Highly efficient methane generation from untreated microalgae biomass

Klassen V, Blifernez-Klassen O, Wibberg D, Winkler A, Kalinowski J, Posten C, Kruse O (2017)
Biotechnology for Biofuels 10(1): 186.

Zeitschriftenaufsatz | Veröffentlicht | Englisch
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Abstract / Bemerkung
Background The fact that microalgae perform very efficiently photosynthetic conversion of sunlight into chemical energy has moved them into the focus of regenerative fuel research. Especially, biogas generation via anaerobic digestion is economically attractive due to the comparably simple apparative process technology and the theoretical possibility of converting the entire algal biomass to biogas/methane. In the last 60 years, intensive research on biogas production from microalgae biomass has revealed the microalgae as a rather challenging substrate for anaerobic digestion due to its high cell wall recalcitrance and unfavorable protein content, which requires additional pretreatment and co-fermentation strategies for sufficient fermentation. However, sustainable fuel generation requires the avoidance of cost/energy intensive biomass pretreatments to achieve positive net-energy process balance. Results Cultivation of microalgae in replete and limited nitrogen culture media conditions has led to the formation of protein-rich and low protein biomass, respectively, with the last being especially optimal for continuous fermentation. Anaerobic digestion of nitrogen limited biomass (low-N BM) was characterized by a stable process with low levels of inhibitory substances and resulted in extraordinary high biogas, and subsequently methane productivity [750 ± 15 and 462 ± 9 mLN g−1 volatile solids (VS) day−1, respectively], thus corresponding to biomass-to-methane energy conversion efficiency of up to 84%. The microbial community structure within this highly efficient digester revealed a clear predominance of the phyla Bacteroidetes and the family Methanosaetaceae among the Bacteria and Archaea, respectively. The fermentation of replete nitrogen biomass (replete-N BM), on the contrary, was demonstrated to be less productive (131 ± 33 mLN CH4 g−1VS day−1) and failed completely due to acidosis, caused through high ammonia/ammonium concentrations. The organization of the microbial community of the failed (replete-N) digester differed greatly compared to the stable low-N digester, presenting a clear shift to the phyla Firmicutes and Thermotogae, and the archaeal population shifted from acetoclastic to hydrogenotrophic methanogenesis. Conclusions The present study underlines the importance of cultivation conditions and shows the practicability of microalgae biomass usage as mono-substrate for highly efficient continuous fermentation to methane without any pretreatment with almost maximum practically achievable energy conversion efficiency (biomass to methane).
Biofuel Biogas Methane Microalgae mono-substrate Nitrogen limitation Continuous anaerobic fermentation/digestion Maximal energy conversion efficiency Microbial community Ammonia/ammonium inhibition
Biotechnology for Biofuels
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Klassen V, Blifernez-Klassen O, Wibberg D, et al. Highly efficient methane generation from untreated microalgae biomass. Biotechnology for Biofuels. 2017;10(1): 186.
Klassen, V., Blifernez-Klassen, O., Wibberg, D., Winkler, A., Kalinowski, J., Posten, C., & Kruse, O. (2017). Highly efficient methane generation from untreated microalgae biomass. Biotechnology for Biofuels, 10(1), 186. doi:10.1186/s13068-017-0871-4
Klassen, Viktor, Blifernez-Klassen, Olga, Wibberg, Daniel, Winkler, Anika, Kalinowski, Jörn, Posten, Clemens, and Kruse, Olaf. 2017. “Highly efficient methane generation from untreated microalgae biomass”. Biotechnology for Biofuels 10 (1): 186.
Klassen, V., Blifernez-Klassen, O., Wibberg, D., Winkler, A., Kalinowski, J., Posten, C., and Kruse, O. (2017). Highly efficient methane generation from untreated microalgae biomass. Biotechnology for Biofuels 10:186.
Klassen, V., et al., 2017. Highly efficient methane generation from untreated microalgae biomass. Biotechnology for Biofuels, 10(1): 186.
V. Klassen, et al., “Highly efficient methane generation from untreated microalgae biomass”, Biotechnology for Biofuels, vol. 10, 2017, : 186.
Klassen, V., Blifernez-Klassen, O., Wibberg, D., Winkler, A., Kalinowski, J., Posten, C., Kruse, O.: Highly efficient methane generation from untreated microalgae biomass. Biotechnology for Biofuels. 10, : 186 (2017).
Klassen, Viktor, Blifernez-Klassen, Olga, Wibberg, Daniel, Winkler, Anika, Kalinowski, Jörn, Posten, Clemens, and Kruse, Olaf. “Highly efficient methane generation from untreated microalgae biomass”. Biotechnology for Biofuels 10.1 (2017): 186.
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Metabolic survey of Botryococcus braunii: Impact of the physiological state on product formation.
Blifernez-Klassen O, Chaudhari S, Klassen V, Wördenweber R, Steffens T, Cholewa D, Niehaus K, Kalinowski J, Kruse O., PLoS One 13(6), 2018
PMID: 29879215

81 References

Daten bereitgestellt von Europe PubMed Central.

