Beyond the Fossil Fuel Era: On the Feasibility of Sustainable

Article pubs.acs.org/EF

Beyond the Fossil Fuel Era: On the Feasibility of Sustainable Electricity Generation Using Biogas from Microalgae Frank ter Veld* Department of Plant Biochemistry, Ruhr-University Bochum, D-44801, Bochum, Germany ABSTRACT: In this century, biofuels will play an important role as fossil fuel alternatives. However, the long-term sustainability of large-scale biomass-based energy production chains is largely unknown. The current study evaluates the effect of nitrogen and phosphorus nutrient recovery on net energy ratio (NER) and land use, comparing a prospective industrial-scale microalgae production system with established maize agriculture. The functional unit was the delivery of 1.0 TWh of electrical energy using biomethane firing. Nutrient recovery was modeled by embedding anaerobic digestion (AD) as downstream processing step in the biomass production chains. The main finding was that maize-based biomethane electricity provision outperforms a prospective microalgae system in terms of NER, estimated at 4.9 and 3.2, respectively, when utilizing cogenerated heat. In the absence of external fossil fuel input, the renewable maize- and microalgae-based systems would require surface areas of 6.2 × 104 and 3.9 × 104 ha, respectively. Sustainability of microalgae-based biofuel production is not set by areal productivity or microalgal lipid content but rather by nutrient recovery, which is an important finding that requires prioritization in microalgae research.

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have been presented as a future biomass supply,6 also due to various high algae biomass productivity claims.7,8 However, the idea of producing biogas from microalgae is by no means new and was proposed in the early 1950s.9 Because it makes little sense to develop renewable biofuel systems that rely strongly on finite fossil fuel inputs, this paper presents an energy input−output model of zero-emission systems that operate independently from fossil fuel energy inputs. Cyanobacteria Spirulina (Arthrospira platensis), abusively called “microalgae” in this study, cultivated in high rate ponds (HRPs), are used as feedstock for anaerobic digestion (AD), with maize-based biogas production serving as a reference. In contrast to previous life-cycle analysis studies on microalgae energy production,10−13 published experimental data were preferred and the use of empirical formulas was avoided, if possible. The contributions of this paper are as follows: (1) maizebased biomethane production outperforms a prospective microalgae system, in terms of net energy ratio (i.e., ratio of energy produced to energy required for fuel production; abbreviated hereafter as NER); (2) a prospective microalgae system requires 35% less land area, compared to maize, and (3) the performance, in terms of NER, of microalgae-based biogas production is set by the provision and extraction of nutrients rather than areal productivity and/or microalgal lipid content.

INTRODUCTION This century will see the gradual and inevitable exhaustion of the Earth’s fossil energy resources, necessitating new sustainable resources that will need to progressively replace finite fossil fuel reserves for the provision of energy. Moreover, efficient use of resources, fossil fuel-related emissions, and, importantly, government policy have resulted in a new industrial era that has set itself the bold task of developing a fully renewable energy infrastructure. Unlike the exploitation of fossil fuel reserves, requiring energy input downstream of the fuel product only, biomassbased energy requires considerable upstream input, such as process energy and feedstock supply, including CO2 in case of microalgae cultivation. These upstream requirements dictate the concept of extracting key process nutrients, such as nitrogen and phosphorus, at the end of the biofuel production cycle to be used as biofertilizer . Taken together, future biofuel production will need to rely heavily on complex systems capable of efficient feedstock recycling. Hence, it was soon recognized by European Union (EU) governments that the complete life-cycle of future biomass production systems should be analyzed thoroughly1 to safeguard the sustainability of biofuel production.2 Indeed, harvesting an infinite solar energy supply will depend on Earth’s finite material resources, and, in this study, system sustainability is set by the reaggregation of nutrient resources as downstream processing step. Of note, for an in-depth review on the general concept of sustainability, the reader is referred to ref 3. If biomass-based energy is to be successful on an industrial scale, important concerns such as increased eutrophication, acidification, soil erosion, and the implications of genetically modified organism disposal4 will need to be minimized.5 Biogas, which is a 60/40% v/v mixture of methane and CO2, has been receiving increased attention as a possible renewable energy resource. Although, primarily, cattle manure and maize silage is currently being used as biogas feedstock, microalgae © 2012 American Chemical Society

