Abstract
This study investigated the effect of enzymatic and hydrothermal pretreatment approaches on the solubilization of organic matter, structure, and biogas yield from microalgal biomass. The soluble chemical oxygen demand (sCOD) concentration increased by 1.21–3.30- and 5.54–6.60-fold compared to control by enzymatic and hydrothermal pretreatments respectively. The hydrothermal pretreatment affected the structural changes in the microalgal biomass markedly; nonetheless, increased enzymatic concentration also had a definite effect on it as determined by qualitative approaches like scanning electron microscopy and Fourier transform infrared spectroscopy. Also, the hydrothermal pretreatment (100 °C for 30 min) resulted in the highest biogas production potential (P) of 765.37 mLg−1 VS at a maximum biogas production rate (Rm) of 22.66 mLg−1 day−1 with a very short lag phase (λ) of 0.07 days. The biogas production of pretreated microalgal biomass particularly at higher enzyme dose (20%, 24 h) and higher hydrothermal pretreatment temperature (120 °C, 30 min) showed a significant but weak correlation (R = 0.53) with sCOD, thus demonstrating that the less organic matter was used up for the biogas production. The modified Gompertz model explained the anaerobic digestion of microalgal biomass more accurately and had a better fit to the experimental data comparatively because of the low root mean square error (3.259–16.728), residual sum of squares (78.887–177.025), and Akaike’s Information Criterion (38.605–62.853).
Similar content being viewed by others
Explore related subjects
Discover the latest articles, news and stories from top researchers in related subjects.Data availability
All data generated or analyzed during this study are included in this published article.
References
Abdel-Raouf N, Al-Homaidan AA, Ibraheem IBM (2012) Microalgae and wastewater treatment. Saudi J Biol Sci 19:257–275. https://doi.org/10.1016/j.sjbs.2012.04.005
Abudi ZN, Hu Z, Abood AR (2020) Anaerobic co-digestion of mango leaves and pig manure: performance assessment and kinetic analysis. Biomass Convers Biorefinery 1–11. https://doi.org/10.1007/s13399-020-00665-6
Alam MA, Wan C, Guo SL, Zhao ZQ, Huang ZY, Yang YL, Chang JS, Bai FW (2014) Characterization of the flocculating agent from the spontaneously flocculating microalga Chlorella vulgaris JSC-7. J Biosci Bioeng 118:29–33. https://doi.org/10.1016/j.jbiosc.2013.12.021
Alzate ME, Muñoz R, Rogalla F, Fdz-Polanco F, Pérez-Elvira SI (2012) Biochemical methane potential of microalgae: influence of substrate to inoculum ratio, biomass concentration and pretreatment. Bioresour Technol 123:488–494. https://doi.org/10.1016/j.biortech.2012.06.113
Angelidaki I, Sanders W (2004) Assessment of the anaerobic biodegradability of macropollutants. Rev Environ Sci Bio/Technol 3:117–129. https://doi.org/10.1007/s11157-004-2502-3
Angelidaki I, Alves M, Bolzonella D, Borzacconi L, Campos JL, Guwy AJ, Kalyuzhnyi S, Jenicek P, van Lier JB (2009) Defining the biomethane potential (BMP) of solid organic wastes and energy crops: a proposed protocol for batch assays. Water Sci Technol 59:927–934. https://doi.org/10.2166/wst.2009.040
AOAC (2000) Association of Official Analytical Chemists, 17th edn. Official Methods of Analysis, Maryland
Appels L, Degrève J, Van der Bruggen B, Impe JV, Dewil R (2010) Influence of low temperature thermal pre-treatment on sludge solubilisation, heavy metal release and anaerobic digestion. Bioresour Technol 101:5743–5748. https://doi.org/10.1016/j.biortech.2010.02.068
Bailey JE, Ollis DF (1986) Biochemical engineering fundamentals. McGraw Hill Book Company, New York
