Mass-Scale Algal Biomass Production Using Algal Biofilm Reactor

Research Article pubs.acs.org/journal/ascecg

Mass-Scale Algal Biomass Production Using Algal Biofilm Reactor and Conversion to Energy and Chemical Precursors by Hydropyrolysis Poonam Choudhary,†,‡ Anushree Malik,*,† and Kamal K. Pant‡ †

Applied Microbiology Laboratory, Centre for Rural Development and Technology and ‡Chemical Engineering Department, Indian Institute of Technology (IIT) Delhi, Hauz Khas, New Delhi 110016, India S Supporting Information *

ABSTRACT: A pilot-scale algal biofilm reactor (P-ABR) was assessed for its potential to provide a continuous supply of high volume algal biomass to be utilized as feedstock for hydropyrolysis. The half-year long performance assessment showed significantly high productivity of 15−20 g m−2 d−1 with uniform biochemical composition. Hydropyrolysis (HyPy) using ZSM-5 was used to convert and partition ABR-grown algal biomass components into energy-rich biocrude (HyPyO), nutrient-rich aqueous condensate (HyPyA), carbon-rich solid residue (HyPyS), and gases. The effect of temperature on yield and composition of different HyPy products was quantified in terms of carbon and nitrogen recovery. The maximum yield of biocrude was 31% at 200 °C and decreased to 18% with an increase in temperature up to 300 °C. The influence of temperature on recovery of nitrogen showed preferential accumulation of nitrogen in the aqueous phase with increasing temperature. The highest carbon recovered was 41% in the form of biocrude (HyPyO) at 200 °C followed by 31% in HyPyA at 300 °C. In the context of energy and nutrient recovery potential of each of the HyPy products, applications of different fractions was explored for development of a sustainable algal biorefinery. KEYWORDS: Algal biofilm reactor, Performance assessment, Hydropyrolysis, Nutrient recovery, Algal biorefinery

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researched to convert biomass into bio-oil and biochar.8,9 In spite of high biomass conversion efficiency (70%), huge energy requirements make it economically and energetically limited.10 However, processes like anaerobic digestion and hydropyrolysis convert wet biomass into biogas and biocrude, respectively, at low to moderate temperature conditions. While algal biogas production is economical, incomplete biomass conversion and loss of protein as ammonia leads to less energy output. Unlike conventional pyrolysis, hydropyrolysis (HyPy) operates at moderate conditions and converts whole algal biomass into biocrude (30−50% of dry feedstock) with a relatively high heating value (25−35 MJ/kg), solid residue, a gaseous mixture (N2, H2, CO2, CO, CH4), and an aqueous product rich in organics.11,12 Among all physical parameters affecting the yield and composition of hydropyrolysis products, reaction temperature is considered to be a critical parameter for organic conversion with hot-compressed water.13 Since severe reactions favor decarboxylation, cracking, steam reforming, and gasification reactions of liquid/char intermediates with the formation of gaseous products, selection of temperature range

INTRODUCTION Microalgae have been indicated as robust potential alternatives to traditional resources due to their ability to be used as a feedstock for not only a variety of biofuels but also other valueadded chemicals. The commercialization of microalgal biofuels, however, has been hampered by the high cost of production and subsequent harvesting with inefficient bioconversions.1,2 Recent attempts have been toward developing alternate cultivation systems in the form algal biofilm systems with facility of in situ harvesting.3 A number of successful systems like the algal turf scrubber (ATS) and rotating algal biofilm reactor (RABR) have been reported to produce high biomass productivities (10−30 g m−2 d−1) and avoid energy intensive processes to produce dewatered feedstock for biofuels.4,5 Although a number of lab-scale systems have been developed and tested, research on pilot-scale algal biofilm systems for production of biofuels are still limited. Even if the harvesting and low productivity limitations are addressed using algal biofilm systems, there remains a significant gap in efficient biomass conversion into biofuels.6 Most of the algal biomass conversion methods involve concentration and drying of biomass, especially for biodiesel and bioethanol.7 Recently, a high temperature and pressure conversion method such as fast pyrolysis is being increasingly © XXXX American Chemical Society

Received: January 21, 2017 Revised: March 8, 2017 Published: March 22, 2017 A

DOI: 10.1021/acssuschemeng.7b00233 ACS Sustainable Chem. Eng. XXXX, XXX, XXX−XXX

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ACS Sustainable Chemistry & Engineering is important to obtain the desired HyPy product.14 Moreover, selection of the appropriate catalyst can reduce the temperature and pressure of the reaction as well improve the quality of biocrude produced. The presence of deoxygenation catalysts such as zeolites favors degradation of algal biomass into long chain hydrocarbon and/or aromatic range compounds.15 In view of the above reports, research on algae needs to be focused on improving biomass cultivation, harvesting, and subsequent biomass conversion. In this context, the current study presents a novel integration of algal biofilm production and direct conversion of wet algal biomass into biocrude and coproducts by hydropyrolysis. Additionally, long-term assessment of a pilot-scale algal biofilm reactor (P-ABR) was also part of the study to ensure the durability and sustainability of the system for continuous availability of biomass to produce biofuel precursors and chemicals. The applications of each of the coproducts have been explored for maximum recovery by recycling of nutrients.