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METHODOLOGY Goal and Scope Definition. The main objective of this study was to demonstrate the impact of incorporating anaerobic digestion (AD) in a microalgae biomass-based biofuel production cascade. This was achieved by an extensive review of literature data and by comparing the energy balance of a Received: March 15, 2012 Revised: May 18, 2012 Published: May 21, 2012 3882

dx.doi.org/10.1021/ef3004569 | Energy Fuels 2012, 26, 3882−3890

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prospective microalgae industrial-scale cultivation process with established maize agriculture for the production of biomethane. Both systems are located in northern Germany. The following assumptions have been made: energy inputs related to construction works, machinery, and equipment were omitted; microalgae cultivation was situated in a coastal area, resulting in seawater or brackish water being available as culture medium at no cost; mild summers and covered HRP design resulted in negligible water loss; gas turbine efficiency was not influenced by the presence of CO2 in the biogas mixture; 100% nutrient recovery was modeled in the microalgae production system. Functional Unit. In this study, the functional unit is defined as the delivery of an energy service of 1.0 TWh electricity to the grid; this is, by approximation, the residential electricity demand of a city of 500 000 inhabitants. System performance was calculated for a period of 1 year. System Overview. As depicted schematically in Figure 1, a natural gas power plant with combined cycle (NGCC), with or

Photosynthetic blue-green cyanobacteria Spirulina (Arthrospira platensis), abusively called “microalgae” in this study, was chosen as model organism. Spirulina thrives best at temperatures of 35−37 °C and a high pH of 10−11.22 It tolerates high saline concentrations23 and occurs naturally in alkali salt lakes,22 allowing the use of seawater or brackish water for cultivation.24 Because of the filamentous nature of Spirulina, with single cylindrical cells being organized into multicellular trichomen up to 1 mm in length,22 microstraining was shown to be an effective downstream harvesting step.25,26 It is crucial to stress that microalgae mass production facilities of any significant magnitude currently do not exist and that the theoretical biomass production rates of any prospective microalgae facility can only be approximated at best. Since experimental data on HRP microalgae cultivation are still scarce, irradiation-dependent microalgae productivity was estimated based on three independent experimental HRP data sources27−29 (Figure 2).

Figure 1. Schematic representation of the microalgae production cascade analysis.

without carbon capture and storage (CCS) technology, serves as carbon feedstock supplier, resulting in CO2 being transported either as flue gas or as refined CO2. Biomass is produced by microalgae cultivation in covered high-rate ponds (HRPs), harvested by sedimentation and subsequent microstraining. The obtained algal slurry is fed into a wet anaerobic digestion system of continuously stirred tank reactor (CSTR) design. The digestate, which is rich in essential nutrients and organic carbon, is finally used as high-quality biofertilizer surrogate, replacing energy-intensive industrial fertilizer. The reference biogas production system is based on existing maize agriculture, according to published methods.14−18 Maize biomass is digested using dry anaerobic digestion of plug-flow design, allowing for ∼70% and 100% nitrogen and phosphorus recycling, respectively.14 System boundaries are determined for one annual process cycle, including the carbon flows of all feedstock and products, providing 1.0 TWh of electricity to the grid. The energy life cycle ignores energy inputs related to system materials and infrastructure and focuses on material flows within one cycle. Mass Cultivation of Microalgae. In the current study, microalgae cultivation is performed in a prospective massculturing facility consisting of covered HRP raceways with a depth of 30 cm and a total solar collection area of 29 ha per pond, being 35 times larger than the largest HRPs ever built19yet still conservative and being a factor 3 smaller than a pond-size estimate, according to a recent engineering feasibility study focusing on wastewater treatment by Lundquist and co-workers.20 Ponds are lined with poly(vinyl chloride) (PVC) and covered with high-transmission low-density polyethylene (LDPE) foil.21

Figure 2. Dependence of microalgal areal productivity, in grams dryweight per day per m,2 on the daily amount photosynthetic active radiation (PAR, expressed in units of kWh m−2 d−1). Based on temperature-corrected data at 20 °C from refs 27, 28, and 29.