Baldan B, Andolfo P, Navazio L, Tolomio C, Mariani P (2009) Cellulose in algal cell wall : an “in situ” localization. Eur J Histochem 45:51. https://doi.org/10.4081/1613
Bohutskyi P, Phan D, Spierling RE, Kopachevsky AM, Bouwer EJ, Lundquist TJ, Betenbaugh MJ (2019) Production of lipid-containing algal-bacterial polyculture in wastewater and biomethanation of lipid extracted residues: enhancing methane yield through hydrothermal pretreatment and relieving solvent toxicity through co-digestion. Sci Total Environ 653:1377–1394. https://doi.org/10.1016/j.scitotenv.2018.11.026
Bong CPC, Lim LY, Lee CT, Ho WS, Klemeš JJ (2017) The kinetics for mathematical modelling on the anaerobic digestion of organic waste - a review. Chem Eng Trans 61:1669–1674. https://doi.org/10.3303/CET1761276
Borowitzka MA, Moheimani NR (2013) Algae for biofuels and energy. Springer, Netherlands. https://doi.org/10.1007/978-94-007-5479-9
Bozzola JJ, Russell LD (1999) Electron microscopy: principles and techniques for biologists. Jones and Bartlett Publishers, Boston. http://113.160.249.209:8080/xmlui/handle/123456789/5419
Carrère H, Dumas C, Battimelli A, Batstone DJ, Delgenès JP, Steyer JP, Ferrer I (2010) Pretreatment methods to improve sludge anaerobic degradability: a review. J Hazard Mater 183:1–15. https://doi.org/10.1016/j.jhazmat.2010.06.129
Chen PH, Oswald WJ (1998) Thermochemical treatment for algal fermentation. Environ Int 24:889–897. https://doi.org/10.1016/S0160-4120(98)00080-4
Chen H, Xia A, Zhu X et al (2022) Hydrothermal hydrolysis of algal biomass for biofuels production: a review. Bioresour Technol 344:126213. https://doi.org/10.1016/J.BIORTECH.2021.126213
Chevalier F, Chobert J-M, Popineau Y, Nicolas MG, Haertlé T (2001) Improvement of functional properties of β-lactoglobulin glycated through the Maillard reaction is related to the nature of the sugar. Int Dairy J 11:145–152. https://doi.org/10.1016/S0958-6946(01)00040-1
Dar RA (2017) Bioprospects of microlagal isolates from water logged area of Punjab for biogas production. Punjab Agricultural University, Ludhiana
Dar RA, Phutela UG (2020) Enzymatic and hydrothermal pretreatment of newly isolated Spirulina subsalsa BGLR6 biomass for enhanced biogas production. Waste Biomass Valor 11:3639–3651. https://doi.org/10.1007/s12649-019-00712-y
Dar RA, Parmar M, Dar EA, Sani RK, Phutela UG (2021) Biomethanation of agricultural residues: potential, limitations and possible solutions. Renew Sustain Energy Rev 135:110217. https://doi.org/10.1016/j.rser.2020.110217
Demuez M, Mahdy A, Tomás-Pejó E, González-Fernández C, Ballesteros M (2015) Enzymatic cell disruption of microalgae biomass in biorefinery processes. Biotechnol Bioeng 112:1955–1966. https://doi.org/10.1002/bit.25644
Domozych DS, Ciancia M, Fangel JU, Mikkelsen MD, Ulvskov P, Willats WGT (2012) The cell walls of green algae: a journey through evolution and diversity. Front Plant Sci 3:82. https://doi.org/10.3389/fpls.2012.00082
Donoso-Bravo A, Pérez-Elvira S, Aymerich E, Fdz-Polanco F (2011) Assessment of the influence of thermal pre-treatment time on the macromolecular composition and anaerobic biodegradability of sewage sludge. Bioresour Technol 102:660–666. https://doi.org/10.1016/j.biortech.2010.08.035
Eaton A (2005) Standard methods for the examination of water and wastewater, 21st edn. APHA-AWWA-WEF, Washington D.C
Ehimen EA, Holm-Nielsen J-B, Poulsen M, Boelsmand JE (2013) Influence of different pre-treatment routes on the anaerobic digestion of a filamentous algae. Renew Energy 50:476–480. https://doi.org/10.1016/J.RENENE.2012.06.064
