG emissions with
504
ca. 42 % (resulting in an emission of 0.85 kg CO2eq) and decrease NER to values below
505
1.99 In classic ORP cultivars the energy consumption can vary between 0.24-1.12 W m-2
506
or more specifically between 3.7-5.7 kWh per kg algal oil.5,99 The reason for this
507
variation is that the main parameter to be optimized during cultivation is the productivity,
508
more than the energy consumption. Microalgae need proper mixing to avoid
509
photoinhibition and photolimitation and to attain high photosynthetic efficiency, for
510
instance by keeping high flow velocities and turbulence levels. Chiaramonti et al. (2013)
511
showed how redesign of raceway ponds can optimize the energy consumption without
512
compromising productivity.100 Another strategy to reduce the input of fossil energy is to
513
increase the share with renewable energy. LCA studies which included renewable
514
electricity as an alternative to grid electricity are rather scarce. Note that in real life
515
situations a photovoltaic energy panel has larger PE compared to most microalgae; the
516
advantage of microalgae is that excess energy can be stored efficiently. Another
517
advantage is that energy consumed on site only has minor transport and distribution
518
losses. Collet et al. (2014) demonstrated how wind turbines and photovoltaic panels
519
could be integrated on site to provide the electricity demand of an 80 ha ORP cultivar.89
520
At 20 g m-2 day-1 algal productivity, the NER and GHG emissions were reduced with 18
521
and 21 %, respectively. They demonstrated that the impact of the electricity source on
522
GHG emissions corresponds with the same effect as increasing the algal productivity
523
from 10 to 30 g m-2 day-1. This three-fold increase in productivity would require
ACS Paragon Plus Environment
27
Environmental Science & Technology
Page 28 of 62
524
biochemical and technical developments on the long-term, while installing wind turbines
525
and solar panels is more straightforward at short-term. Positive effects of wind energy
526
on energy balances were also demonstrated by Beal et al. (2015) in scenarios 10e, 10g
527
and 10i.58
528
Effects from the nutrient source were also studied. Woertz and co-workers conducted
529
an LCA study on the production of algal biodiesel, in which CO2 and WW were
530
considered as inputs for cultivation (scenario 7).83 The energy demand for CO2 supply
531
and distribution was ca. 17 % of the total demand (1.05×107 MJ year-1). Based on
532
detailed mass and energy balances, calculated GHG emissions were 70 % lower than
533
those of conventional diesel fuel, meeting the minimum 50 % reduction requirements
534
set by EPARFS2 and even below the GHG reduction threshold for 2018 set by the
535
European Directive on Renewable Energy.97 GHG emissions from algal biodiesel were
536
estimated at 29 g CO2eq MJ-1, beneath the level for low-sulfur diesel and biodiesel from
537
soya bean (83 g CO2eq MJ-1), at least when taking into consideration also the indirect
538
land use changes. The lower oil content (10 %) implies low biodiesel but high LEA yield
539
(LEA was used for the generation of electricity via AD). This case resulted in GHG
540
emissions as low as to 3 g CO2eq MJ-1, showing again the prominent role of the
541
electricity demand in the GHG emission indicator. The energy balance (NER) in turn
542
was high (2.2 MJ per MJ-1 FAME). The authors also quantified the increase in emissions
543
associated with the use of chemical fertilizers. Having a manufacturing GHG emission
544
factor of 3 g CO2eq g-1 nitrogen, emissions increased with 6 % with respect to the 89 %
545
N recycle case represented in scenario 7, requiring a fertilizer input of 116,250 kg
546
nitrogen year-1.
ACS Paragon Plus Environment
28
Page 29 of 62
Environmental Science & Technology
547
3.1.2 Algal Renewable Diesel (RD)
548
Figure 5 shows the NER and GHG emissions associated with the production of algal
549
derived biofuels. The general trend is that the results do not vary a lot whether
550
producing FAME or RD. This was confirmed by Zaimes and Khanna (2010) (scenarios
551
2a-2c in Figure 4 compared to scenarios 4a-4c in Figure 5).91 The impact of the
552
scenario prior to the final conversion step was higher. The results showed that HTL
553
would be the preferred pathway rather than lipid extraction or pyrolysis, at least from an
554
LCA point of view. Frank et al. (2011; 2013) compared RD production obtained either
555
via lipid extraction (scenario 3a) or via HTL (scenario 3b), both followed by HT.90,103 Key
556
variables were the biocrude yield and nitrogen content, along with the hydrogen
557
demand for HT. They concluded that too high HTL yields impedes the valorization of the
558
solid LEA residue via AD (too low C:N ratios). Instead, catalytic hydrothermal
559
gasification (CHG) of LEA to biogas and ammonia was used for the production of CHP
560
in the HTL route. Despite the fact that HTL requires high pressure and temperature, the
561
direct energy use was higher for the WSE route as pressure-homogenization was
562
required in the latter (high electricity demand). The HTL route required ca. 2 times less
563
algal biomass to reach similar RD yields compared to the WSE route. Still, WSE
564
resulted in considerably lower CHG emissions, because after nutrient recycling (NR)
565
from the residual aqueous phase up to 5 times less ammonia and 1.5 times less
566
phosphorus were required additionally, whereas in the HTL process an important
567
amount of nitrogen ends up in the biocrude (5.7 wt% N compared to 0.2 wt% N in WSE
568
lipid oil). The lower GHG emissions in the WSE route were also the result from AD (low
569
heat demand + electricity generation). The scenarios 2a-2b (WSE route) and 12a-12b
ACS Paragon Plus Environment
29
Environmental Science & Technology
Page 30 of 62
570 571
Figure 5. NER and GHG emissions associated with the production of algal derived RD
572
production, obtained after hydrotreating of extracted lipid oil (green), HTL biocrude (blue)
573
and pyrolysis oil (red). Gaseous fuels (black) are shown for comparison.
ACS Paragon Plus Environment
30
Page 31 of 62
Environmental Science & Technology
574
(pyrolysis route) showed high NER and GHG emissions, as in both belt drying was
575
used.102 The effect of drying is also observed by comparing the results in scenarios 1a-
576
1b (for WSE only dewatering required) compared to scenarios 10a-10d (dewatering +
577
thermal drying required for intake in pyrolysis unit). Another example of the impact from
578
drying activities is shown in the scenarios 7a-7b (HTL, minimal dewatering) and
579
scenarios 11a-11b (pyrolysis, dewatering + thermal drying).105
580
By using flue gas as carbon source significant reductions in GHG emissions can be
581
achieved.55,106,107 Rickman et al. (2013) conducted an LCA study on utility-connected
582
systems to evaluate the feasibility of integrating algae cultivars in PP for CO2
583
biosequestration.108 As considerable energy requirements were associated with
584
pumping of large gas and fluid volumes, the authors pointed out the need of integrated
585
systems which effectively can reduce CO2 emissions. The costs and credits associated
586
with the processing of flue gas is not fully clear in the current literature, some do take
587
these into account and others not. Recently, Laurens (2017) also claimed the urgent
588
need for more detailed studies on how microalgae cultivars could be integrated within or
589
close to existing industrial facilities,5 including PP, natural gas plants, bioethanol and
590
ammonia plants, each of them having different CO2 purities and supply costs.109
591
3.2. Water Footprint
592
The water footprint (WF) is the total freshwater quantity embedded in a production
593
scenario, including ground and surface water (blue WF) and rain water (green WF). This
594
indicator is important, particularly in regions that experience water shortage and
595
aridification risks. The WF depends on the local climate and the actual process
596
design.110 Estimation of the WF is a complex task as it is highly sensitive to evaporation
597
rates and hydraulic retention times. Yang et al. (2011) reported 3727 kg water per dry
ACS Paragon Plus Environment
31
Environmental Science & Technology
Page 32 of 62
598
kg algal biomass.111 A better comparison is based on the water quantity embedded
599
against the energy content of the biofuel produced. WF between 1-62 L water per MJ−1
600
of energy produced were reported.87,112,113 By recirculating harvest water the WF was
601
reduced by 84 % and by using sea water it was further reduced to 90 %. However,
602
using seawater has indirect effects on MFSP, NER and GHG, as the presence of salt is
603
considered as ´dead´ mass to be processed. In comparison, the WF of lignocellulosic
604
bioethanol, corn bioethanol and soya biodiesel were estimated at 11-171, 1-18, 2-91 L
605
MJ-1.113,114 Data from pilot-scale reactors (ORP and PBR) operated in 3 different
606
seasons (summer, fall and winter) were considered by Pérez-López et al. to evaluate
607
the environmental burdens.115 The energy use for temperature regulation contributed
608
significantly. The production of the high added-value phycocyanin was reported by
609
Papadeki et al., including associated environmental impacts to evaluate the
610
sustainability of the extraction process.116 The recovery of this bioactive compound was
611
highly dependent on the amount of biomass, consumables and energy supplied.