Renewable energy futures: targets, scenarios, and pathways
Martinot E, Dienst C, Weiliang L, Qimin C., 2007

An economic and technical evaluation of microalgal biofuels.
Stephens E, Ross IL, King Z, Mussgnug JH, Kruse O, Posten C, Borowitzka MA, Hankamer B., Nat. Biotechnol. 28(2), 2010
PMID: 20139944

Borowitzka MA, Moheimani NR., 2013

Biofuels from microalgae-A review of technologies for production, processing, and extractions of biofuels and co-products
Brennan L, Owende P., 2010
Microalgal hydrogen production.
Kruse O, Hankamer B., Curr. Opin. Biotechnol. 21(3), 2010
PMID: 20399635



Raceways-based production of algal crude oil
Chisti Y., 2013
Multifactorial comparison of photobioreactor geometries in parallel microalgae cultivations
Wolf J, Stephens E, Steinbusch S, Yarnold J, Ross IL, Steinweg C., 2016

Biochemical methane potential (BMP) of solid organic substrates: evaluation of anaerobic biodegradability using data from an international interlaboratory study
Raposo F, Fernández-Cegrí V, De MA, Borja R, Béline F, Cavinato C., 2011
Biogas production: current state and perspectives.
Weiland P., Appl. Microbiol. Biotechnol. 85(4), 2009
PMID: 19777226
Food waste to bioenergy via anaerobic processes
Thi NBD, Sen B, Chen CC, Kumar G, Lin CY., 2014
Waste-to-wealth for valorization of food waste to hydrogen and methane towards creating a sustainable ideal source of bioenergy
Thi NBD, Lin C-Y, Kumar G., 2016
Anaerobic digestion of Algae.
GOLUEKE CG, OSWALD WJ, GOTAAS HB., Appl Microbiol 5(1), 1957
PMID: 13403639
Efficiency and biotechnological aspects of biogas production from microalgal substrates.
Klassen V, Blifernez-Klassen O, Wobbe L, Schluter A, Kruse O, Mussgnug JH., J. Biotechnol. 234(), 2016
PMID: 27449486
Protease pretreated Chlorella vulgaris biomass bioconversion to methane via semi-continuous anaerobic digestion
Mahdy A, Mendez L, Ballesteros M, González-Fernández C., 2015
Autohydrolysis and alkaline pretreatment effect on Chlorella vulgaris and Scenedesmus sp. methane production
Mahdy A, Mendez L, Ballesteros M, González-Fernández C., 2014
Thermal pretreatment of algae for anaerobic digestion.
Marsolek MD, Kendall E, Thompson PL, Shuman TR., Bioresour. Technol. 151(), 2013
PMID: 24189036
Effect of high pressure thermal pretreatment on Chlorella vulgaris biomass: organic matter solubilisation and biochemical methane potential
Mendez L, Mahdy A, Demuez M, Ballesteros M, González-Fernández C., 2014
Effects of thermal pretreatment on anaerobic digestion of Nannochloropsis salina biomass.
Schwede S, Rehman ZU, Gerber M, Theiss C, Span R., Bioresour. Technol. 143(), 2013
PMID: 23831893
Biomethane production using fresh and thermally pretreated Chlorella vulgaris biomass: a comparison of batch and semi-continuous feeding mode
Mendez L, Mahdy A, Ballesteros M, González-Fernández C., 2015
Ammonia inhibition in anaerobic digestion: a review
Yenigün O, Demirel B., 2013
Algae biomass as an alternative substrate in biogas production technologies—Review
Dȩbowski M, Zieliński M, Grala A, Dudek M., 2013
Anaerobic co-digestion on improving methane production from mixed microalgae (Scenedesmus sp., Chlorella sp.) and food waste: kinetic modeling and synergistic impact evaluation
Zhen G, Lu X, Kobayashi T, Kumar G, Xu K., 2016
Carbohydrate-enriched cyanobacterial biomass as feedstock for bio-methane production through anaerobic digestion
Markou G, Angelidaki I, Georgakakis D., 2013
A novel one-stage cultivation/fermentation strategy for improved biogas production with microalgal biomass.
Klassen V, Blifernez-Klassen O, Hoekzema Y, Mussgnug JH, Kruse O., J. Biotechnol. 215(), 2015
PMID: 26022425
Anaerobic biotechnology for industrial wastewater treatment.
Speece RE., Environ. Sci. Technol. 17(9), 1983
PMID: 22656942
Acutodesmus obliquus as a benchmark strain for evaluating methane production from microalgae: influence of different storage and pretreatment methods on biogas yield
Gruber-Brunhumer MR, Jerney J, Zohar E, Nussbaumer M, Hieger C, Bochmann G., 2015
Microalgae as substrates for fermentative biogas production in a combined biorefinery concept.
Mussgnug JH, Klassen V, Schluter A, Kruse O., J. Biotechnol. 150(1), 2010
PMID: 20691224
Reconstruction of the lipid metabolism for the microalga Monoraphidium neglectum from its genome sequence reveals characteristics suitable for biofuel production.
Bogen C, Al-Dilaimi A, Albersmeier A, Wichmann J, Grundmann M, Rupp O, Lauersen KJ, Blifernez-Klassen O, Kalinowski J, Goesmann A, Mussgnug JH, Kruse O., BMC Genomics 14(), 2013
PMID: 24373495
Inhibition of starch synthesis results in overproduction of lipids in Chlamydomonas reinhardtii.
Li Y, Han D, Hu G, Sommerfeld M, Hu Q., Biotechnol. Bioeng. 107(2), 2010
PMID: 20506159
The methane fermentation of carbohydrates
Symons GE, Buswell AM., 1933
Biogas production from algae and cyanobacteria through anaerobic digestion: a review, analysis, and research needs
Bohutskyi P, Bouwer E., 2013
Methanogenic fermentation of fresh and ensiled plant materials
Zubr J., 1986