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months. The uniformity in nature of biofilm was determined by microscopic analysis. The homogeneity of algal biomass (in terms of ultimate analysis) obtained after every two harvests was confirmed statistically by single factor ANOVA. Feedstock Preparation and Characterization for Hydropyrolysis. To prepare feedstock for hydropyrolysis, algal biomass was harvested by manual scraping. The harvested biomass from different cycles of cultivation was collected and stored at 4 °C until use. The wet algal biomass slurry was prepared with the addition of water in a ratio of 6:1 (water/biomass) and subsequently used as feedstock for hydropyrolysis experiments. The remaining biomass was dried in an oven at 80 °C for 24 h and stored in a moisture-free environment for assessment of elemental composition of algal biomass. Volatile solids (VS) and ash content of the algal biomass were calculated through an EPA Method. The ash content was measured as weight fraction after combustion at 550−600 °C for 6 h. The elemental composition in terms of nitrogen, carbon, and hydrogen (in % wt/wt sample) was determined using an elemental analyzer (vario EL III, Elementar Analysen systeme GmbH), and oxygen was calculated by difference. All measurements were repeated in duplicate, and a mean value is reported. As a part of structural characterization, a thermogravimetry− differential scanning calorimetry (TGA−DSC) analysis of the algal biomass was performed using a TGA-Q600 instrument (supplied by TA Instruments Waters-LLC, USA) with an air flow of 100 mL/min from 25 to 900 °C at a heating rate of 10 °C/min. Hydropyrolysis Experiment. Hydropyrolysis experiments were carried out in a custom-made 1 L stainless steel (SS-316) stirred reactor with a maximum operating temperature of 450 °C and a maximum pressure of 5.9 MPa.16 The temperature control was provided by a jacketed furnace and coiled tube. A condenser combined with a chiller is attached at the outlet of the reactor to condense the vapor. The noncondensables were collected in the glass pipette from which gas samples were taken for analysis. The whole reactor assembly was connected to a PID controller which was used to maintain temperature, pressure, and stirring speed. To start with, the reactor was charged with algal biomass slurry with a typical water to biomass (W/B) ratio of 6:1 and catalyst to biomass (C/B) ratio of 1:10 using a zeolite (ZSM-5). ZSM-5 was the powdered ammonium form (SAR = 55). The ZSM-5 was selected for the study due to its unique characteristics such as strong acid sites, medium pore size, and high silica−alumina ratio (SAR) for its catalyst activity toward cracking and aromatization which provides better aromatic yield than other zeolite catalysts.17 Once the algal slurry and catalyst were fed to the reactor, it was sealed. Then, the reactor was continuously charged with nitrogen until a constant desired pressure of 25 bar (kg m−2) was achieved. Pressure of the vessel was controlled by a back pressure regulator (BPR). The operational parameter being investigated was reaction temperature (150 °C −300 °C) while keeping other parameters (pressure, retention time, and W/B ratio) constant. The run time of 20 min was taken from the point the reactor reaches the final test temperature without including heat-up times. A stirring speed of 120 rpm was maintained for all the runs. The vapors formed during the run were passed through a horizontal shell and tube condenser, which was maintained at 2 ± 0.1 °C, and the condensable vapors were separated through a separation funnel into liquid and gas phases. The gas products were sampled through a gas collector pipette for analyzing the composition. After each run, the reactor was cooled to room temperature by pumping tap water through cooling coils located outside the reactor. For each run, at least two independent experiments were conducted, and the average values with standard deviations were reported. Product Separation and Quantification. After the reactor was cooled, the liquid condensate collected in a separation funnel was weighed and filtered. The slurry from the reactor comprised an aqueous and organic phase with solid residue and was recovered and subsequently filtered, separated, and weighed. The slurry was mixed with dichloromethane and filtered through Whatman filter paper (#1). The organic and aqueous layers were separated and collected as different product fractions. The separated and filtered aqueous fraction