612
Advanced extraction processes such as ultrasound assisted extraction were
613
recommended to decrease the environmental impact.
614
The impact on the water usage from large-scale cultivation of microalgae is still on
615
debate. Introduction of large water volumes at high temperature may have effects on
616
the evaporation rate, especially in arid regions. Increasing the reutilization of harvest
617
water and the adaption towards seawater input are research areas which deserve
618
further attention.117 The recovery of nutrients from harvest water, which otherwise also
619
would be an environmental burden, also reduces the WF.115 The high impact of
620
freshwater availability in the USA on the algae cultivar location was recently
ACS Paragon Plus Environment
32
Page 33 of 62
Environmental Science & Technology
621
demonstrated by Venteris et al.119 Important in the decision taking is the actual salinity
622
of the freshwater source, which should vary close to the salinity of the cultivars to
623
reduce the amount of make-up water. Prospects are therefore strain dependent. The
624
cultivation of microalgae in the vicinity of thermal PP is attractive, not only for CO2
625
biosequestration but also because PP consume large amounts of cooling water, as
626
recently quantified for China.120 The cooling water could be re-utilized for microalgae
627
cultivation and the WW could be treated to use again as cooling water, closing the water
628
cycle.
629
3.3 Toxicity and Biodiversity in Aquatic Ecosystems
630
The water quality and consumption are important sustainability indicators of aquatic
631
cultivation systems. They depend on the algal strains used and on the microbial
632
ecology. Many algae species can be grown in low-grade WW to levy pressure on
633
natural freshwater resources.121-123 By doing so, alongside WW remediation credits, it is
634
also possible to procure water and nutrients at lower cost for cultivation at large scale. A
635
wide range of pollutants can be assimilated by microalgae including carbon, NOx, SOx
636
and heavy metals.4 Microalgae can use both organic and inorganic C, N (in the form of
637
ammonium, nitrate or nitrite) and P. Elevated levels may trigger negative impacts such
638
as algal blooms and oxygen depletion during nights (due to decomposition of dead
639
algae).124 Eutrophication due to accidental release of culture media into the environment
640
is a potential risk for the ecologic biodiversity.125,126 The bioremediation of polluted water
641
streams suffering from algal blooms could generate additional biomass which can be
642
used to increase the biofuel production capacity, provided residual N, P and S can be
643
controlled properly. Large-scale cultivation of microalgae can be considered as a
ACS Paragon Plus Environment
33
Environmental Science & Technology
Page 34 of 62
644
“controlled eutrophication” process and needs to be well managed by an adequate
645
nutrient supply and by harvesting at regular intervals.
646
3.4 Wastewater Treatment and Nutrient Recycle
647
Microalgae cultivation can fit in as a secondary treatment unit in traditional WW
648
treatment facilities, with possibilities to obtain effluents within standards set for surface
649
discharge.51 This approach alleviates negative impacts on the aquatic biodiversity and
650
allows to recover valuable nutrients, which favors the overall energy balance and GHG
651
emissions.87,127 The use of WW not only can reduce the chemical fertilizer demand but it
652
can also minimize the resources needed for chemical WW treatment. Several types of
653
wastewater (WW), produced by municipal (MWW), agricultural (AWW) or industrial
654
(IWW) sources, may be used for microalgae cultivation.127-131 Microalgae based
655
research has demonstrated the potential and the challenges in combining WW nutrient
656
removal and biofuel production.123,132-142 The algae growth is strongly affected by the
657
WW composition and even for the same WW source population dynamics exist.140
658
Table S3 in the Supporting Information shows the potential of various microalgae
659
strains in different WW treatments. The results show that especially AWW sources
660
provide higher biomass and lipid productivities, which plays in favor of algal farming in
661
rural areas, though MWW sources in non-rural areas may provide nutrients on a larger
662
and more continuous basis. In animal manure effluents, the N:P ratio is so high that it
663
cannot be remediated by crops only, but too high nutrient concentrations in AWW may
664
require dilution first, otherwise it would reduce light penetration considerably.144 Dilution
665
however has a great impact on nutrient removal efficiency, biomass accumulation and
666
lipid productivity.142,145-148 Research has been carried on primary and secondary treated
667
MWW, essentially in activated sludge plants, as well in municipal centrates obtained
ACS Paragon Plus Environment
34
Page 35 of 62
Environmental Science & Technology
668
from the sludge centrifuge. Municipal centrate has been found as an encouraging
669
growth medium, especially for Chlorella which provided the highest lipid productivity
670
reported.132 Industrial WW contains much lower levels of phosphorous and ammonia,
671
and in some occasions it is enriched with heavy metals, which can affect growth rates.
672
Ruiz-Martinez and co-workers studied the removal of N and P from the effluent of a
673
submerged anaerobic membrane bioreactor.145 They used a lab-scale PBR in which
674
algae were cultured in semi-continuous mode for 42 days, assuring stable pH in the
675
growth medium by adding CO2. Despite the variations in N and P concentrations, the
676
anaerobic effluent resulted to be suitable for growing microalgae, with biomass
677
productivities reaching 0.23 g L-1 day-1 and nutrient removal efficiencies of 67 and 98 %
678
for NH4+ and PO43- at optimized conditions, respectively. Similarly, submerged
679
membrane photobioreactors (MPBR, see Figure S7) were recently reviewed by Luo et
680
al. for microalgae cultivation applied to WW treatment.148 MPBR technology combines
681
conventional PBR with a membrane to allow higher flexibility for WW feed composition
682
and operational conditions. MPBR play an important role in optimization, but the
683
challenge is to avoid fouling which can lead to operational problems. Applying
684
immobilized microalgal technology in MPBRs has the potential to mitigate fouling risks.
685
4. SOCIO-ECONOMIC IMPACT
686
Data available till-date focus on benefits and hurdles related to the economy of the
687
production process itself, rather than on socio-economic concerns.149 Only few reviews
688
on the sustainability of microalgae production systems included socio-economic
689
impacts.25,26,150 Qualitative or semi-quantitative indicators include social well-being and
690
acceptability. Social well-being refers to fulfilment of basic human needs such as food
ACS Paragon Plus Environment
35
Environmental Science & Technology
Page 36 of 62
691
security and employment. Social acceptability includes factors such as public opinion,
692
transparency, effective stakeholders’ participation and waste management risks.
693
Recently a set of more specific socio-economic indicators were proposed by the US
694
Department of Energy:109 food security, employment, ROI, NPV, energy security
695
premium, depletion of non-renewable energy, fuel price volatility, trade volume and
696
terms, effective stakeholder participation, transparency, public opinion, income and
697
works days lost due to injury. The public confidence in the microalgae based industry is
698
hindered by the lack of reliable information, production transparency and by the data
699
heterogeneity on health and environmental issues.151 Aspects of the public opinion
700
include potential for generating new jobs, odours, esthetical aspects, water usage,
701
recent media reports, perception towards potential use of genetically modified algae and
702
already established perceptions such as rise in food prices and deforestation associated
703
with first generation biofuels.152,153 One important benefit of setting up an algae based
704
industry is the projection and creation of new jobs in the farming, refining and supply
705
sector.150-153 Established algae companies have reported considerable numbers of jobs
706
for pilot plants.5,28 Algae based industry and rural development can support each other
707
mutually, as land costs in rural areas are lower and biomass transport costs strongly
708
motivates biofuel processing near the algal cultivars.75,150 Depending on whether the
709
project is local or global, the public acceptability may vary.128 Technologies that are
710
accepted in one region may be rejected in other regions. As the large scale algal
711
biobased industry is not established yet, the public acceptability may vary over time.