Microalgae growth is temperature-dependent and productivity was temperature-corrected, according an empirical equation.30 Next, to illustrate the fact that microalgae growth is light-limited in northern Europe, data points were reduced by applying a saturation kinetics Monod-like function.31 Annual solar irradiation and maximal daily temperature data for northern Germany (i.e., the city of Bremen) were obtained from the European Joint Research Centre Institute for Energy32 (Table 1), with cosine best-fits being used for further calculations. Using the relationship obtained in Figure 2, monthly microalgae yield (t dw ha−1 m−1) was estimated based on irradiation and temperature data. It should be noted that this estimate exclusively applies to covered HRP cultivation of microalgae at a depth of 30 and at an optimal density of ∼0.37 g L−1, based on refs 33 and 34, and paddle-wheel mixing at a 3883


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heterocyst cells are capable of nitrogen fixation, N must be supplied externally during cultivation, because of the fact that nitrogen fixation significantly reduces growth.55,56 Harvesting of Microalgae. Microalgae thrive best in dilute cultures, because of intrinsic photoinhibition and self-shading.57 This dilute nature of the microalgae culture, with an optimum being observed at 0.37 g L−1 in field-scale HRP cultivation,33,34,58 results in vast amounts of culture medium that must be handled. The first harvesting step consists of so-called “lamellar sedimentation”, resulting in an ∼50-fold higher cell density of 16.7 ± 0.29 g L−1 (1.7% w/v).25,26,40 Next, the microalgal suspension is further concentrated by vibrating microscreens, yielding a microalgal slurry of 45.0 ± 1.3 g L−1 (4.5% w/v).25,26,34 The sedimentation harvesting step is energy-demanding, since it mostly involves pumping large volumes of dilute culture medium, because of the very low biomass-to-water ratio (the average reported electrical energy demand is 367 ± 153 Wh m−3).26,58,59 The subsequent microscreening step processes an ∼50-fold lower culture volume and requires an electrical energy input of 9.5 ± 4.8 Wh m−3.25,26,60 In tandem, these downstream processing technologies achieve a recovery of 90%−95%.25 Anaerobic Digestion of Microalgae. The protagonist role of anaerobic digestion (AD) as an efficient energy and nutrient conversion system in industrial biomass-based energy production cascades will be outlined in this section. Following two-step harvesting, the obtained microalgal slurry contains enough total suspended solids (4.5% w/v TSS) to be further processed using wet AD, with the continuously stirred tank reactor (CSTR) being the most common configuration for lowTSS (2%−10% w/v) substrates.61 Although a comprehensive AD description is beyond the scope of this study, AD allows for the degradation of polymeric organic substrates and is a complex process, involving various groups of micro-organisms catalyzing three consecutive steps. First, the enzymatic, albeit rate-limiting in the complete AD cascade, hydrolysis of complex (polymeric) organic compounds, producing sugars and amino acids, followed by their rapid conversion into volatile fatty acids and, subsequently, acetic acid (also known as acidogenesis and acetogenesis, respectively). Finally, methanogenesis results in the formation of CH4 and CO2 (i.e., biogas, metabolic water, and other constituents such as NH3 and H2S, depending on the elemental composition of the substrate).62 In contrast to the industrial scale presented here, the use of microalgal biomass as the sole AD substrate has so far only been demonstrated in bench-scale experiments,63−65 with recent confirmatory studies reporting similar results.66,67 Importantly, experimental CH4 yields are presented in this study and theoretical estimates were ignored to avoid overestimation of biogas production.68 On average, the AD process is able to digest 73.7% ± 9.6% of the microalgal biomass17,69,70 at an hydraulic retention time (HRT) of ∼1 month, yielding experimentally validated CH4 and CO2 outputs of 350 ± 49 and 152 ± 21 Nm3 CH4 and CO2 per tonne of volatile solids (VS), respectively.64,65,71 VS constitute 88.0% ± 1.4% of the microalgae TSS.64,65 The retention and separation of nutrients from the gaseous CH4 and CO2 output streams in AD biomass conversion is of prime importance for the sustainability of biofuel production cascades. Because of the fact that microalgae have a considerably lower C/N ratio, compared to plants (∼7 vs 37), microalgal biomass AD results in a significant formation of ammonium ions (NH4+). With the aid of the empirical Buswell