MATERIALS AND METHODS

Long-Term Performance Assessment of P-ABR. The design of the pilot-scale algal biofilm reactor (P-ABR) unit was based on our previously reported lab-scale ABR3 with slight modifications to enhance biomass productivity and durability for long-term operation. The unit was constructed using an HDPE (high density polyethylene)made nutrient vessel (100 L), submersible water pump (Model-MSW 10), and a nonwoven spun-bond fabric as the biofilm support material. The nonwoven fabric was selected on the basis of high attachment efficiency, durability, and ease of harvesting as optimized in our previous studies. The fiber sheet of 1 m2 surface area was positioned in an inclined orientation at an angle of 19° to allow the gravitational flow of the medium into the nutrient vessel. A customized dripping system made of acrylic was positioned at the top end of the biofilm support to ensure uniform distribution of the nutrient medium over the biofilm support, recirculated by a submersible pump placed in a nutrient vessel. The system was operated under greenhouse conditions (T = 25−45 °C; light intensity: 50−60 μmol m−2 s−1). The light intensity was monitored daily, and any decrease in light intensity lower than the defined value was balanced with suitable LED lights. To begin, exponentially growing active algal consortium was inoculated in a nutrient vessel filled with 100 L of tap water media containing Na2CO3 (0.02 g L−1), NaNO3 (0.15 g L−1), and KH2PO4 (0.0125 g L−1). The unit was run for the first 12 days to establish the initial growth of algae on the surface of the biofilm material. Once the support material was uniformly covered with green thick biofilm, the biofilm was harvested by manual scrapping. The colonies remaining after harvest were used as inoculum for next growth cycle and so on. The performance of P-ABR was evaluated for a period of six months from spring (March−May) 2015 to summer (June−August) 2015 by measurement of biomass productivity and biofilm thickness. During this time, the biomass was harvested 24 times, once a week by manual scraping with nutrient replacement. The biomass productivity (g m−2 d−1) and biofilm thickness (μm) was measured after every harvest as mentioned in our earlier study.3 For measurement of biofilm thickness, harvested wet biomass was quantified volumetrically and expressed as V. Using the total volume of wet biomass (V) and the cultivation surface area (S), the algal biofilm thickness (t) was estimated as t = V/ S. To determine the dry weight of the harvested biofilm (W), it was dried at 60 °C for at least 24 h in an oven. The daily biomass productivity (P) was estimated as the ratio of the net dry biomass weight (W) produced over the total cultivation surface area (S), over the entire cultivation period Δt.

P=

W S × Δt

(1)

The temperature and pH of the system was not controlled and monitored to observe the stability of the system for a period of six B


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Figure 1. Biomass productivity and biofilm thickness of ABR grown biomass evaluated for a six month time period. was termed as HyPyA. The organic layer was passed over dry sodium sulfate to remove the remaining moisture and then filtered again. The solvent in the organic layer was evaporated in a rotary evaporator at room temperature, and remaining residue was collected, weighed, and named as HyPyO. The reactor was rinsed using dichloromethane, and the resulted suspension was filtered and added to the previously separated organic layer. The solid residue left on the filter paper was weighed, named as HyPyS, and kept for further analysis. The material balance for all runs based on different product yields was calculated. The gas yield was determined by the difference as described in reported studies.18,19 Additionally, the measurements were also confirmed by a soap bubble flow meter. All the yields were expressed on the basis of dry weight of algae used. All yields reported are the average values with standard errors of duplicate experimental results. The product yields were calculated using the following equations:

HyPyO (%) = organic fraction × 100/dry weight of algae

Preparation and Characterization for Hydropyrolysis section. Carbon and nitrogen recoveries for HyPy products were estimated according to methods described by Yu et al.30 Calculations for energy recovery in terms of higher heating value (HHV) of products with respect to HHV of raw algal biomass based on the Dulong formula were done as mentioned by Yu et al.30 The net energy return (NER) was calculated as the ratio of total energy output to direct energy input according to the equation20 below

NER = Eo/Ei

where Ei is sum of energy input associated with pumping required for algal cultivation (Ecul) and energy required in hydropyrolysis reaction (Ehypy). Energy required in hydropyrolysis was calculated by the equations described in Jena et al.19The energy associated with illumination is not being considered as developed ABR is a prototype to be used outdoors under natural sunlight. Here, Eo is the energy output as high heating value (HHV). All the reported values represent the mean values for two independent runs.

(2)

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HyPyS (%) = solid biomass fraction × 100/dry weight of algae (3)

HyPyA (%) = aqueous fraction × 100/dry weight of algae

(4)

Gas yield (%) = 100 − (HyPyO + HyPyS + HyPyA)

(5)

(6)

RESULTS AND DISCUSSION Performance and Efficiency of P-ABR. The performance of P-ABR was evaluated for six months with regular monitoring of the nature and thickness of biofilm. During the six months of operation, no replacement of biofilm support was required. As compared to the cotton fabric used by Gross and Wen,42 which deteriorated and needed replacement after six months of operation, the nonwoven fabric used in the study was more durable. The nature of the algal biofilm as observed microscopically showed consortia consisting of Chlorella and Phormidium (data not shown). With the development of biofilm and increasing thickness, the biofilm composition was found to be dominated by filamentous Phormidium species which remained consistent during six months. Apart from culture consistency, the pH of the growth medium showed variation ranging from 7.8 to 10.1 with biofilm growth. It was interesting to note that temperature of the medium did not exceed 35 °C even when the environmental temperature in peak summer reached up to 45 °C. This could be attributed to evaporative cooling due to constant pumping and flow of water over the biofilm surface. The long-term monitoring and measurement showed variations in biomass productivity from 16.8−20 g m−2 d−1. The thickness of the biofilm was constant with small variations (Figure 1). Although the biomass productivity varied during the six month period of the pilot operation, the variations were still