712
The competition for the use of arable land is an important aspect, often widely
713
discussed in different social communities. Laurens (2017) proposed to perform
ACS Paragon Plus Environment
36
Page 37 of 62
Environmental Science & Technology
714
Resource Assessment in addition to LCA, quantifying the total amount of product
715
manufactured using a specific process given the amount of input resources (land, water,
716
CO2 and nutrients) available within a specific area.5 These data should indicate how
717
much extra resources should be transported from more distant areas. A study published
718
by Wigmosta et al. (2011) considered the land, water and resource availability in the
719
USA, and concluded that ca. 4.3×107 ha of available land was suitable for algal
720
cultivation open ponds, which corresponded with a potential production of 2.20×1011 L
721
of algal oil per year, equivalent 48 % of the annual petroleum imports in the USA
722
(2011).154 It was estimated that 5.5 % of USA land area would be required in addition to
723
reach these levels of production. The water consumption, however, would exceed 2-3
724
times the current agricultural water needs. The impact of land use can be minimized to
725
a great extent as algae can be cultivated on marginal lands. However, with regard to
726
temperature and light intensity, many areas identified as suitable for algae cultivation
727
are tropical, where the availability of water is limited and evaporation losses are
728
considerable (arid zones). Concerns still exist in the public opinion regarding the use of
729
land for large scale biofuel production.150 Impacts resulting from direct changes (gas flux
730
due to construction of ponds on arable land) and indirect changes (purpose of land used
731
and associated emissions) and the pressure on freshwater availability can be minimized
732
when off-shore cultivation of (macro)algae is implemented. For instance, the
733
“Submariner” research group studied the prospects of associating algae cultivation with
734
an off-shore wind farm in the Baltic sea, with annual algal biomass yields of 1.2 kg per
735
m2 sea surface.155
736
5. CONCLUSIONS AND FUTURE PROSPECTS
ACS Paragon Plus Environment
37
Environmental Science & Technology
Page 38 of 62
737
Microalgae can play an important role in the development of sustainable production
738
systems. Sustainability is the capacity of a process or system to continue while being
739
able to meet the needs of future generations. In practice, the sustainability of
740
microalgae production systems is evaluated based on techno-economic assessment
741
(TEA), life cycle analysis (LCA) and socio-economic impact. Recent TEA studies
742
pointed out that current projections for large scale production of microalgal biofuels are
743
not for the near future, due to their low cost competitiveness as compared to fossil fuels
744
and biofuels from other biomass sources. Although the data are highly heterogeneous
745
in nature (depending on the model assumptions and boundaries), the studies agreed in
746
the fact that biomass productivity was the parameter with the highest impact. The high
747
cost is mainly associated with the high energy demand for algae cultivation, harvesting
748
and drying. Flocculation combined with centrifugation or filtration technology is actually
749
the most cost-effective harvesting method. Conversion methods that directly act on
750
diluted wet algae biomass slurry are highly desired to reduce the effect of drying, such
751
as hydrothermal liquefaction (HTL) and anaerobic digestion (AD). In large scale biofuel
752
production, the financial feasibility of multi product scenarios is improved signifcantly
753
compared to single product scenarios. The unit production costs of high added-value
754
chemicals are much higher, as they are typically produced in non-optimal growth
755
conditions and at smaller scales. But, these costs are countered by a high revenue and
756
therefore their commercial production has better projections for the near future. Still,
757
these compounds have limited market niches and volumes at present. LCA of various
758
algal biofuel production scenarios have shown considerable variations, not only
759
depending on the scenario input parameters but also depending on model assumptions
ACS Paragon Plus Environment
38
Page 39 of 62
Environmental Science & Technology
760
and boundaries. Recent studies have demonstrated the positive effect of the integration
761
of renewable energy technologies within algal cultivars to reduce the greenhouse gas
762
emissions emitted during the life cycle of algal biofuels. Whereas on the long-term algal
763
biotechnology will play an important role to increase the biomass productivity,
764
renewable energy technologies can offer innovative solutions on the short term. Other
765
imminent algae based research fields include the integration of cultivation with industrial
766
CO2 point source facilities and the use of wastewaters (WW) and/or seawater to reduce
767
the nutrient requirements and the water footprint. Agricultural WW sources can provide
768
a sustainable nutrient source for cultivation in rural areas, whereas municipal WW may
769
be used for cultivars in urban areas. Finally, as part of the overall sustainable analysis,
770
the socio-economic benefits and burdens require a more uniform and quantified study in
771
the final evaluation.
772
AUTHOR INFORMATION.
773
Corresponding Author
774
*Phone: +86 10 6278 4701; e-mail:
[email protected].
775
Notes
776
The authors declare no competing financial interest.
777
Author contributions
778
The manuscript was written through contributions of all authors. All authors have given
779
approval to the final version of the manuscript. ‡These authors contributed equally.
780
ACKNOWLEDGEMENTS
ACS Paragon Plus Environment
39
Environmental Science & Technology
Page 40 of 62
781
This work was supported by the Tsinghua University Initiative Scientific Research
782
Program (grant number: 20161080094) and National Recruitment Program of Global
783
Youth Experts (The National Youth 1000 – Talent Program) of China (grant number:
784
20151710227).
785
LIST OF ACRONYMS
786
AD
anaerobic digestion
787
ASPFT
advanced supercritical pulverized fuel technology
788
ATS
algal turf scrubbers
789
AWW
agricultural wastewater
790
BF
bioflocculation
791
C
Centrifugation
792
CHF
chitosan flocculation
793
CHG
catalytic hydrothermal gasification
794
CHP
combined heat and power
795
CAF
cationic flocculation
796
DAF
dissolved air flotation
797
DSE
dry solid extraction
798
FAME
fatty acid methyl esters
799
FARM
Farm-level Algae Risk Model
800
FPPBR
flat panel photobioreactors
801
FT
Fischer-Tropsch synthesis
802
GHG
greenhouse gas
803
HT
hydrotreating
ACS Paragon Plus Environment
40
Page 41 of 62
Environmental Science & Technology
804
HTL
hydrothermal liquefaction
805
IGCC
integrated gasification combined cycle
806
IWW
industrial wastewater
807
LCA
Life cycle analysis
808
LCI
Life cycle inventory
809
LEA
lipid extracted algal biomass
810
MPBR
membrane photobioreactors
811
MWW
municipal wastewater
812
NER
net energy ratio
813
NGCC
natural gas combined cycle
814
NPV
net present value
815
NR
nutrient recycling
816
ORP
open raceway ponds
817
PBR
photobioreactors
818
PF
Pressure filtration
819
PTW
pump to wheels
820
PE
photosynthetic efficiency
821
PP
power plant
822
PPC
paddle wheel pond circulation
823
RABR
rotating algal biofilm reactor
824
SV
Switch-value
825
TEA
techno-economic assessment
826
TPBR
tubular photobioreactors
ACS Paragon Plus Environment
41
Environmental Science & Technology
827
WSE
wet solid extraction
828
WTP
well to pump
829
WTW
well to wheels
830
WW
wastewater
831
REFERENCES
Page 42 of 62
832
(1) Godfray, H. C. J.; Beddington, J. R.; Crute, I. R.; Haddad, L.; Lawrence, D.; Muir,
833
J. F.; Pretty, J.; Robinson, S.; Thomas, S. M.; Toulmin, C. Food security: the challenge
834
of feeding 9 billion people. Sci. 2010, 327(5967), 812-818.
835
(2) Goli, A.; Shamiri, A.; Talaiekhozani, A.; Eshtiaghi, N.; Aghamohammadi, N.; Aroua,
836
M. K. An overview of biological processes and their potential for CO2 capture. J.
837
Environ. Manage. 2016, 183(Part 1), 41-58.
838
(3) Scarlat, N.; Dallemand, J.-F.; Monforti-Ferrario, F.; Nita, V. The role of biomass
839
and bioenergy in a future bioeconomy: policies and facts. Environ. Develop. 2015, 15,
840
3-34.
841
(4) Vuppaladadiyam, A. K.; Yao, J. G.; Florin, N.; George, A.; Wang, X.; Labeeuw, L.;
842
Jiang, Y.; Davis, R. W.; Abbas, A.; Ralph, P. Impact of flue gas compounds on
843
microalgae and mechanisms for carbon assimilation and utilization ‐ a review.
844
ChemSusChem 2017, 11(2): 334-355.
845
(5) Laurens, L. M. L. State of technology review - algae bioenergy, An IEA bioenergy,
846
inter-task strategic project, National Renewable energy Laboratory, Golden, CO, USA,
847
2017.
ACS Paragon Plus Environment
42
Page 43 of 62
Environmental Science & Technology
848
(6) Chiaramontia, D.; Prussi, M.; Buffi, M.; Rizzo, A. M.; Pari, L. Review and
849
experimental study on pyrolysis and hydrothermal liquefaction of microalgae for biofuel
850
production. Appl. Energ. 2017, 185(Part2), 963-972.
851
(7) Ishika, T.; Navid R.Moheimani, N. R.; Bahri., P. A. Sustainable saline microalgae
852
co-cultivation for biofuel production: a critical review. Renew. Sust. Energ. Rev. 2017,
853
78, 356-368.
854
(8) Khetkorn, W.; Rastogi, R. P.; AranIncharoensakdi, A.; Lindblad, P.; Madamwar, D.;
855
Pandey, A.; Larroche, C. Microalgal hydrogen production - a review. Bioresour,
856
Technol. 2017, 243, 1194-1206.
857
(9) Gaurav, N.; Sivasankari, S.; GSKiran, G. S.; Ninawe, A.; Selvin, J. Utilization of
858
bioresources for sustainable biofuels: a review. Renew. Sustain. Energ. Reviews 2017,
859
73, 205-214.