Table 1. Average Solar Irradiation and Temperature Data for the City of Bremen, Germany (Obtained from the European Union Photovoltaic Geographical Information System102), Calculation of Photosynthetically Active Radiation (PAR) (According to ref 103), and Estimation of Monthly Microalgae Dry Weight (dw) Yield Per Month per ha, based on Figure 2 month January February March April May June July August September October November December

daily solar input (Wh m−2 d−1 PAR)

daytime temp (°C)

270 2.3 720 3.8 1020 5.8 1620 10.1 2520 14.2 2595 16.8 2370 19.1 1950 19.6 1305 16.2 795 11.8 345 6.5 240 2.7 April−September microalgae production:

monthly microalgae yield per ha (t dw ha−1 m−1) 0.10 0.40 1.04 2.13 3.62 4.95 5.21 4.01 2.16 0.75 0.15 0.04 22.07

flow rate of 15 cm s−1,35−37 demanding an electrical process energy of 2.39 ± 0.83 MWh ha−1, based on refs 35 and 38−40. Upstream Feedstock Requirements of Microalgae. Feedstock requirements were estimated based on a reported elemental composition of microalgae: C1.00H2.04O0.64N0.13P0.01,6,41,42 yielding 1.66 t CO2 per tonne microalgae dry weight produced. Carbon dioxide is supplied to the microalgae system by a modern (1996) NGCC power plant (Unit “EC-7” of the “Eemscentrale”, in The Netherlands, rated at a capacity of 341 MW). In 2006, this NGCC had an electric efficiency of 52.5% and delivered 2.04 and 1.67 TWh electricity and heat, respectively, firing 4.43 × 108 Nm3 of natural gas (equaling 3.89 TWh, i.e., a power plant efficiency of 95%). In 2006, this NGCC emitted 7.8 × 105 tonnes of CO2 into the atmosphere.43 Power plant flue gas, containing ∼13% v/v CO2, is transported to the HRP cultivation site using blowers. The pumping distance was based on the areal requirements of microalgae cultivation, as discussed below. The blower power requirement is 13.1 ± 2.8 kWh t CO2−1 km−1 (refs 11, 40, and 44) for flue gas as is. Alternatively, flue gas CO2 is first captured using CCS technology, resulting in a power plant electrical power output reduction of 18.2 ± 5.0%,45−47 corresponding to, in the case of the natural gas power plant chosen for this study, 474 kWh t CO2−1 (at annual electrical power and CO2 outputs of 204 GWh and 7.8 × 10 5 tonnes, respectively).43 Subsequently, the concentrated CO2 stream is transported to the site of microalgae cultivation, requiring 2.04 ± 0.26 kWh t CO2−1 km−1.48,49 A minor part of microalgae carbon demand is met by seawater dissolved inorganic carbon.50 Nitrogen (N) and phosphorus (P) upstream feedstock requirements during cultivation are reported to amount to 100.3 ± 9.5 and 10.9 ± 1.6 kg per tonne microalgae dry weight, respectively.6,22,42,51,52 In case N (supplied as urea or ammonium) and P (supplied as superphosphate or diammonium phosphate) originate from external sources, the production of 1 kg of N and P requires 13.7 ± 0.34 and 3.44 ± 0.19 kWh, respectively.18,52−54 Of note, although Spirulina 3884


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Figure 3. Sankey diagrams of carbon (A) and energy (B) flows of microalgae production for the provision of an electrical energy service of 1000 GWhel to the grid. Internal carbon flows, in units of 103 t C a−1, are shown, including external seawater inorganic carbon. Energy inputs and outputs of unit operations from and to the grid, respectively, are indicated in GWh a−1. Estimation of microalgae biomass caloric value was based on ref 104. The required energy input associated with mineral fertilizer production is shown as a gray arrow, being matched by the energy embedded in the digestate of anaerobic digestion (AD) as biofertilizer. Solar irradiation input flow was omitted from this graph for the sake of clarity.