Qualitative Characterization of HyPy Products. The composition of gas products were analyzed using GC (Nucon series-5700) equipped with a carbosphere column, thermal conductivity detector (TCD), and argon as the carrier gas. The temperature of injector and detector were 120 and 150 °C, respectively. The chromatograms were recorded, and peak areas were calculated using WinAcds 6.2 software. H2, CO, CH4, CO2, and CO were identified from their retention time as obtained by gas chromatograph of a calibration mixture.16 To determine chemical composition of HyPyO, GC-MS equipped with a GC/MS clarus 500 fitted with an Elite 5-MS column (30 m length, 0.25 mm i.d., and 0.5 m film thickness) with helium as the carrier gas was used.18 The HyPyO sample was mixed with dichloromethane and injected with a no split ratio. The peaks were identified by comparison with mass spectra available at the NIST library. The aqueous phase was separated, centrifuged, and further filtered for nutrient analysis (NO3−N, total dissolved phosphate (TDP), total ammonical nitrogen (TAN), chemical oxygen demand (COD)) as described previously.3 The determination of pH measurements were done with a Hanna pH meter (Hanna pHep HI 98107). Total organic carbon was measured by a HACH persulfate method (Hach method 8039; detection limit 20−170 mg L−1). The elemental compositions of the organic, solid residue, and aqueous fractions were determined as mentioned in the Feedstock C


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Table 1. Characterization of Algal Biomass as HyPy Feedstock Obtained in Different Seasons in Terms of Ultimate and Proximate Analysisa ultimate analysis months March April May June July August a

N 5.23 5.31 5.21 5.23 5.27 5.27

± ± ± ± ± ±

proximate analysis

C 0.04 0.01 0.01 0.04 0.03 0.03

39.32 38.61 39.95 36.65 37.15 38.95

± ± ± ± ± ±

H 0.61 0.8 0.81 0.82 0.51 0.5

5.25 5.29 5.01 5.26 5.36 5.36

± ± ± ± ± ±

VS 0.03 0.04 0.04 0.07 0.03 0.2

86.7 85.2 84.8 85.8 86.1 85.4

± ± ± ± ± ±

Ash 0.7 0.6 0.9 0.5 0.4 0.8

13.3 14.8 15.2 14.2 13.9 14.6

± ± ± ± ± ±

0.2 0.1 0.3 0.4 0.2 0.2

All values are expressed as %TS (total solids). VS: volatile solids.

less as compared to other reported studies.21,22 The reason could be the simplified and durable design of P-ABR as compared to RBC used by Sebestyén et al.21 The inclined biofilm support and ease of harvesting algal biomass in P-ABR makes the system easy to operate with the least maintenance. Also, the simple design of P-ABR avoided the error due to manual handling or mechanical errors. Hence, P-ABR showed good efficiency in terms of biomass productivity with fewer challenges. Algal Biomass Characterization: Homogeneity and Thermal Stability of Algal Biofilm. The algal biomass harvested in different months was characterized to assess the variation in feedstock quality due to seasonal variations (Table 1). The investigation of the ultimate analysis of raw algal biomass for six months showed slight variation (insignificant difference, p > 0.05), indicating the stabilized nature of ABR and homogeneity in composition of algal biomass. With 86% volatile matter and appropriate elemental composition, ABR grown biomass was found to be a suitable feedstock as energy carrier (Table 1). In order to determine the temperature range for complete conversion of algal biomass and to analyze decomposition behavior, simultaneous TGA/DSC analysis was performed. The TGA and DSC curves of the tested algal biomass showed that around 65% of the biomass was lost when heated from 150 to 600 °C, attributed to decomposition of the principal components of the algal biomass (Figure S1). A similar decomposition trend was shown by Anand et al.8 when Spirulina was heated under identical conditions. The notable increase in decomposition was observed between 200 and 300 °C with maximum degradation, suggesting a suitable temperature range for maximum biomass conversion into pyrolytic products. With a further increase in temperature above 300 °C, biomass loss decreases due to an exothermic effect indicating the devolatilization. Temperature higher than 400 °C showed constant degradation. A further increase in temperature may lead to depolymerization and lead to char formation and less yield of oil fractions. The TGA test results were in agreement with the reported Chlorella species23 and other cyanobacteria8 which followed multiple-step degradation when heated from 100 to 600 °C. Effect of Temperature Variation on Product Distribution and Yield. This is the first study utilizing algal biofilm directly as a feedstock for hydropyrolysis at a lower temperature range (150−300 °C) than the temperature being used in conventional pyrolysis and hydrothermal liquefaction (450− 550 °C) of algal biomass obtained from suspended cultures. Although HyPy was operated for 20 min with moderate temperature and pressure, no change in quality of ZSM-5 after reaction was observed. In the present study, deactivation studies were not carried out; however, no change in catalyst

structure was observed after the reaction. The different product fractions obtained after HyPy reaction were separated and quantified. The variation in temperature showed significant effect on yield and distribution of different HyPy products as shown in Table 2. The total mass balance at different Table 2. Yield and Distribution of Different HyPy Products at Different Temperatures temperature (°C)