860
(10) Chew, K. W:; Yap, J. Y.; Show, P. L.; Suan, N. H.; Juan, J. C.; Ling, T. C.; Lee,
861
D.-J.; Chang, J.-S. Microalgae biorefinery: high value products perspectives. Bioresour.
862
Technol. 2017, 229, 53-62.
863
(11) De Corato, U.; De Bari, I.; Viola, E.; Pugliese, M. Assessing the main
864
opportunities of integrated biorefining from agro-bioenergy co/by-products and
865
agroindustrial residues into high-value added products associated to some emerging
866
markets: a review. Renew. Sustain. Energ. Rev 2018, 88, 326-346.
867
(12) Budzianowski, W. M. High-value low-volume bioproducts coupled to bioenergies
868
with potential to enhance business development of sustainable biorefineries. Renew.
869
Sustain. Energ. Rev. 2017, 70, 793-804.
ACS Paragon Plus Environment
43
Environmental Science & Technology
870
Page 44 of 62
(13) Raheem, A.; Prinsen, P.; Vuppaladadiyam, A. K.; Zhao, M.; Luque, R. A review
871
on
872
developments. J. Clean. Prod. 2018, 181, 42-59.
sustainable
microalgae
based
biofuel
and
bioenergy
production:
recent
873
(14) Juneja, A.; Murthy, G. S. Evaluating the potential of renewable diesel production
874
from algae cultured on wastewater: techno-economic analysis and life cycle
875
assessment. AIMS Energy 2017, 5(2), 239-257.
876
(15) Razzak, S. A.; Ali, S. A. M.; Hossain, M. M.; deLasa, H. Biological CO2 fixation
877
with production of microalgae in wastewater - a review. Renew. Sustain. Energ. Rev.
878
2017, 76, 379-390.
879
(16) Ansari, F. A.; Singh, P.; Guldhe, A.; Bux, F. Microalgal cultivation using
880
aquaculture wastewater: Integrated biomass generation and nutrient remediation. Algal
881
Res. 2017, 21,169-177.
882
(17) Delrue, F.; Álvarez-Díaz, P. D.; Fon-Sing, S.; Fleury, G.; Sassi, J.-F. The
883
environmental biorefinery: using microalgae to remediate wastewater, a win-win
884
paradigm. Energies 2016, 9(3), 132-151.
885
(18) Bulgariu L.; Bulgariu D. Sustainable Utilization of Marine Algae Biomass for
886
Environmental Bioremediation. In: Tripathi B.; Kumar, D. (eds.), Prospects and
887
Challenges in Algal Biotechnology, 2017, Springer, Singapore.
888
(19) Fasaei, F.; Bitter, J. H.; Slegers, P. M.; van Boxtel, A. J. B. Techno-economic
889
evaluation of microalgae harvesting and dewatering systems. Algal Res. 2018, 31, 347-
890
362.
891
(20) Acién, F. G.; Molina, E.; Fernández-Sevilla, J. M.; Barbosa, M.; Gouveia, L.;
892
Sepúlveda, C.; Bazaes, J.; Arbib, Z. 20 - Economics of microalgae production A2 -
ACS Paragon Plus Environment
44
Page 45 of 62
Environmental Science & Technology
893
Gonzalez-Fernandez, Cristina. In Microalgae-Based Biofuels and Bioproducts, Muñoz,
894
R. Ed. Woodhead Publishing: 2017; pp. 485-503.
895
(21) Laurens, L. M. L.; Markham, J.; Templeton, D. W.; Christensen, E. D.; Van
896
Wychen, S.; Vadelius, E. W.; Chen-Glasser, M.; Dong, T.; Davis, R.; Pienkos, P. T.
897
Development of algae biorefinery concepts for biofuels and bioproducts; a perspective
898
on process-compatible products and their impact on cost-reduction. Energ. Environ. Sci.
899
2017, 10, 1716-1738.
900
(22) Quiroz-Arita, C.; Sheehan, J. J.; Bradley, T. H. Life cycle net energy and
901
greenhouse gas emissions of photosynthetic cyanobacterial biorefineries: Challenges
902
for industrial production of biofuels. Algal Res. 2017, 46, 445-452.
903 904
(23) Ketzer, F.; Skarka, J.; Rösch, C. Critical review of microalgae LCA studies for bioenergy production. BioEnergy Res. 2018, 11(1), 95-105.
905
(24) Pérez-López, P.; de Vree, J. H.; Feijoo, G.; Bosma, R.; Barbosa, M. J.; Moreira,
906
M. T.; Wijffels, R. H.; van Boxtel, A. J. B.; Kleinegris, D. M. M. Comparative life cycle
907
assessment of real pilot reactors for microalgae cultivation in different seasons. Appl.
908
Energy 2017, 205(Supplement C), 1151-1164.
909
(25) Efroymson, R. A.; Dale, V. H.; Langholtz, M. H. Socioeconomic indicators for
910
sustainable design and commercial development of algal biofuel systems. Gcb
911
Bioenergy. 2017, 9(6), 1005-1023.
912
(26) Davis, R. E.; Fishman, D. B.; Frank, E. D.; Johnson, M. C.; Jones, S. B.; Kinchin,
913
C. M.; Skaggs, R. L.; Venteris, E. R.; Wigmosta, M. S. Integrated evaluation of cost,
914
emissions and resource potential for algal biofuels at the national scale. Environ. Sci.
915
Technol. 2014, 48, 6035-6042.
ACS Paragon Plus Environment
45
Environmental Science & Technology
Page 46 of 62
916
(27) Ruiz, J.; Olivieri, G.; de Vree, J.; Bosma, R.; Willems, P.; Reith, J. H.; Eppink, M.
917
H. M.; Kleinegris, D. M. M.; Wijffels, R. H.; Barbosa, M. J. Towards industrial products
918
from microalgae. Energy Environ. Sci. 2016, 9(10), 3036-3043.
919
(28) Barry, A.; Wolfe, A.; English, C.; Ruddick,C.; Lambert, D. National Algal Biofuels
920
Technology Review; Bioenergy Technologies Office: Office of Energy Efficiency and
921
Renewable Energy, 2016.
922
(29) Quinn, J. C.; Davis, R. The potentials and challenges of algae based biofuels: a
923
review of the techno-economic, life cycle, and resource assessment modeling.
924
Bioresour. Technol. 2015, 184, 444-452.
925 926 927 928
(30) Norsker, N.-H.; Barbosa, M. J.; Vermuë, M. H.; Wijffels, R. H. Microalgal production - a close look at the economics. Biotechnol. Adv. 2011, 29, (1), 24-27. (31) Slade, R.; Bauen, A. Micro-algae cultivation for biofuels: cost, energy balance, environmental impacts and future prospects. Biomass Bioenerg. 2013, 53, 29-38.
929
(32) Jones, S.; Zhu, Y.; Anderson, D.; Hallen, R.; Elliot, D.; Schmidt, A.; Albrecht, K.;
930
Hart, T.; Butcher, M.; Drennan, C.; Snowden-Swan, L.; Davis, R.; Kinchin, C. Process
931
Design and Economics for the Conversion of Algal Biomass to Hydrocarbons: Whole
932
Algae Hydrothermal Liquefaction and Upgrading, PNNL-23227, 2014, Pacific Northwest
933
National Laboratory, USA.
934
(33) Hoffman, J. Techno-economic assessment of micro-algae production systems,
935
2016.
936
https://digitalcommons.usu.edu/gradreports/789.
937 938
All
Graduate
Plan
B
and
other
Reports.
789.
(34) Barlow, J.; Sims, R. C.; Quinn, J. C. Techno-economic and life-cycle assessment of an attached growth algal biorefinery. Bioresour. Biotechnol. 2016, 220, 360-368.
ACS Paragon Plus Environment
46
Page 47 of 62
Environmental Science & Technology
939
(35) Rezvani, S.; Moheimani, N. R.; Bahri, P. A. Techno-economic assessment of
940
CO2 bio-fixation using microalgae in connection with three different state-of-the-art
941
power plants. Comput. Chem. Eng. 2016, 84, 290-301.
942
(36) Ghasemi Naghdi, F.; González González, L. M.; Chan, W.; Schenk, P. M.
943
Progress on lipid extraction from wet algal biomass for biodiesel production. Microb.
944
Biotechnol. 2016, 9(6), 718-726.
945
(37) Kim, J.; Yoo, G.; Lee, H.; Lim, J.; Kim, K.; Kim, C. W.; Park, M. S.; Yang, J.-W.
946
Methods of downstream processing for the production of biodiesel from microalgae.
947
Biotechnol. Adv. 2013, 31(6), 862-876.
948
(38) Dassey, A. J.; Theegala, C. S. Harvesting economics and strategies using
949
centrifugation for cost effective separation of microalgae cells for biodiesel applications.