Fdz-Polanco F, Velazquez R, Perez-Elvira SI, Casas C, del Barrio D, Cantero FJ, Fdz-Polanco M, Rodriguez P, Panizo L, Serrat J, Rouge P (2008) Continuous thermal hydrolysis and energy integration in sludge anaerobic digestion plants. Water Sci Technol 57:1221–1226. https://doi.org/10.2166/wst.2008.072
Feng GD, Zhang F, Cheng LH, Xu XH, Zhang L, Chen HL (2013) Evaluation of FT-IR and Nile Red methods for microalgal lipid characterization and biomass composition determination. Bioresour Technol 128:107–112. https://doi.org/10.1016/j.biortech.2012.09.123
Fernández-Rodríguez MJ, Rincón B, Fermoso FG, Jiménez AM, Borja R (2014) Assessment of two-phase olive mill solid waste and microalgae co-digestion to improve methane production and process kinetics. Bioresour Technol 157:263–269. https://doi.org/10.1016/j.biortech.2014.01.096
Fu Q, Zhang H, Chen H, Liao Q, Xia A, Huang Y, Zhu X, Reungsang A, Liu Z (2018) Hydrothermal hydrolysis pretreatment of microalgae slurries in a continuous reactor under subcritical conditions for large–scale application. Bioresour Technol 266:306–314. https://doi.org/10.1016/J.BIORTECH.2018.06.088
Ganesh Saratale R, Kumar G, Banu R, Xia A, Periyasamy S, Saratale GD (2018) A critical review on anaerobic digestion of microalgae and macroalgae and co-digestion of biomass for enhanced methane generation. Bioresour Technol 262:319–332. https://doi.org/10.1016/j.biortech.2018.03.030
Gerken HG, Donohoe B, Knoshaug EP (2013) Enzymatic cell wall degradation of Chlorella vulgaris and other microalgae for biofuels production. Planta 237:239–253. https://doi.org/10.1007/s00425-012-1765-0
Geun Goo B, Baek G, Choi DJ, Park YI, Synytsya A, Bleha R, Seong DH, Lee CG, Park JK (2013) Characterization of a renewable extracellular polysaccharide from defatted microalgae Dunaliella tertiolecta. Bioresour Technol 129:343–350. https://doi.org/10.1016/j.biortech.2012.11.077
González-Fernández C, Molinuevo-Salces B, García-González MC (2011) Evaluation of anaerobic codigestion of microalgal biomass and swine manure via response surface methodology. Appl Energy 88:3448–3453. https://doi.org/10.1016/j.apenergy.2010.12.035
González-Fernández C, Sialve B, Bernet N, Steyer JP (2012) Comparison of ultrasound and thermal pretreatment of Scenedesmus biomass on methane production. Bioresour Technol 110:610–616. https://doi.org/10.1016/j.biortech.2012.01.043
Grosser A (2017) The influence of decreased hydraulic retention time on the performance and stability of co-digestion of sewage sludge with grease trap sludge and organic fraction of municipal waste. J Environ Manage 203:1143–1157. https://doi.org/10.1016/j.jenvman.2017.04.085
Ji XY, Lin WD, Zhang WD, Yin F, Zhao XL, Wang CM, Liu J, Yang H (2016) Evaluation of methane production features and kinetics of Bougainvillea spectabilis Willd waste under mesophilic conditions. Afri J Biotechnol 38:1537–1543. https://doi.org/10.1080/15567036.2015.1079569
Kassim MA, Bhattacharya S (2016) Dilute alkaline pretreatment for reducing sugar production from Tetraselmis suecica and Chlorella sp. biomass. Process Biochem 51:1757–1766. https://doi.org/10.1016/j.procbio.2015.11.027
Keymer P, Ruffell I, Pratt S, Lant P (2013) High pressure thermal hydrolysis as pre-treatment to increase the methane yield during anaerobic digestion of microalgae. Bioresour Technol 131:128–133. https://doi.org/10.1016/j.biortech.2012.12.125
Khalid A, Arshad M, Anjum M et al (2011) The anaerobic digestion of solid organic waste. Waste Manag 31:1737–1744. https://doi.org/10.1016/j.wasman.2011.03.021