HyPyO (%)

HyPyA (%)

HyPyS (%)

gases (%)

150 200 250 300

21.8 31.0 24.3 18.0

29.2 30.42 24.45 19.35

42.3 30.1 41.4 41.5

6.7 8.48 9.85 21.15

temperatures varied from 86% to 90% which is comparable to reported studies.24 At higher temperatures, incomplete mass closure was dominant which is likely due to loss of water and volatiles.23 Results showed an increase in yield of HyPyO from 21% to 30% with an increase in temperature from 150 to 200 °C with highest value at 200 °C with a 20 min retention time. In a comparative assessment of catalyst type affecting biocrude yield from Chlorella biomass, Ross et al.25 reported a maximum yield of 27.3 (wt %) at 350 °C with 1 h reaction time. Chen et al.26 used mixed culture algae (mixture of microalgae, macroalgae, bacteria, and others) from a wastewater treatment plant and reported the maximum yield of biocrude as 49.9% at 300 °C with 1 h retention time. The biomass composition of algal biomass also critically affects the temperature and time required to degrade biomass by HyPy with a wide variation in yield of products.27 A significant decrease in HyPyO yield was observed as the temperature increased from 200 to 250 °C and then 300 °C, suggesting thermal decomposition of oil into fractions which is distributed in either solid or aqueous fractions. Jena et al.27 also observed an increase in yield of biocrude with an increase in temperature reaching a maximum of 39.9% at 350 °C which later dropped to 36.0% at 380 °C. A similar trend of variation in biocrude yield with an increase in temperature was observed by Chang et al.24 and Eboibi et al.28 However, none of the studies have reported a highest yield at low temperature (200 °C). With an increase in temperature from 150 to 200 °C, the yield of solid residue decreased due to conversion of biomass components into oily fractions in HyPyO. However, further increase in temperature increased the yield of solids up to 41%, possibly due to polymerization reactions leading to formation of char. This observation was also consistent with previous studies reporting variation in yields of HyPy products with temperature.29 Additionally, with an increase in temperature D


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Figure 2. Effect of temperature on carbon recoveries (a) and nitrogen recoveries (b) distributed in different hydropyrolysis product fractions.

Figure 3. Distribution of different compounds in organic biocrude fraction with variation in temperature.

from 250 to 300 °C, gaseous yield also increased from 9.8% to 21.1%. At lower temperatures, hydrolysis of polysaccharides and proteins to small molecules, followed by dehydration, deoxygenation, and decarboxylation reactions, converts more solid residue into biocrude (HyPyO). A further increase in

temperature could have decreased the hydrolysis rate and increased repolymerization reactions leading to degradation of biocrude into gases, as observed by a drastic increase in gas yield. Additionally, a decrease in yield of the aqueous phase from 24% at 250 °C to 19% at 300 °C was observed, indicating E


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Figure 4. Effect of temperature on COD, TOC, and TAN (a) and nitrate-N and TDP (b) concentrations in aqueous fraction of HyPy.

In contrast, the CR of the aqueous product initially increased with reaction temperature, but the value reached a peak of 39.7% at 250 °C, after which it started to decrease slightly. Figure 2a shows that more than one-third of the total carbon in the original untreated biomass was converted into water-soluble organic matter at temperatures above 250 °C, similar to reported studies.26,30 The recovery of nitrogen in different fractions is shown in Figure 3b. Most of the nitrogen was recovered in the aqueous fraction indicating the production of organic acids and amino acids by deamination reactions. The nitrogen recovery of HyPyO increased up to 200 °C and thereafter decreased at higher temperatures. The reason could be the degradation of amino acids at higher temperatures and formation of amides with other biomass degradation compounds. Above 250 °C, nitrogen recoveries in organics and solids reached a plateau and showed no variation (Figure 2b). At temperatures higher than 250 °C, the nitrogen content increased in gases and aqueous fractions, indicating a majority of denitrogenation and decarboxylation of protein hydrolysates into amines/ amides.24,31,32 The decreasing nitrogen content of HyPyO is favorable as fuel, and the increasing nitrogen content (amino acids, amides, amines) in the aqueous fraction is advantageous

higher organic conversion of water-soluble material into gases. Similar results of increasing gas yield and decreasing solid yield with an increase in temperature were reported for HyPy of Spirulina,27 Chlorella,24 and mixed culture algae biomass.26 Recovery of Carbon and Nitrogen in Different Product Phases. Temperature showed significant variation in carbon and nitrogen recovery in different HyPy products. The effect of reaction temperature on the carbon recovery (CR) in different fractions of hydropyrolysis, including HyPyO, HyPyS, and aqueous phase (HyPyA), is shown in Figure 2a. At a temperature of 150 °C, the CR value of solids was above 60%, which may be due to a high percentage of unreacted solids as evident from the green appearance of the resultant HyPyS. Furthermore, CR values decreased from 60% to 20% when the reaction temperature was increased from 150 to 250 °C. A simultaneous increase in CR of HyPyO was observed with maximum recovery at 200 °C (Figure 2a). Although the carbon content of HyPyO increased from 55.2% to 68.3% with an increase in temperature from 200 to 300 °C, lower yield at higher temperature led to less recovery at 300 °C. Yu et al.30 also reported an increase in CR of biocrude from 3.1% to 43.2% with a simultaneous decrease in CR of solids from 73.9% to 11.8% as temperature was increased from 180 to 240 °C. F