950
Bioresour. Technol. 2013, 128, 241-245.
951
(39) Vandamme, D.; Foubert, I.; Muylaert, K. Flocculation as a low-cost method for
952
harvesting microalgae for bulk biomass production. Trends Biotechnol. 2013, 31(4),
953
233-239.
954
(40) Wan, C.; Alam, M. A.; Zhao, X.-Q.; Zhang, X.-Y.; Guo, S.-L.; Ho, S.-H.; Chang,
955
J.-S.; Bai, F.-W. Current progress and future prospect of microalgal biomass harvest
956
using various flocculation technologies. Bioresour. Technol. 2015, 184, 251-257.
957
(41) Schlesinger, A.; Eisenstadt, D.; Bar-Gil, A.; Carmely, H.; Einbinder, S.; Gressel,
958
J. Inexpensive non-toxic flocculation of microalgae contradicts theories; overcoming a
959
major hurdle to bulk algal production. Biotechnol. Adv. 2012, 30(5), 1023-1030.
960 961
(42) Xu, Y.; Purton, S.; Baganz, F. Chitosan flocculation to aid the harvesting of the microalga Chlorella sorokiniana. Bioresour. Technol. 2013, 129, 296-301.
ACS Paragon Plus Environment
47
Environmental Science & Technology
Page 48 of 62
962
(43) Rwehumbiza, V. M.; Harrison, R.; Thomsen, L. Alum-induced flocculation of
963
preconcentrated Nannochloropsis salina: residual aluminium in the biomass, FAMEs
964
and its effects on microalgae growth upon media recycling. Chem. Eng. J. 2012, 200,
965
168-175.
966
(44) Chen, F.; Liu, Z.; Li, D.; Liu, C.; Zheng, P.; Chen, S. Using ammonia for algae
967
harvesting and as nutrient in subsequent cultures. Bioresour. Technol. 2012, 121, 298-
968
303.
969
(45) Lee, A. K.; Lewis, D. M.; Ashman, P. J. Microbial flocculation, a potentially low-
970
cost harvesting technique for marine microalgae for the production of biodiesel. J. Appl.
971
Phycol. 2009, 21(5), 559-567.
972
(46) Lee, J.; Cho, D.-H.; Ramanan, R.; Kim, B.-H.; Oh, H.-M.; Kim, H.-S. Microalgae-
973
associated bacteria play a key role in the flocculation of Chlorella vulgaris. Bioresour.
974
Technol. 2013, 131, 195-201.
975
(47) Powell, R. J.; Hill, R. T. Rapid aggregation of biofuel-producing algae by the
976
bacterium Bacillus sp. strain RP1137. Appl. Environ. Microbiol. 2013, 79(19), 6093-
977
6101.
978 979
(48) Ferguson, C.; Logsdon, G.; Curley, D. Comparison of dissolved air flotation and direct filtration. Water Sci. Technol. 1995, 31(3-4), 113-124.
980
(49) Downing, J.; Bracco, E.; Green, F.; Ku, A.; Lundquist, T.; Zubieta, I.; Oswald, W.
981
Low cost reclamation using the Advanced Integrated Wastewater Pond Systems®
982
Technology and reverse osmosis. Water Sci. Technol. 2002, 45(1), 117-125.
983 984
(50) Mo, W.; Soh, L.; Werber, J. R.; Elimelech, M.; Zimmerman, J. B. Application of membrane dewatering for algal biofuel. Algal Res. 2015, 11, 1-12.
ACS Paragon Plus Environment
48
Page 49 of 62
Environmental Science & Technology
985
(51) Olivares, J. A.; Baxter, I.; Brown, J.; Carleton, M.; Cattolico, R. A.; Taraka, D.;
986
Detter, J. C.; Devarenne, T. P.; Dutcher, S. K.; Fox, D. T. National Alliance for
987
Advanced Biofuels and Bio-Products Final Technical Report; Donald Danforth Plant
988
Science Center, 2014.
989
(52) Zhou, W.; Cheng, Y.; Li, Y.; Wan, Y.; Liu, Y.; Lin, X.; Ruan, R. Novel fungal
990
pelletization-assisted technology for algae harvesting and wastewater treatment. Appl.
991
Biochem. Biotechnol. 2012, 167(2), 214-228.
992
(53) Vandamme, D.; Pontes, S. C. V.; Goiris, K.; Foubert, I.; Pinoy, L. J. J.; Muylaert,
993
K. Evaluation of electro‐coagulation–flocculation for harvesting marine and freshwater
994
microalgae. Biotechnol. Bioeng. 2011, 108(10), 2320-2329.
995 996
(54) Gouveia, L. Microalgae as a Feedstock for Biofuels. In Microalgae as a Feedstock for Biofuels, Springer Berlin Heidelberg, 2011; pp. 1-69.
997
(55) Richardson, J. W.; Johnson, M. D.; Outlaw, J. L. Economic comparison of open
998
pond raceways to photo bio-reactors for profitable production of algae for transportation
999
fuels in the Southwest. Algal Res. 2012, 1, 93–100.
1000
(56) Rogers, J. N.; Rosenberg, J. N.; Guzman, B. J.; Oh, V. H.; Mimbela, L. E.,
1001
Ghassemi, A.; Betenbaugh, M. J.; Oyler, G. A.; Donohue, M. D. A critical analysis of
1002
paddlewheel-driven raceway ponds for algal biofuel production at commercial scales.
1003
Algal Res. 2014, 4, 76–88.
1004
(57) Richardson, J. W.: Johnson, M. D.; Zhang, X.; Zemke, P.; Chen, W.; Hub, Q. A
1005
financial assessment of two alternative cultivation systems and their contributions to
1006
algae biofuel economic viability. Algal Res. 2014, 4, 96-104.
ACS Paragon Plus Environment
49
Environmental Science & Technology
Page 50 of 62
1007
(58) Beal, C. M.; Gerber, L. N.; Sills, D. L.; Huntley, M. E.; Machesky, S. C.; Walsh, M.
1008
J.; Tester, J. W.; Archibald, I.; Granados, J.; Greene, C. H. Algal biofuel production for
1009
fuels and feed in a 100-ha facility: a comprehensive techno-economic analysis and life
1010
cycle assessment. Algal Res. 2015, 10, 266-279.
1011 1012
(59) Pearce, M.; Shemfe, M.; Sansom, C. Techno-economic analysis of solar integrated hydrothermal liquefaction of microalgae. Appl. Energy 2016, 166, 19-26.
1013
(60) Batan, L. Y.; Graff, G. D.; Bradley, T. H. Techno-economic and Monte Carlo
1014
probabilistic analysis of microalgae biofuel production system. Bioresour. Technol.
1015
2016, 219, 45-52.
1016
(61) Williams, P. J. le B.; Laurens, L. M. L. Microalgae as biodiesel & biomass
1017
feedstocks: review & analysis of the biochemistry, energetics & economics. Energy
1018
Environ. Sci. 2010, 3, 554–590.
1019
(62) Patel, M.; Zhang, X.; Kumar, A. Techno-economic and life cycle assessment on
1020
lignocellulosic biomass thermochemical conversion technologies: a review. Renew.
1021
Sustain. Energ. Rev. 2016, 53, 1486-1499.
1022
(63) Ou, L.; Thilakaratne, R.; Brown, R. C.; Wright, M. M. Techno-economic analysis
1023
of transportation fuels from defatted microalgae via hydrothermal liquefaction and
1024
hydroprocessing. Biomass Bioenergy 2015, 72, 45-54.
1025
(64) Zhu, Y.; Jones, S. B.; Anderson, D. B.; Hallen, R. T.; Schmidt, A. J.; Albrecht, K.
1026
O.; Elliott, D. C. Techno-Economic Analysis of Whole Algae Hydrothermal Liquefaction
1027
(HTL) and Upgrading System. 2015 Algae Biomass Summit, Washington, DC, USA,
1028
September 29-October 2, 2015.
ACS Paragon Plus Environment
50
Page 51 of 62
Environmental Science & Technology
1029
(65) Thilakaratne, R.; Wright, M. W.; Brown, R. C. A techno-economic analysis of
1030
microalgae remnant catalytic pyrolysis and upgrading to fuels. Fuel 2014, 128, 104-112.
1031
(66) Dong, T.; Knoshaug, E. P.; Davis, R.; Laurens, L. M. L. L.; Van Wychen, S.;
1032
Pienkos, P. T.; Nagle, N. Combined algal processing: a novel integrated biorefinery
1033
process to produce algal biofuels and bioproducts. Algal Res. 2016, 19, 316-323.
1034 1035
(67) Gomez, J. A.; Hoffner, K.; Barton, P. I. From sugars to biodiesel using microalgae and yeast. Green Chem. 2016, 18(2), 461-475.