Khan MA, Alqadami AA, Otero M, Siddiqui MR, Alothman ZA, Alsohaimi I, Rafatullah M, Hamedelniel AE (2019) Heteroatom-doped magnetic hydrochar to remove post-transition and transition metals from water: Synthesis, characterization, and adsorption studies. Chemosphere 218:1089–1099. https://doi.org/10.1016/J.CHEMOSPHERE.2018.11.210
Kim DH, Jeong E, Oh SE, Shin HS (2010) Combined (alkaline+ultrasonic) pretreatment effect on sewage sludge disintegration. Water Res 44:3093–3100. https://doi.org/10.1016/j.watres.2010.02.032
Krishnamoorthy A, Rodriguez C, Durrant A (2022) Sustainable approaches to microalgal pre-treatment techniques for biodiesel production: a review. Sustain 14:9953. https://doi.org/10.3390/SU14169953
Kumar G, Sivagurunathan P, Thi NBD, Zhen G, Kobayashi T, Kim SH, Xu K (2016) Evaluation of different pretreatments on organic matter solubilization and hydrogen fermentation of mixed microalgae consortia. Int J Hydrogen Energy 41:21628–21640. https://doi.org/10.1016/j.ijhydene.2016.05.195
Laureano-Perez L, Teymouri F, Alizadeh H, Dale BE (2005) Understanding factors that limit enzymatic hydrolysis of biomass: characterization of pretreated corn stover. Appl Biochem Biotechnol 124:1081–1099. https://doi.org/10.1385/abab:124:1-3:1081
Lee K, Kim D, Park KY, Hyundong Lee, Chorong Kim (2016) Effect of hydrothermal pretreatment for enhanced biogas production using micro-algal biomass. Int J Bio-Science Bio-Technology 8:67–76. https://doi.org/10.14257/ijbsbt.2016.8.4.08
Lu W, Alam MA, Pan Y, Wu J, Wang Z, Yuan Z (2016) A new approach of microalgal biomass pretreatment using deep eutectic solvents for enhanced lipid recovery for biodiesel production. Bioresour Technol 218:123–128. https://doi.org/10.1016/j.biortech.2016.05.120
Mahdy A, Mendez L, Ballesteros M, González-Fernández C (2014) Autohydrolysis and alkaline pretreatment effect on Chlorella vulgaris and Scenedesmus sp. methane production. Energy 78:48–52. https://doi.org/10.1016/j.energy.2014.05.052
Martín Juárez J, Riol Pastor E, Fernández Sevilla JM, Torre RM, García-Encina PA, Rodríguez SB (2018) Effect of pretreatments on biogas production from microalgae biomass grown in pig manure treatment plants. Bioresour Technol 257:30–38. https://doi.org/10.1016/j.biortech.2018.02.063
Mata TM, Martins AA, Caetano NS (2010) Microalgae for biodiesel production and other applications: a review. Renew Sustain Energy Rev 14:217–232. https://doi.org/10.1016/j.rser.2009.07.020
Murdock JN, Wetzel DL (2009) FT-IR microspectroscopy enhances biological and ecological analysis of algae. Appl Spectrosc Rev 44:335–361. https://doi.org/10.1080/05704920902907440
Mussgnug JH, Klassen V, Schlüter A, Kruse O (2010) Microalgae as substrates for fermentative biogas production in a combined biorefinery concept. J Biotechnol 150:51–56. https://doi.org/10.1016/j.jbiotec.2010.07.030
Oliveira JV, Alves MM, Costa JC (2014) Design of experiments to assess pre-treatment and co-digestion strategies that optimize biogas production from macroalgae Gracilaria vermiculophylla. Bioresour Technol 162:323–330. https://doi.org/10.1016/j.biortech.2014.03.155
Pancha I, Chokshi K, Maurya R, Bhattacharya S, Bachani P, Mishra M (2016) Comparative evaluation of chemical and enzymatic saccharification of mixotrophically grown de-oiled microalgal biomass for reducing sugar production. Bioresour Technol 204:9–16. https://doi.org/10.1016/j.biortech.2015.12.078
Park JBK, Craggs RJ, Shilton AN (2011) Wastewater treatment high rate algal ponds for biofuel production. Bioresour Technol 102:35–42. https://doi.org/10.1016/j.biortech.2010.06.158