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recovery data in Figure 4a and b. With increasing temperatures, the COD and TOC values reduced from 9500 and 11,000 mg L−1 at 150 °C to 6000 and 5000 mg L−1 at 200 °C, respectively, also confirmed by distribution of CR in HyPyA. At temperatures above 250 °C, COD and TOC values again increases due to further degradation of HyPyO and partition of organic matter (CR) to aqueous fractions. Apart from high organic content, the aqueous fraction contained high nitrogen concentrations in terms of ammonia and nitrate in line with NR as shown in Figure 4b. The ammonia content (TAN) was found to be above inhibitory levels (2100 mg L −1 ) recommended for either anaerobic digestion or as the algal nutrient medium.24,26,31 The presence of ammonia precursors confirms the decomposition and deamination of amino acids. The high nitrogenous organics in the aqueous products rather than the biocrude oil is advantageous because less acid and nitrogen compounds require less upgradation steps for increasing the fuel value of biocrude. Although studies have been performed to recycle the aqueous fraction as an algal nutrient medium, most of these used very high dilution with distilled water36 or supplementation with additional nutrients.37 However, LCA studies by Patel et al.38 showed that nutrient cycling of the aqueous phase for cultivation has marginal environmental benefits than anaerobic digestion. Sustainable Applications of Biofilm-Derived Hydropyrolysis Products. The ABR-grown biomass hydropyrolysed under different temperature conditions showed variability in distribution and yield of different products. The overall characterization in terms of carbon recovery showed that most of the carbon was recovered in HyPyO (42%) at 200 °C and in the aqueous fraction (36%) at 250 °C. Around 17−30% of carbon recovery was observed in the solid residue (HyPyS). The highest energy recovery in HyPyO was 61% (at 300 °C) with an HHV value of 32 MJ kg−1, whereas other coproducts (aqueous and solids) showed maximum energy recoveries of 18−30%. Although the energy value and recovery of HyPyO observed in the study was found to be comparable with reported studies on mixed and pure algae,24,26,30,39 it needs further upgrading to be used as transportation fuels because of high oxygen and nitrogen contents.40,29 Although solids and aqueous fractions showed lower energy recoveries, nutrient recoveries were high enough to be utilized and recycled. The balanced carbon content (21−31%) of solids (HyPyS) is generally considered to be optimum to be used as biochar.18,41 Moreover, the high carbon content and improved C/N ratio (15) makes HyPyS a suitable candidate for biogas production. This additional energy output from biogas can offset the external heat and power input for the HyPy process. The net energy return was calculated to be 1.4, considering biocrude as the only energy output of the process. However, the energy balance of anaerobic digestion of algal biofilm showed a net energy return of 1.0 when grown in TAP media.3 The hydropyrolysis followed by anaerobic digestion can increase NER up to 2.5, which is toward the higher side of values reported for algal biofuels. Barlow et al.22 assessed the sustainability of hydrothermal liquefaction of biomass from a rotating algal biofilm reactor and reported a net energy ratio (NER) of 1.65 based on a well-to-product system boundary. The economic analysis of RABR and ATS by Gross and Wen42 and Pizarro et al.,43 respectively, have shown that although the capital cost for mechanized biofilm systems is much higher than that of open pond raceways (ORP) the high productivity with robust culture management in algal biofilm systems may lead to