1036
(68) Beopoulos, A.; Cescut, J.; Haddouche, R.; Uribelarrea, J.-L.; Molina-Jouve, C.;
1037
Nicaud, J.-M. Yarrowia lipolytica as a model for bio-oil production. Prog. Lipid Res.
1038
2009, 48(6), 375-387.
1039
(69) Doshi, A.; Pascoe, S.; Coglan, L.; Rainey, T. The financial feasibility of
1040
microalgae biodiesel in an integrated, multioutput production system. Biofuels, Bioprod.
1041
Biorefin. 2017, 11(6), 991-1006.
1042
(70) Bravo-Fritz, C. P.; Sáez-Navarrete, C. A.; Herrera-Zeppelin, L. A.; Varas-Concha,
1043
F. Multi-scenario energy-economic evaluation for a biorefinery based on microalgae
1044
biomass with application of anaerobic digestion. Algal Res. 2016, 16, 292-307.
1045
(71) Wen, X.; Du, K.; Wang, Z.; Peng, X.; Luo, L.; Tao, H.; Xu, Y.; Zhang, D.; Geng,
1046
Y.; Li, Y. Effective cultivation of microalgae for biofuel production: a pilot-scale
1047
evaluation of a novel oleaginous microalga Graesiella sp. WBG-1. Biotechnol. Biofuels
1048
2016, 9(1), 123-135.
1049
(72) Laurens, L. M. L.; Chen-Glasser, M.; McMillan, J. D. A perspective on renewable
1050
bioenergy from photosynthetic algae as feedstock for biofuels and bioproducts. Algal
1051
Res. 2017, 24(Part A), 261-264.
ACS Paragon Plus Environment
51
Environmental Science & Technology
1052 1053
Page 52 of 62
(73) Rizwan, M.; Lee, J. H.; Gani, R. Optimal design of microalgae-based biorefinery: Economics, opportunities and challenges. Appl. Energy 2015, 150, 69-79.
1054
(74) Fernandez, F. G. A.; Sevilla, J. M. F.; Grima, E. M. Microalgae: The Basis of
1055
Mankind Sustainability, Case Study of Innovative Projects-Successful Real Cases,
1056
InTech,
1057
https://www.intechopen.com/books/case-study-of-innovative-projects-successful-real-
1058
cases/microalgae-the-basis-of-mankind-sustainability: 2017.
Llamas,
B.
(Ed.),
DOI:
10.5772/67930.
Available
from:
1059
(75) van der Voort, M. P. J.; Spruijt, J.; Potters, J.; de Wolf, P. L.; Elissen, H. J. H.
1060
Socio-economic assessment of algae-based PUFA production, Public output report of
1061
the PUFAChain project, Göttingen, 2017, pp. 79, Available online at www.pufachain.eu.
1062 1063
(76) Spolaore, P.; Joannis-Cassan, C.; Duran, E.; Isambert, A. Commercial applications of microalgae. J. Biosci. Bioeng. 2006, 101(2), 87-96.
1064
(77) Skjånes, K.; Rebours, C.; Lindblad, P. Potential for green microalgae to produce
1065
hydrogen, pharmaceuticals and other high value products in a combined process. Crit.
1066
Rev. Biotechnol. 2013, 33(2), 172-215.
1067 1068
(78) G. P. ‘t Lam, J. A. van der Kolk, A. Chordia, M. H. Vermuë, G. Olivieri, M. H. M. Eppink and R. H. Wijffels, ACS Sustainable Chem. Eng., 2017, 5(7), 6046-6057.
1069
(79) da Costa Sousa, L.; Foston, M.; Bokade, V.; Azarpira, A.; Lu, F.; Ragauskas, A.
1070
J.; Ralph, J.; Dale, B.; Balan, V. Isolation and characterization of new lignin streams
1071
derived from extractive-ammonia (EA) pretreatment. Green Chem. 2016, 18(15), 4205-
1072
4215.
ACS Paragon Plus Environment
52
Page 53 of 62
Environmental Science & Technology
1073
(80) Prinsen, P.; Narani, A.; Rothenberg, G. Lignin depolymerisation and
1074
lignocellulose fractionation by solvated electrons in liquid ammonia. ChemSusChem
1075
2017, 10(5), 1022-1032.
1076
(81) Xiaowei, L.; , B.; , P.; Colosi, L. M.; , M. G.; , J.; Clarens, A. F. Pilot-scale data
1077
provide enhanced estimates of the life cycle energy and emissions profile of algae
1078
biofuels produced via hydrothermal liquefaction. Bioresour. Technol. 2013, 148, 163-
1079
171.
1080 1081
(82) GREET 2011, Argonne GREET Model. (available at http://greet.es.anl.gov/main, accessed 15th April 2018).
1082
(83) Woertz, I. C.; Benemann, J. R.; Du, N.; Unnasch, S.; Mendola, D.; Mitchell, B. G.;
1083
Lundquist, T. J. Life cycle GHG emissions from microalgal biodiesel - a CA-GREET
1084
model. Environ. Sci. Technol. 2014, 48(11), 6060-6068.
1085
(84) Taelman, S. E.; Sfez, S. Environmental Life Cycle Assessment (LCA) of algae
1086
production in North West Europe (NWE), Public Output report of the EnAlgae project,
1087
Swansea, 2015. Available online at http://www.enalgae.eu/public-deliverables.htm;.
1088
(85) Stephenson, A. L.; Kazamia, E.; Dennis, J. S.; Howe, C. J.; Scott, S. A.; Smith, A.
1089
G. Life-cycle assessment of potential algal biodiesel production in the United Kingdom:
1090
a comparison of raceways and air-lift tubular bioreactors. Energy Fuels. 2010, 24(7),
1091
4062-4077.
1092 1093 1094 1095
(86) Malik, A.; Lenzen, M.; Ralph, P. J.; Tamburic, B. Hybrid life-cycle assessment of algal biofuel production. Bioresour. Technol. 2015, 184, 436-443. (87) Gnansounou, E.; Raman, J. K. Life cycle assessment of algae biodiesel and its co-products. Appl. Energy 2016, 161, 300-308.
ACS Paragon Plus Environment
53
Environmental Science & Technology
Page 54 of 62
1096
(88) Clarens, A. F.; Resurreccion, E. P.; White, M. A.; Colosi, L. M. Environmental life
1097
cycle comparison of algae to other bioenergy feedstocks. Environ. Sci. Technol. 2010,
1098
44(5), 1813-1819.
1099
(89) Collet, P.; Lardon, L.; Hélias, A.; Bricout, S.; Lombaert-Valot, I.; Perrier, B.;
1100
Lépine, O.; Steyer, J.-P.; Bernard, O. Biodiesel from microalgae - life cycle assessment
1101
and recommendations for potential improvements. Renew. Energ. 2014, 71, 525-533.
1102
(90) Frank, E.; Han, J.; Palou-Rivera, I.; Elgowainy, A.; Wang, M. Life-cycle analysis
1103
of algal lipid fuels with the GREET model. ANL/ESD/11-5. Argonne National Laboratory,
1104
2011. Available at http://greet.es.anl.gov/publications).
1105
(91) Zaimes, G. G.; Khanna, V. Environmental sustainability of emerging algal
1106
biofuels: a comparative life cycle evaluation of algal biodiesel and renewable diesel.
1107
Environ. Prog. Sustainable Energy 2013, 32(4), 926-936.
1108
(92) Quinn, J. C.; Hanif, A.; Sharvelle, S.; Bradley, T. H. Microalgae to biofuels: life
1109
cycle impacts of methane production of anaerobically digested lipid extracted algae.
1110
Bioresour. Technol. 2014, 171, 37-43.
1111
(93) Soh, L.; Montazeri, M.; Haznedaroglu, B. Z.; Kelly, C.; Peccia, J.; Eckelman, M.
1112
J.; Zimmerman, J. B. Evaluating microalgal integrated biorefinery schemes: empirical
1113
controlled growth studies and life cycle assessment. Bioresour. Technol. 2014, 151, 19-
1114
27.
1115
(94) Ponnusamy, S.; Reddy, H. K.; Muppaneni, T.; Downes, C. M.; Deng, S. Life cycle
1116
assessment of biodiesel production from algal bio-crude oils extracted under subcritical
1117
water conditions. Bioresour. Technol. 2014, 170, 454-461.
ACS Paragon Plus Environment
54
Page 55 of 62
Environmental Science & Technology
1118
(95) Azadi, P.; Brownbridge, G.; Mosbach, S.; Smallbone, A.; Bhave, A.; Inderwildi,
1119
O.; Kraft, M. The carbon footprint and non-renewable energy demand of algae-derived
1120
biodiesel. Appl. Energy 2014, 113, 1632-1644.