formula,72 later modified by Boyle to include phosphorus (P) and sulfur (S),73 theoretical NH4+ formation can be estimated. Based on the elemental composition of microalgae, AD will yield ∼91 g of NH4+ per kg of algal biomass digested, which is consistent with observed NH4+ concentrations in the liquid digestate after 28 days.65,66 To date, only one report addresses P recycling using AD, wherein 100% is recovered in the AD digestate and residual sludge.59 In the prospective microalgae cultivation system, 100% N and P recovery is modeled. AD is a downstream processing step of relatively low energy intensity; the electrical and thermal energy demand of CSTR systems is rated at 30.9 ± 10.4 and 30.9 ± 4.7 kWh per tonne dw of microalgae biomass stream, respectively.15,17,18,74 Biogas Production Using Maize as a Reference System. Maize silage-based biogas production is a welldocumented process and, briefly, the production cascade consists of (1) field preparation (transport and spreading of digestate or fertilizers, ploughing, and crumbling); (2) sowing; (3) pesticide application; (4) harvesting and transportation; (5) silo compaction; (6) AD feeding; and (7) digestate transportation.18 The combined energy input for the maize agriculture production cascade is 2.92 ± 0.38 MWh ha−1.17,75 Because of climate- and regional-dependent productivity variances, the average maize areal yield in northern Europe is ∼10.8 ± 1.8 t dry matter ha−1.16,17,75,76 Maize cultivation is an

open system resulting in significant upstream feedstock (i.e., nitrogen, phosphorus, and potassium (NPK)) fertilizer losses. Fertilizer runoff is estimated at ∼35.0 and ∼0.5 kg ha−1 of nitrogen and phosphorus, respectively.14 Including these losses, maize cultivation requires 144.7 ± 9.1, 55.7 ± 12.1, and 89.3 ± 18.8 kg ha−1 of nitrogen, phosphorus, and potassium, respectively.18,53,77 The production of 1 kg N, P, and K, requires 13.7 ± 0.34, 3.44 ± 0.19 and 1.94 ± 0.19 kWh, respectively.18,52,53 The plug-flow AD process has electrical and thermal energy demands of 29.0 ± 2.1 and 27.2 ± 4.7 kWh per tonne dry-weight of maize biomass, respectively.17,74 Data Analysis and Statistics. Reported data are presented as arithmetic means ± standard deviation (SD). Energy and carbon flow analysis was performed using STAN 2.0 (Inka software, Institute for Water Quality, Resource and Waste Management, Technical University, Vienna, Austria).78

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RESULTS AND DISCUSSION Based on the detailed engineering model of industrial-scale biomethane production cascades using microalgae or maize as substrates, it is now possible to analyze and compare the energy life cycle and land area demand. Estimation of Microalgae Productivity in Northern Europe. Figure 2 shows microalgae growth rates based on 3885


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processed data from refs 27, 28, and 29, cultivated in HRP with a depth of 30 cm, at various locations worldwide. Relevant for the microalgae production cascade under study is the quasilinear range observed up to ∼2.5 kWh m−2 d−1. A best-estimate for monthly microalgae production can now be constructed based on average solar irradiation and daytime temperature data for northern Germany (see Table 1), resulting in a peak monthly dry-weight areal productivity of 5 tonnes per ha during the months of June and July. Excluding the colder period from October until March as cultivation period, the total annual microalgae biomass production is estimated at 22.1 t dw ha−1 a−1 (or 12.3 g dw m−2 d−1, assuming a cultivation period of 180 days) (see Table 1). This yield estimate for the northern Germany location exclusively applies to microalgae cultivation at a cell density of ∼0.37 g L−1 using covered HRP technology with a depth of 30 cm and a mixing rate of 15 cm s−1. Carbon and Energy Flows of Industrial-Scale Microalgae-to-Biogas Unit Operations. Figure 3A shows the results of a carbon flow analysis for the production of biogas, using covered HRP microalgae cultivation, coupled to a centralized NGCC power plant delivering an electrical energy service of 1.0 TWh (and concomitantly 0.91 TWh of heat). The carbon conversion of AD yields similar carbon downstream outputs for CH4 and digestate flowsmainly due to the fact that nearly 25% of the microalgae biomass substrate is not degraded during AD. Of note, intensive research into the digestibility of micro-organisms has identified cyanophage lysis80 as an elegant, albeit speculative, DSP step with low process energy demand.81 Although minor discrepancies are observed in the carbon balances of individual unit operations, due to inherent inconsistencies in volume to mass conversions, upstream carbon requirements of microalgae are almost exclusively covered by CO2 recycling (Figure 3A). Obviously, field-scale operation will not allow for 100% conversion efficiencies for individual harvesting and recycling steps, likely resulting in a higher demand for external carbon input. The current prospective microalgae-to-biogas cascade requires a minor external carbon input as inorganic seawater bicarbonate. In Figure 3B calculated energy flows are shown. The total system electrical energy input for blower operation, paddlewheel mixing, lamellar sedimentation, microscreening, and digester operation is estimated at 327 GWhel (Table 2), requiring 606 GWh of primary energy, based on an electric efficiency of 52.5% of the NGCC power plant used in this study. This results in a NER of 3.15 with heat utilization (1000 GWhel + 906 GWhth provided). Harvesting of microalgae biomass represents the most energy-intensive step, because of the dilute nature of a microalgae culture: handling 1.5 billion m3 of culture medium requires an energy input of 165 GWhel. An additional energy-intensive unit operation in the paddlewheel mixing of the HRPs, rated at 63 GWhel. The delivery of NGCC flue gas requires 63 GWhel and strongly depends on transport distance. This implies that biogas firing should take place in close proximity to the site of microalgae cultivation, thereby minimizing biogas and flue gas transport. Alternatively, CCS technology can be employed to first capture CO2 first, followed by transport to the site of microalgae cultivation. However, this configuration would result in a significant increase in process energy, mostly due to the energy-intensive CCS step, lowering NGCC electrical efficiency; in the system under study, this would represent 182 GWhel. Furthermore, 10 GWhel would additionally need to be added for CO2 pipeline transport. Hence, equipping power plants with CCS technology