Passos F, Ferrer I (2014) Microalgae conversion to biogas: thermal pretreatment contribution on net energy production. Environ Sci Technol 48:7171–7178. https://doi.org/10.1021/es500982v
Passos F, García J, Ferrer I (2013a) Impact of low temperature pretreatment on the anaerobic digestion of microalgal biomass. Bioresour Technol 138:79–86. https://doi.org/10.1016/J.BIORTECH.2013.03.114
Passos F, Solé M, García J, Ferrer I (2013b) Biogas production from microalgae grown in wastewater: effect of microwave pretreatment. Appl Energy 108:168–175. https://doi.org/10.1016/j.apenergy.2013.02.042
Passos F, Uggetti E, Carrère H, Ferrer I (2014) Pretreatment of microalgae to improve biogas production: a review. Bioresour Technol 172:403–412. https://doi.org/10.1016/j.biortech.2014.08.114
Passos F, Hom-Diaz A, Blanquez P, Vicent T, Ferrer I (2016) Improving biogas production from microalgae by enzymatic pretreatment. Bioresour Technol 199:347–351. https://doi.org/10.1016/J.BIORTECH.2015.08.084
Pirwitz K, Rihko-Struckmann L, Sundmacher K (2016) Valorization of the aqueous phase obtained from hydrothermally treated Dunaliella salina remnant biomass. Bioresour Technol 219:64–71. https://doi.org/10.1016/J.BIORTECH.2016.06.095
Pitt RE, Cross TL, Pell AN, Schofield P, Doane PH (1999) Use of in vitro gas production models in ruminal kinetics. Math Biosci 159:145–163. https://doi.org/10.1016/S0025-5564(99)00020-6
Prajapati SK, Malik A, Vijay VK, Sreekrishnan TR (2015) Enhanced methane production from algal biomass through short duration enzymatic pretreatment and codigestion with carbon rich waste. RSC Adv 5:67175–67183. https://doi.org/10.1039/C5RA12670C
Pramanik SK, Suja FB, Porhemmat M, Pramanik BK (2019) Performance and kinetic model of a single-stage anaerobic digestion system operated at different successive operating stages for the treatment of food waste. Processes 7:600. https://doi.org/10.3390/pr7090600
Rajput AA, Zeshan, Visvanathan C (2018) Effect of thermal pretreatment on chemical composition, physical structure and biogas production kinetics of wheat straw. J Environ Manage 221:45–52. https://doi.org/10.1016/J.JENVMAN.2018.05.011
Saratale RG, Kumar G, Banu R, Xia A, Periyasamy S, Saratale GD (2018) A critical review on anaerobic digestion of microalgae and macroalgae and co-digestion of biomass for enhanced methane generation. Bioresour Technol 262:319–332. https://doi.org/10.1016/j.biortech.2018.03.030
Sialve B, Bernet N, Bernard O (2009) Anaerobic digestion of microalgae as a necessary step to make microalgal biodiesel sustainable. Biotechnol Adv 27:409–416. https://doi.org/10.1016/j.biotechadv.2009.03.001
Siengchum T, Isenberg M, Chuang SSC (2013) Fast pyrolysis of coconut biomass - an FTIR study. Fuel 105:559–565. https://doi.org/10.1016/j.fuel.2012.09.039
Sills DL, Gossett JM (2012) Using FTIR to predict saccharification from enzymatic hydrolysis of alkali-pretreated biomasses. Biotechnol Bioeng 109:353–362. https://doi.org/10.1002/bit.23314
Singh NK, Dhar DW (2011) Microalgae as second generation biofuel: a review. Agron Sustain Dev 31:605–629. https://doi.org/10.1007/s13593-011-0018-0
Sivagurunathan P, Kumar G, Mudhoo A, Rene ER, Saratale GD, Kobayashi T, Xu K, Kim SH, Kim DH (2017) Fermentative hydrogen production using lignocellulose biomass: an overview of pre-treatment methods, inhibitor effects and detoxification experiences. Renew Sustain Energy Rev 77:28–42. https://doi.org/10.1016/j.rser.2017.03.091
Stanier RY, Kunisawa R, Mandel M, Cohen-Bazire G (1971) Purification and properties of unicellular blue-green algae (order Chroococcales). Bacteriol Rev 35:171–205. https://doi.org/10.1128/br.35.2.171-205.1971