1121
(96) Adesanya, V. O.; Cadena, E.; Scott, S. A.; Smith, A. G. Life cycle assessment on
1122
microalgal biodiesel production using a hybrid cultivation system. Bioresour. Technol.
1123
2014, 163, 343-3(98)
1124
(97) European Parliament et EC. Directive 2009/28/EC of the European parliament
1125
and of the council of 23 April 2009 on the promotion of the use of energy from
1126
renewable sources and amending and subsequently repealing directives 2001/77/EC
1127
and 2003/30/EC, 2009.
1128
(98) Pérez-López, P.; Feijoo, G.; Moreira, M. T. Sustainability assessment of blue
1129
biotechnology processes: addressing environmental, social and economic dimensions,
1130
2018. In: Benetto, E.; Gericke, K., Guiton, M. (Eds.), Designing sustainable
1131
technologies, products and policies. Springer, Cham, 2018.
1132
(99) Medeiros, D. L.; Sales, E. A.; Kiperstok, A. Energy production from microalgae
1133
biomass: the carbon footprint and energy balance, 4th International Workshop Advances
1134
in Cleaner Production "Integrating Cleaner Production into Sustainable Strategies", São
1135
Paulo (Brazil), May 2013.
1136
(100) Chiaramonti, D.; Prussi, M.; Casini, D.; Tredici, M. R.; Rodolfi, L.; Bassi, N.;
1137
Zittelli, G. C.; Bondioli, P. Review of energy balance in raceway ponds for microalgae
1138
cultivation: re-thinking a traditional system is possible. Appl. Energ. 2013, 102, 101-
1139
111.
ACS Paragon Plus Environment
55
Environmental Science & Technology
Page 56 of 62
1140
(101) Handler, R. M.; Shonnard, D. R.; Kalnes, T. N.; Lupton, F. S. Life cycle
1141
assessment of algal biofuels: influence of feedstock cultivation systems and conversion
1142
platforms. Algal Res. 2014, 4, 105-115.
1143 1144
(102) Pragya, N.; Pandey, K. K. Life cycle assessment of green diesel production from microalgae. Renewable Energy 2016, 86, 623-632.
1145
(103) Frank, E. D.; Elgowainy, A.; Han, J.; Wang, Z. Life cycle comparison of
1146
hydrothermal liquefaction and lipid extraction pathways to renewable diesel from algae.
1147
Mitig. Adapt. Strateg. Glob. Change 2013, 18, 137-158.
1148
(104) Fortier, M.-O. P.; Roberts, G. W.; Stagg-Williams, S. M.; Sturm, B. S.M. Life
1149
cycle assessment of bio-jet fuel from hydrothermal liquefaction of microalgae. Appl.
1150
Energy 2014, 122, 73-82.
1151
(105) Bennion, E. P.; Ginosar, D. M.; Moses, J.; Agblevor, F.; Quinn, J. C. Lifecycle
1152
assessment of microalgae to biofuel: comparison of thermochemical processing
1153
pathways. Appl. Energy 2015, 154, 1062-1071.
1154
(106) Jacob, A.; Xia, A.; Murphy, J. D. A perspective on gaseous biofuel production
1155
from micro-algae generated from CO2 from a coal-fired power plant. Appl. Energy 2015,
1156
148, 396-402.
1157
(107) Gutierrez-Arriaga, C. G.; Serna-Gonzalez, M.; Ponce-Ortega, J. M.; El-Halwagi,
1158
M. M. Sustainable integration of algal biodiesel production with steam electric power
1159
plants for greenhouse gas mitigation. ACS Sustain. Chem. Eng. 2014, 2(6), 1388-1403.
1160
(108) Rickman, M.; Pellegrino, J.; Hock, J.; Shaw, S.; Freeman, B. Life-cycle and
1161
techno-economic analysis of utility-connected algae systems. Algal Res. 2013, 2(1), 59-
1162
65.
ACS Paragon Plus Environment
56
Page 57 of 62
1163 1164
Environmental Science & Technology
(109) Efroymson, R. Sustainable development of algae for biofuel, DOE Bioenergy Technologies Office Project Peer Review, 2017.
1165
(110) Guieysse, B.; Béchet, Q.; Shilton, A. Variability and uncertainty in water demand
1166
and water footprint assessments of fresh algae cultivation based on case studies from
1167
five climatic regions. Bioresour. Technol. 2013, 128, 317-323.
1168
(111) Yang, J.; Xu, M.; Zhang, X.; Hu, Q.; Sommerfeld, M.; Chen, Y. Life-cycle
1169
analysis on biodiesel production from microalgae: water footprint and nutrients balance.
1170
Bioresour. Technol. 2011, 102(1), 159-165.
1171 1172
(112) Subhadra, B. G.; Edwards, M. Coproduct market analysis and water footprint of simulated commercial algal biorefineries. Appl. Energy 2011, 88(10), 3515-3523.
1173
(113) Harto, C.; Meyers, R., Williams, E. Life cycle water use of low carbon transport
1174
fuels. Energy Policy 2010, 38, 4933-4944.
1175
(114) Dominguiz-Faus, R.; Powers, S.E.; Burken, J. E.; Alvarez P. J. The water
1176
footprint of biofuels: a drink or drive issue. Environ. Sci. Technol. 2009, 43, 3005-3010.
1177
(115) Pérez-López, P.; de Vree, J. H.; Feijoo, G.; Bosma, R.; Barbosa, M. J.; Moreira,
1178
M. T.; Wijffels, R. H.; van Boxtel, A. J. B.; Kleinegris, D. M. M. Comparative life cycle
1179
assessment of real pilot reactors for microalgae cultivation in different seasons. Appl.
1180
Energy 2017, 205(Supplement C), 1151-1164.
1181
(116) Papadaki, S.; Kyriakopoulou, K.; Tzovenis, I.; Krokida, M. Environmental impact
1182
of phycocyanin recovery from Spirulina platensis cyanobacterium. Innovative Food Sci.
1183
Emerg. Technol. 2017, 44(Supplement C), 217-223.
1184 1185
(117) Groom, M. J.; Gray, E. M.; Townsend, P. A. Biofuels and biodiversity: principles for creating better policies for biofuel production. Conserv. Biol. 2008, 22(3), 602-609.
ACS Paragon Plus Environment
57
Environmental Science & Technology
1186 1187
Page 58 of 62
(118) Kröger, M.; Müller-Langer, F. Review on possible algal-biofuel production processes. Biofuels 2012, 3, 333-349.
1188
(119) Venteris, E. R.; McBride, R. C.; Coleman, A. M.; Skaggs, R. L.; Wigmosta, M. S.
1189
Siting Algae cultivation facilities for biofuel production in the United States: trade-offs
1190
between growth rate, site constructability, water availability, and infrastructure. Environ.
1191
Sci. Technol. 2014, 48, 3559-3566.
1192 1193
(120) Zhang, C.; Anadon, L. D. Life cycle water use of energy production and its environmental impacts in China. Environ. Sci. Technol. 2013, 47, 14459-14467.
1194
(121) Nayak, M.; Karemore, A.; Sen, R. Performance evaluation of microalgae for
1195
concomitant wastewater bioremediation, CO2 biofixation and lipid biosynthesis for
1196
biodiesel application. Algal Res. 2016, 16, 216-223.
1197 1198
(122) Hoh, D.; Watson, S.; Kan, E. Algal biofilm reactors for integrated wastewater treatment and biofuel production: A review. Chem. Eng. J. 2016, 287, 466-473.
1199
(123) Xiao, L.; Young, E. B.; Grothjan, J. J.; Lyon, S.; Zhang, H.; He, Z. Wastewater
1200
treatment and microbial communities in an integrated photo-bioelectrochemical system
1201
affected by different wastewater algal inocula. Algal Res. 2015, 12, 446-454.
1202 1203
(124) Burkholder, J. M.; Glibert, P. M.; Skelton, H. M. Mixotrophy, a major mode of nutrition for harmful algal species in eutrophic waters. Harmful Algae 2008, 8(1), 77-93.
1204
(125) Usher, P. K.; Ross, A. B.; Camargo-Valero, M. A.; Tomlin, A. S.; Gale, W. F. An
1205
overview of the potential environmental impacts of large-scale microalgae cultivation.
1206
Biofuels 2014, 5(3), 331-349.
1207
(126) Handler, R. M.; Canter, C. E.; Kalnes, T. N.; Lupton, F. S.; Kholiqov, O.;
1208
Shonnard, D. R.; Blowers, P. Evaluation of environmental impacts from microalgae
ACS Paragon Plus Environment
58
Page 59 of 62
Environmental Science & Technology
1209
cultivation in open-air raceway ponds: Analysis of the prior literature and investigation of
1210
wide variance in predicted impacts. Algal Res. 2012, 1(1), 83-92.