for applications in extraction of chemicals and its precursors. The partitioning of nitrogen into the aqueous phase and carbon recovery in solid residue and gas fractions at higher temperatures showed feasibility of hydropyrolysis for the desired product with slight variation in process conditions. Molecular Composition of HyPyO. The molecular composition of HyPyO was done by GC-MS. Owing to the low volatility, only a fraction of HyPyO could be analyzed by GC. Thus, the data provided information for the volatile fraction and are not necessarily representative for the total HyPyO. The identification of compounds was done by computer matching with a mass spectral library. The identified compounds could be categorized into the following groups: fatty acids derivatives, heterocyclic compounds, cyclic oxygenates, and hydrocarbons. Their relative amounts at different temperatures are shown in Figure 3. It was observed that HyPyO produced at 200 °C contained mostly fatty acids derivatives, heterocyclic compounds, and branched amides formed by degradation of lipids, carbohydrates, and proteins, respectively. Some major compounds in the categories were hexadecanoic acid, piperidinone, dodecanamide, benzaldehyde, acetophenone, indole, and phenolic compounds. Above 250 °C, the fatty acids derivatives significantly reduced to 10%, while the saturated hydrocarbon and aromatics increased up to 34%, which is higher than reported studies on ZSM-catalyzed pyrolysis/hydropyrolysis of algae.15,31 Studies have also confirmed the advantages of zeolites for higher aromatic yield15,17 of bio-oil containing significantly low amounts of oxygen and nitrogen.8 Higher temperatures trigger further decarboxylation of fatty acid derivatives into hydrocarbons and recombination reactions to form cyclic oxygenates. The intermediate-formed amine groups start forming cyclic amine/amides at temperatures above 250 °C, which subsequently get distributed to the aqueous products as evident from nitrogen recovery of aqueous fraction. Although a decrease in nitrogen content of HyPyO was advantageous, a simultaneous increase in oxygen content due to cyclic oxygenates is not considered to be desirable. Moreover, heterocyclic compounds in HyPyO may be degraded and distributed to solid residues as reflected by its high carbon recoveries at higher temperatures. Overall analysis showed that although higher temperatures produce HyPyO with a high percentage of hydrocarbons, the yield was lower. Lower temperatures produced high yield of HyPyO but lower aromatic/heteroaromatic functionality. However, low pH of HyPyO formed by a ZSM-catalyzed reaction makes it unsuitable for direct application. Therefore, use of alkaline catalysts (Na2CO3 or K2CO3) is recommended to improve pH and quality of biocrude.19,33 These catalysts are reported to produce high yield of biocrude; however, the content is dominated by phenolic compounds with a less percentage of hydrocarbons as compared to zeolites.34,35 Characterization of Aqueous Phase (HyPyA). From nutrient analysis, high TAN and TOC values were observed in the aqueous phase. The pH values of the aqueous phases were determined immediately after completion of the reaction and were found to range between 5.6 and 6.0 due to the presence of organic acids. In a study, Chen et al.26 showed that organic acid content was one of the major products in the aqueous fraction, and content was increased with a further increase in temperature due to degradation of amino acids. The COD, TOC, TDP, and nitrate-N measured in aqueous samples produced at different temperatures were compared with carbon G


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ACS Sustainable Chemistry & Engineering cost reductions at larger scale.44 In an another assessment to determine the energy return on investment (EROI), Beal et al.45 concluded that algal biocrude can be economically competitive by using methods like (a) wastewater as the nutrient medium, (b) flue gases as the CO2 source, (c) minimized pumping, (d) avoiding energy intensive harvesting and dewatering, and (e) biomass conversions using wet biomass. With a simplified design, minimum cost, and optimized process of extracting valuables and generation of biofuel feedstock, ABR used in the present study could be a potential biorefinery agent. The aqueous phase, which was 11−17% of the total product yield, was one of the major coproducts of hydropyrolysis. The maximum nitrogen recovery (88%) showed a high potential of nutrient recovery and recycling as an algal growth medium. In spite of environmental benefits, this route is not considered to be viable for complete recovery of nitrogen, which is a major fraction, and needed high dilutions to avoid inhibitions. In this context, Garcia-Moscoso et al.46 used flash hydrolysis of algae, and recovered liquid hydrolysate was used for extraction of amino acids and peptides. In an another approach by Barbera et al.,47 minerals were recovered from liquid hydrolysate by precipitation, and residual lipid-rich solids were used as biofuel intermediates. Chen et al.48 proved that by using ultrasonically assisted extraction some nitrogenous compounds can be recovered with simultaneous denitrogenation of biocrude. In order to recover maximum energy and biochemicals from algal biomass, the conversion and recovery routes should be chosen carefully for a sustainable biorefinery.