Table 2. Carbon and Energy Flow of Microalgae Production, with Centralized (NGCC) Power Generation, for an Electrical Energy Service of 1000 GWhel to the Grida unit operation Power plant CH4 CO2 electricity heat efficiency losses Flue gas delivery blower operation Microalgae cultivation CO2 nitrogen

carbon (tonnes)

reference(s) 43

−9.02 × 104 +9.12 × 104

−1906 +1000 +906 +100 −63

−13.0 × 104 −804 −22

phosphorus fermentable carbon seawater bicarbonate paddle-wheel mixing microalgae biomass Harvesting lamellar sedimentation microscreening Anaerobic digestion, AD microalgae biomass digester operation CH4 CO2 digestate nitrogen phosphorus

energy (GWh)

−10.1 × 104

11, 40, 44

69 6, 18, 42, 31, 32, 34 6, 18, 31, 32, 34, 42 17, 69, 70

−3.35 × 104 −63 +26.5 × 104

−26.5 × 104

+2488

calculated

−152

26, 58, 59

−13

25, 26, 60

−2448

calculated

−36 +9.02 × 104 +3.85 × 104 +10.1 × 104

Total energy input (GWh):

35, 38, 39, 69

15, 17, 18, 74

+2006 +275 +537 +15 327

64, 17, 72, 72,

65, 71 69, 70 73 73

a

Estimation of the microalgae biomass caloric value was based on ref 104. Annual energy plus carbon inputs and outputs of individual unit operations are indicated with a minus sign (−) and a plus sign (+), respectively.

is only of interest when long-distance CO2 transport is required. In both cases, CO2 feedstock supply can be regarded as energy-intensive, rated at 13.1 ± 2.8 and 2.04 ± 0.26 kWh t CO 2 −1 km −1 for flue gas and purified CO 2 , respectively.18,43,48,52,53 Hence, the use of power plants and carbon suppliers, appearing beneficial at first, from an environmental point of view, should thus be treated with caution for industrialscale systems. Indeed, this energy-intensive delivery of CO2 as upstream carbon feedstock was identified in this study, but ignored in other life-cycle studies.13 A proposed solution is the use of wastewater as organic carbon, nitrogen, and phosphorus feedstock, which, in essence, would represent the solar-energydriven bioconversion of one (waste) biomass into another.12,20,82 Whether this workaround will ever be economically viable remains questionable as long as the output stream provides little added value to the initial waste feedstock. 3886