1211 1212
(127) Mata, T. M.; Martins, A. A.; Caetano, N. S. Microalgae for biodiesel production and other applications: a review. Renew. Sustain. Energ. Rev. 2010, 14(1), 217-232.
1213
(128) Devine-Wright, P. In A cross-national, comparative analysis of public
1214
understanding of, and attitudes towards nuclear, renewable and fossil-fuel energy
1215
sources, Proceedings of the 3rd conference of the EPUK (Environmental Psychology in
1216
the UK) network: Crossing Boundaries - The Value of Interdisciplinary Research, 2003;
1217
160-173.
1218
(129) Rawat, I.; Gupta, S. K.; Shriwastav, A.; Singh, P.; Kumari, S.; Bux, F.
1219
Microalgae Applications in Wastewater Treatment. In Bux, F. and Chisti. Y- (Eds.),
1220
Algae Biotechnology, Springer, Cham, 2016, pp. 249-268.
1221
(130) Razzak, S. A.; Hossain, M. M.; Lucky, R. A.; Bassi, A. S.; de Lasa, H. Integrated
1222
CO2 capture, wastewater treatment and biofuel production by microalgae culturing - a
1223
review. Renew. Sustain. Energ. Rev. 2013, 27, 622-653.
1224
(131) Gabriel Acién, F; Gómez-Serrano, M.; Morales-Amaral, M.; Fernández-Sevilla,
1225
Molina-Grima, E. Wastewater treatment using microalgae: how realistic a contribution
1226
might it be to significant urban wastewater treatment? Appl. Microbiol. Biotechnol. 2016,
1227
100(21), 9013-9022.
1228
(132) Zhou, W.; Li, Y.; Min, M.; Hu, B.; Chen, P.; Ruan, R. Local bioprospecting for
1229
high-lipid producing microalgal strains to be grown on concentrated municipal
1230
wastewater for biofuel production. Bioresour. Technol. 2011, 102(13), 6909-6919.
ACS Paragon Plus Environment
59
Environmental Science & Technology
1231 1232
Page 60 of 62
(133) Kröger, M.; Müller-Langer, F. Review on possible algal-biofuel production processes. Biofuels 2012, 3, 333-349.
1233
(134) Cho, S.; Luong, T, T.; Lee, D.; Oh, Y.-K.; Lee, T. Reuse of effluent water from a
1234
municipal wastewater treatment plant in microalgae cultivation for biofuel production.
1235
Bioresour. Technol. 2011, 102(18), 8639-8645.
1236
(135) Komolafe, O.; Velasquez Orta, S. B.; Monje-Ramirez, I.; Yáñez Noguez,
1237
Harvey, A. P.; Orta Ledesma, M. T. Biodiesel production from indigenous microalgae
1238
grown in wastewater. Bioresour. Technol. 2014, 154, 297-304.
1239
(136) Chinnasamy, S.; Bhatnagarab, A.; Hunt, R. W.; Das, K. C. Microalgae
1240
cultivation in a wastewater dominated by carpet mill effluents for biofuel applications.
1241
Bioresour. Technol. 2010, 101(9),3097-3105.
1242
(137) Li, C.; Yang, moustaf.; Xia, X.; Li, Y.; Chen, L.; Zhang, M.; Zhang, L.; Wang, W.
1243
High efficient treatment of citric acid effluent by Chlorella vulgaris and potential biomass
1244
utilization. Bioresour. Technol. 2013, 127, 248-255.
1245
(138) Farooq, W.; Lee, Y.-C.; Ryu, B.-G.; Kim, B.-H.; Kim, H.-S.; Choi, Y.-E.; Yang,
1246
J.-W. Two-stage cultivation of two Chlorella sp. strains by simultaneous treatment of
1247
brewery wastewater and maximizing lipid productivity. Bioresour. Technol. 2013, 132,
1248
230-238.
1249 1250
(139) Johnson, M. B.; Wen, Z. Development of an attached microalgal growth system for biofuel production. Appl. Microbiol. Biotechnol. 2010, 85, 525-534.
1251
(140) Abou-Shanab, R. A. I.; Ji, M. K.; Kim, H. C.; Jung Paeng, K.- J.; Jen, B.-H.
1252
Microalgal species growing on piggery wastewater as a valuable candidate for nutrient
1253
removal and biodiesel production. J. Environ. Manage. 2013, 115(30), 257-264.
ACS Paragon Plus Environment
60
Page 61 of 62
Environmental Science & Technology
1254
(141) Levine, R. B.; Costanza-Robinson, M. S.; Spatafora, G. C. Neochloris
1255
oleoabundans grown on anaerobically digested dairy manure for concomitant nutrient
1256
removal and biodiesel feedstock production. Biomass Bioenergy 2011, 35(1), 40-49.
1257
(142) Zhu, L.; Wang, Z.; Shu, Q.; Takala, J.; Hiltunen, E.; Feng, P.; 1206 Yuan, Z.
1258
Nutrient removal and biodiesel production by integration of freshwater algae cultivation
1259
with piggery wastewater treatment. Water Research 2013, 47(13), 4294-4302.
1260
(143) Garcia, D.; Posadas, E.; Blanco, S.; Acien, G.; Bolado, S.; Muñoz, R.
1261
Evaluation of the dynamics of microalgae population structure and process performance
1262
during piggery wastewater treatment in algal-bacterial photobioreactors. In 15th
1263
International Conference on Environmental Science and Technology, Rhodes, Greece,
1264
2017.
1265
(144) Fenton, O.; Uallacháin, D. Ó. Agricultural nutrient surpluses as potential input
1266
sources to grow third generation biomass (microalgae): a review. Algal Res. 2012, 1(1),
1267
49-56.
1268
(145) Ruiz-Martinez, A.; Martin Garcia, N.; Romero, I.; Seco, A.; Ferrer, J. Microalgae
1269
cultivation in wastewater: nutrient removal from anaerobic membrane bioreactor
1270
effluent. Bioresour. Technol. 2012, 126, 247-253.
1271
(146) Cheng, H.; Tian, G. Identification of a newly isolated microalga from a local
1272
pond and evaluation of its growth and nutrients removal potential in swine breeding
1273
effluent. Desalin. Water Treat. 2013, 51, 2768-2775.
1274
(147) Wang, H.; Xiong, H.; Hui, Z.; Zeng, X. Mixotrophic cultivation of Chlorella
1275
pyrenoidosa with diluted primary piggery wastewater to produce lipids. Bioresour.
1276
Technol. 2012, 104, 215-220.
ACS Paragon Plus Environment
61
Environmental Science & Technology
Page 62 of 62
1277
(148) Luo, Y.; Le-Clech, P.; Henderson, R. K. Simultaneous microalgae cultivation
1278
and wastewater treatment in submerged membrane photobioreactors: a review. Algal
1279
Res. 2017, 24, 425-437.
1280 1281
(149) Oltra, C. Stakeholder perceptions of biofuels from microalgae. Energy Policy 2011, 39(3), 1774-1781.
1282
(150) Dale, B. E.; Anderson, J. E.; Brown, R. C.; Csonka, S.; Dale, V. H.; Herwick, G.;
1283
Jackson, R. D.; Jordan, N.; Kaffka, S.; Kline, K. L.; Lynd, L. R.; Malmstrom, C.; Ong,
1284
R.G.; Richard, T. L.; Taylor, C.; Wang, M. Q. Take a closer look: biofuels can support
1285
environmental, economic and social goals. Environ. Sci. Technol. 2014, 48, 7200-7203.
1286 1287
(151) Zhu, L.; Ketola, T. Microalgae production as a biofuel feedstock: risks and challenges. Int. J. Sustainable Dev. World Ecol. 2012, 19(3), 268-274.
1288
(152) Rösch, C.; Skarka, J.; Kugler, F. Results of the EnAlgae Stakeholder Workshop
1289
on “Benefits and Risks from Biomass Production with Microalgae”; Energetic Algae
1290
(‘EnAlgae’), Project no. 215G: Frankfurt, Germany, 2014.
1291 1292
(153) Chaudhry, A. M.; Barbier, E. B. Water and growth in an agricultural 1135 economy. Agric. Econ. 2013, 44(2), 175-189.
1293
(154) Wigmosta, M. S.; Coleman, A. M.; Skaggs, R. J.; Huesemann, M.H.; Lane, L. J.
1294
National microalgae biofuel production potential and resource demand. Water Resour.
1295
Res. 2011, 47, 1-13.
1296 1297
(155) Christensen, Pia B. et al. 2013. Combined uses – Marine biomass from offshore wind parks. SUBMARINER Report 11/2013.
1298
ACS Paragon Plus Environment
62