Syaichurrozi I (2018) Biogas production from co-digestion Salvinia molesta and rice straw and kinetics. Renew Energy 115:76–86. https://doi.org/10.1016/J.RENENE.2017.08.023
Usman M, Chen H, Chen K, Ren S, Clark JH, Fan J, Luo G, Zhang S (2019) Characterization and utilization of aqueous products from hydrothermal conversion of biomass for bio-oil and hydro-char production: a review. Green Chem 21:1553–1572. https://doi.org/10.1039/C8GC03957G
Wang M, Wang J, Li Y, Li Q, Li P, Luo L, Zhen F, Zhang G, Sun Y (2022) Low-temperature pretreatment of biomass for enhancing biogas production: a review. Ferment 8:562. https://doi.org/10.3390/FERMENTATION8100562
Ward AJ, Lewis DM, Green FB (2014) Anaerobic digestion of algae biomass: a review. Algal Res 5:204–214. https://doi.org/10.1016/J.ALGAL.2014.02.001
Yap BHJ, Crawford SA, Dagastine RR, Scales PJ, Martin GJO (2016) Nitrogen deprivation of microalgae: effect on cell size, cell wall thickness, cell strength, and resistance to mechanical disruption. J Ind Microbiol Biotechnol 43:1671–1680. https://doi.org/10.1007/s10295-016-1848-1
Yoo G, Park MS, Yang JW (2015) Chemical pretreatment of algal biomass. Pretreat Biomass Process Technol 227–258. https://doi.org/10.1016/B978-0-12-800080-9.00012-8
Yu WL, Ansari W, Schoepp NG, Hannon MJ, Mayfield SP, Burkart MD (2011) Modifications of the metabolic pathways of lipid and triacylglycerol production in microalgae. Microb Cell Fact https://doi.org/10.1186/1475-2859-10-91
Zhen G, Lu X, Li YY, Zhao Y (2014) Combined electrical-alkali pretreatment to increase the anaerobic hydrolysis rate of waste activated sludge during anaerobic digestion. Appl Energy 128:93–102. https://doi.org/10.1016/j.apenergy.2014.04.062
Zhen G, Lu X, Kobayashi T, Kumar G, Xu K (2016) Anaerobic co-digestion on improving methane production from mixed microalgae (Scenedesmus sp., Chlorella sp.) and food waste: kinetic modeling and synergistic impact evaluation. Chem Eng J 299:332–341. https://doi.org/10.1016/j.cej.2016.04.118
Zwietering MH, Jongenburger I, RomboutsVan’t Riet FMK (1990) Modeling of the bacterial growth curve. Appl Environ Microbiol 56:1875–1881. https://doi.org/10.1128/aem.56.6.1875-1881.1990
Funding
The Indian Council of Medical Research (ICMR), New Delhi, India, is thankfully acknowledged for providing fellowship to the author Rouf Ahmad Dar under Grant No. 1/3/JRF-2015 (2)/HRD.
Author information
Authors and Affiliations
Contributions
The authors Rouf Ahmad Dar and Urmila Gupta Phutela conceptualized and designed the study. Material preparation, experimentation, investigation, data collection, data validation, and formal analysis was performed by Rouf Ahmad Dar. Rouf Ahmad Dar wrote the first draft of the manuscript and both authors reviewed and edited the manuscript. Urmila Gupta Phutela also contributed to the supervision of the work. The final manuscript was read and approved by all the authors.
Corresponding author
Ethics declarations
Ethics approval and consent to participate
Not applicable.
Consent for publication
Not applicable.
Competing interests
The authors declare no competing interests.
Additional information
Responsible Editor: Ta Yeong Wu
Publisher's note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Dar, R.A., Phutela, U.G. Improvement of Asterarcys quadricellulare biomass solubilization and subsequent biogas production via pretreatment approaches: structural changes and kinetic modeling evaluation. Environ Sci Pollut Res 30, 58450–58465 (2023). https://doi.org/10.1007/s11356-023-26555-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-023-26555-8