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intrinsic demand for N and P, microalgae industrial scale cultivation is successfully being applied for the treatment of wastewater streams.90 Albeit favorable in the latter scenario, in case N and P feedstock need to be produced externally, upstream feedstock requirements apparently become the main driver in setting total microalgae cultivation process energy demand. Alternatively, high biocatalytic capacity of microalgae may be exploited to produce biohydrogen by water splitting.91,92 Importantly, such a system would not merely supply biomass for AD and, hence, would avoid the continuous destruction of precious biocatalytic machinery: the microalgae cells. As such, the process energy for microalgae biomaintenance93 can be minimized. Land Displacement by Microalgae and Maize Cultivation. Because of the expectation that microalgae biomass production rates will be higher than maize, an important advantage of microalgae is the predicted reduced impact on available global land surface.7 Total areal requirements of both biomass production systems for the provision of 1.0 TWhel were calculated and would initially require 2.7 × 104 and 4.9 × 104 ha for the microalgae and maize system, respectively. Such areal requirements are certainly impressive and, for example, would exceed the total area of all greenhouses in The Netherlands, being roughly 1 × 104 ha.94 If these systems are to operate independently from fossil-fuel inputs, additional process energies of 466 and 259 GWhel, respectively, would need to be provided. Moreover, the delivery of 1.0 TWhel electrical energy service, and the above-mentioned process energy, would result in the cogeneration of 1.33 and 1.14 TWh heat for microalgae and maize production, respectively. Based on calculated NER values of 3.15 and 4.87 for microalgae and maize biomass production, respectively, total surface requirements would reach 3.9 × 104 and 6.2 × 104 ha, respectively. Keeping in mind that the total surface area of available arable land in Germany amounts to 1.7 × 107 ha,95 a city of 500 000 inhabitants would be “entitled” to 1.1 × 105 ha; taking these area limitations into consideration gives microalgae biomass production a clear advantage over maize, because it requires 35% less land area. Possible Limitations of This Study. The clear and obvious limitation of this study is the comparison of a prospective with an established biomass production system. There are two ways to obtain a best estimate of a prospective microalgae industrial-scale production system. First, a top-down approach that, to the best of our ability, extrapolates the actual biomass output of existing microalgae production plants to northern European climate conditions (this study). Alternatively, a so-called “bottom-up approach” can be applied, based on the intrinsic biological properties of microalgae, such as photosynthetic efficiency and photo inhibition. Followed by lumping these smaller bits of information together in an effort to finally predict likely productivity of such a reconstructed microalgae cultivation system.96 Obviously, neither of the two approaches is able to predict exactly how industrial-scale microalgae production will perform. Indeed, so far, only one microalgae mass cultivation facility has been in operation: it was financed by the U.S. Department of Energy Aquatic Species Program from 1978 to 1996 and was dedicated solely to the production of biofuel. However, day-to-day operation resulted in algal monocultures being reliably maintained for no more than a few weeks or months.38 Note that the analysis presented here represents a rather optimistic overall appraisal. Downstream processing steps

As shown in Table 2, the production of mineral fertilizer as upstream input for microalgae cultivation would require 826 GWh of energy in the prospective microalgae production cascade. To reduce this fertilizer-related energy input, the impact of N and P recovery using AD was explored, providing biofertilizerwith recent reports supporting the use of AD digestate as biofertilizer.83,84 However, important prerequisites would need to be fulfilled, in that the operation should be continuous with slurry output being applicable as biofertilizer in agriculture. Although the bioavailability of N and P in microalgae digestates has been questioned by Clarens et al.,85 based on results obtained using sewage sludge as biofertilizer,86 a more recent study reported promising results using microalgae digestates.83 However, at an industrial scale, system operation most likely will not be closed and may therefore result in a significant release of greenhouse gases (e.g., CH4 and N2O). Sensitivity Analysis of Microalgae Productivity, Lipid Content, and Nutrient Recycling. As shown in Table 3, Table 3. Effects on System NER of Nutrient Recovery as Biofertilizer, Increased Areal Microalgae Productivity, and Lipid Content (and Concomitant Biomethane Increase)a Lipid Content (% w/w) productivity (t dw ha−1 a−1)

7 (0.35)

14 (0.39)

28 (0.47)

with nutrient recovery

22.1 (realistic) 44.2 88.4

3.15 3.85 4.45

3.59 4.37 5.02

4.48 5.43 6.18

without nutrient recovery

22.1 44.2 88.4

0.89 0.94 0.97

1.00 1.06 1.08

1.22 1.29 1.33

a Value in units of Nm3 CH4 t−1 shown in parentheses. Heat utilization is assumed.