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Springer International Publishing: Cham, Switzerland, 2017; pp 227− 245. (2) Choudhary, P.; Malik, A.; Pant, K. K. Algal Biofilm Systems: An Answer to Algal Biofuel Dilemma. In Algal Biofuels: Recent Advances and Future Prospects; Gupta, S. K., Malik, A., Bux, F., Eds.; Springer International Publishing: Cham, Switzerland, 2017; pp 77−96. (3) Choudhary, P.; Prajapati, S. K.; Kumar, P.; Malik, A.; Pant, K. K. Development and performance evaluation of an algal biofilm reactor for treatment of multiple wastewaters and characterization of biomass for diverse applications. Bioresour. Technol. 2017, 224, 276. (4) Gross, M.; Mascarenhas, V.; Wen, Z. Evaluating algal growth performance and water use efficiency of pilot-scale revolving algal biofilm (RAB) culture systems. Biotechnol. Bioeng. 2015, 112 (10), 2040−2050. (5) Mulbry, W.; Kondrad, S.; Pizarro, C.; Kebede-westhead, E. Treatment of dairy manure effluent using freshwater algae: Algal productivity and recovery of manure nutrients using pilot-scale algal turf scrubbers. Bioresour. Technol. 2008, 99 (17), 8137−8142. (6) Choudhary, P.; Bhattacharya, A.; Prajapati, S. K.; Kaushik, P.; Malik, A. Phycoremediation-Coupled Biomethanation of Microalgal Biomass. Handbook of Marine Microalgae 2015, 483−499. (7) Ranjan, A.; Patil, C.; Moholkar, V. S. Ind. Eng. Chem. Res. 2010, 49, 2979−2985. (8) Anand, V.; Sunjeev, V.; Vinu, R. Catalytic fast pyrolysis of Arthrospira platensis (spirulina) algae using zeolites. J. Anal. Appl. Pyrolysis 2016, 118, 298−307. (9) Garcia-Moscoso, J. L.; Obeid, W.; Kumar, S.; Hatcher, P. G. Flash hydrolysis of microalgae (Scenedesmus sp.) for protein extraction and production of biofuels intermediates. J. Supercrit. Fluids 2013, 82 (x), 183−190. (10) Garcia-perez, M.; Shen, J.; Wang, X. S.; Li, C. Production and fuel properties of fast pyrolysis oil/bio-diesel blends. Fuel Process. Technol. 2010, 91 (3), 296−305. (11) Marker, T. L.; Felix, L. G.; Linck, M. B.; Roberts, M. J. Environ. Prog. Sustainable Energy 2012, 31 (2), 191−199. (12) Chiaramonti, D.; Prussi, M.; Buffi, M.; Rizzo, A. M.; Pari, L. Review and experimental study on pyrolysis and hydrothermal liquefaction of microalgae for biofuel production. Appl. Energy 2017, 185, 963−972. (13) Alba, L. G.; Torri, C.; Samorì, C.; Van der Spek, J.; Fabbri, D.; Kersten, S. R. A.; Brilman, D. W. F. W. Energy Fuels 2012, 26, 642− 657. (14) Orfield, N. D.; Fang, A. J.; Valdez, P. J.; Nelson, M. C.; Savage, P. E.; Lin, X. N.; Keoleian, G. A. Life Cycle Design of an Algal Biorefinery Featuring Hydrothermal Liquefaction: Effect of Reaction Conditions and an Alternative Pathway Including Microbial Regrowth. ACS Sustainable Chem. Eng. 2014, 2, 867−874. (15) Thangalazhy-gopakumar, S.; Adhikari, S.; Chattanathan, S. A.; Gupta, R. B. Catalytic pyrolysis of green algae for hydrocarbon production using H + ZSM-5 catalyst. Bioresour. Technol. 2012, 118, 150−157. (16) Kumar, D.; Pant, K. K. Biomass Convers. Biorefin. 2016, 6, 79− 90. (17) Du, Z.; Ma, X.; Li, Y.; Chen, P.; Liu, Y.; Lin, X.; Lei, H.; Ruan, R. Production of aromatic hydrocarbons by catalytic pyrolysis of microalgae with zeolites: Catalyst screening in a pyroprobe. Bioresour. Technol. 2013, 139, 397−401. (18) Kumar, D.; Pant, K. K. Production and characterization of biocrude and biochar obtained from non-edible de-oiled seed cakes hydrothermal conversion. J. Anal. Appl. Pyrolysis 2015, 115, 77−86. (19) Jena, U.; Das, K. C.; Kastner, J. R. Comparison of the effects of Na 2 CO 3, Ca 3 (PO 4) 2, and NiO catalysts on the thermochemical liquefaction of microalga Spirulina platensis. Appl. Energy 2012, 98, 368−375. (20) Jorquera, O.; Kiperstok, A.; Sales, E. a.; Embiruçu, M.; Ghirardi, M. L. Comparative energy life-cycle analyses of microalgal biomass production in open ponds and photobioreactors. Bioresour. Technol. 2010, 101 (4), 1406−1413.

ASSOCIATED CONTENT

S Supporting Information *

The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acssuschemeng.7b00233. Differential mass loss profiles of ABR-grown untreated algal biomass by thermogravimetry−differential scanning calorimetry (Figure S1). (PDF)

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AUTHOR INFORMATION

Corresponding Author

*E-mails: [email protected]; [email protected]. in. Tel.: +91 11 26591158. Fax: +91 11 26591121. ORCID

Anushree Malik: 0000-0002-2761-0568 Kamal K. Pant: 0000-0002-0722-8871 Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS The authors gratefully acknowledge the Department of Biotechnology (Grant DBT/IC-2/Indo-Brazil/2016-19/06), Government of India for partial financial support. One of the authors (P.C.) acknowledges the CSIR SRF fellowship (Grant 09/086/ (1222)/2015-EMR-I). The authors appreciate the assistance provided by Mr. Suchit (Project staff, Chemical Engineering, IIT Delhi) during the experiments.

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REFERENCES

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Mass-Scale Algal Biomass Production Using Algal Biofilm Reactor

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