modeling a 4-fold or 2-fold higher microalgae areal productivity, as a future possibility when using more-advanced cultivation systems, as reviewed extensively in ref 87, has little impact on system NER, mainly due to a corresponding increase in N and P feedstock. To explore the impact of microalgae biomethane yield on AD, the lipid content was set 2 and 4 times higher, as observed under normal growth conditions (∼7% w/w).68 Higher lipid content increases the caloric value of microalgal biomass and, concomitantly, improves the biomethane yield per kg VS during AD, estimated at 0.39 and 0.47 L CH4 kg VS−1 for microalgal contents of 14% and 28%, respectively, vs. 0.35 L CH4·kg VS−1 at 7% w/w lipid6,29,68,88 (see Table 3). Note that microalgae also contain significant amounts of carbohydrates, yielding additional CH4 upon AD.89 However, by comparison, the impact of increased productivity and/or lipid content on system NER is minor when being compared to nutrient recovery. Indeed, it is ultimately the energetic input associated with N and P feedstock that sets the system NER. As shown in Table 3, by setting both productivity and lipid content 4-fold higher, the system NER does not exceed 1.33, in case nutrient recovery is omitted. Maize and microalgae cultivation strongly deviate in this respect, because of their intrinsic differences in C/N ratio (∼37 vs ∼7, respectively). Hence, fast microalgae growth, favoring them as solar-energy-harvesting organisms over maize, is achieved by the high cellular protein content. Because of this 3887


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with) combined cycle; PAR, photosynthetic active radiation; TSS, total suspended solids; VS, volatile solids

(DSP), which have been reported to be highly energyintensive,40 such as lipid extraction using hexane and culture medium dewatering using centrifugation as the preceding DSP step, were omitted from the biofuel production cascade by opting for AD instead. The current study focuses on the energy inputs related to feedstock streams required for the production of microalgae or maize biomass, such as CO2, N, and P, not the energy input related to the production facilities of the abovementioned biomass cultivation. As an example, the energy content of LDPE foil, as a cover for the HRPs in this study, considering a thickness of 100 μm and a lifetime of 5 years, will require an energy input of ∼100 GWh per year.97 However, including all energy inputs related to biomass production may obscure the impact of individual unit operations, such as CO2 delivery13 and fertilizer demand.98 In conclusion, an important aspect one must keep in mind concerning renewable energy is scale. Any newly developed renewable energy source that intends to have any long-lasting impact as an energy resource whatsoever, will need to fulfill the requirement of reliably providing vast amounts of energy, as required by modern-day metropolises. With the help of lifecycle analysis, nonrenewable and energy-negative systems that apparently function well in benchtop-scale format can easily be identified when they are scaled up to an industrial scale.99 The impact of scale can be exemplified by the fact that microalgae cultivation is faced with a rather odd dilemma, in that evolution has resulted in microalgae that thrive best in a light-limited environment. This has resulted in photosynthetic efficiency of microalgae being highest under light-limited conditions and declining rapidly at light intensities that approach full sunlight.57 Although it is possible to dilute light intensity using intensive mixing in photo bioreactors,100 at an industrial scale, this is not considered very promising.35,98,101 Finally, when focusing on the extraction of energy from biomass only, thereby neglecting the importance of closing material cycles, as shown in this study, new shortages in valuable finite resources will eventually arise for which there will be no future substitute. Hence, the development of sustainable biofuels production systems should move beyond energy as a single-system performance indicator and should rather evaluate biofuel systems as a whole, concerning all material flows involved during its complete life cycle.

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AUTHOR INFORMATION

Corresponding Author

*Tel.: +49 234 32 24535. Fax: +49 234 32 14322. E-mail: [email protected]. Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS I am indebted to Professors Stefan Bringezu (Material Flows and Resource Management, Wuppertal Institute) and Matthias Rögner (Department of Plant Biochemistry, Ruhr−University Bochum) for valuable discussions and a critical reading of the manuscript.

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ABBREVIATIONS: AD, anaerobic digestion; CCS, carbon capture and storage; CHP, combined heat and power; CSTR, continuously stirred tank reactor; HRP, high-rate pond; HRT, hydraulic retention time; NER, net energy ratio; NGCC, natural gas (power plant 3888


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