Braun R., 1982
Ammonia nitrogen and the anaerobic environment on JSTOR
Orris EA., 1961
Toxic effects of ammonia nitrogen in high-rate digestion
Melbinger NR, Donnellon J, Zablatzky HR., 1971
Anaerobic digestion of cyanobacteria and chlorella to produce methane for biofuel
Jegede Abiodun., 2012
Detailed study of anaerobic digestion of Spirulina maxima algal biomass.
Samson R, LeDuyt A., Biotechnol. Bioeng. 28(7), 1986
PMID: 18555423

Methane fermentation of aquatic biomass
Wise DL, Augenstein DC, Ryther JH., 1979

Evaluation of marine algae as a source of biogas in a two-stage anaerobic reactor system
Vergara-Fernández A, Vargas G, Alarcón N, Velasco A., 2008
Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy.
Wang Q, Garrity GM, Tiedje JM, Cole JR., Appl. Environ. Microbiol. 73(16), 2007
PMID: 17586664
Correlations between molecular and operational parameters in continuous lab-scale anaerobic reactors.
Carballa M, Smits M, Etchebehere C, Boon N, Verstraete W., Appl. Microbiol. Biotechnol. 89(2), 2010
PMID: 20878323
Relationship between microbial activity and microbial community structure in six full-scale anaerobic digesters.
Regueiro L, Veiga P, Figueroa M, Alonso-Gutierrez J, Stams AJ, Lema JM, Carballa M., Microbiol. Res. 167(10), 2012
PMID: 22770715
454 pyrosequencing analyses of bacterial and archaeal richness in 21 full-scale biogas digesters.
Sundberg C, Al-Soud WA, Larsson M, Alm E, Yekta SS, Svensson BH, Sorensen SJ, Karlsson A., FEMS Microbiol. Ecol. 85(3), 2013
PMID: 23678985



Community shifts in a well-operating agricultural biogas plant: how process variations are handled by the microbiome.
Theuerl S, Kohrs F, Benndorf D, Maus I, Wibberg D, Schluter A, Kausmann R, Heiermann M, Rapp E, Reichl U, Puhler A, Klocke M., Appl. Microbiol. Biotechnol. 99(18), 2015
PMID: 25998656
Methanogenic population dynamics during semi-continuous biogas fermentation and acidification by overloading.
Blume F, Bergmann I, Nettmann E, Schelle H, Rehde G, Mundt K, Klocke M., J. Appl. Microbiol. 109(2), 2010
PMID: 20148997
Microbial management of anaerobic digestion: exploiting the microbiome-functionality nexus.
Carballa M, Regueiro L, Lema JM., Curr. Opin. Biotechnol. 33(), 2015
PMID: 25682574
Complete genome sequence of the strain Defluviitoga tunisiensis L3, isolated from a thermophilic, production-scale biogas plant.
Maus I, Cibis KG, Wibberg D, Winkler A, Stolze Y, Konig H, Puhler A, Schluter A., J. Biotechnol. 203(), 2015
PMID: 25801333
Sporanaerobacter acetigenes gen. nov., sp. nov., a novel acetogenic, facultatively sulfur-reducing bacterium.
Hernandez-Eugenio G, Fardeau ML, Cayol JL, Patel BK, Thomas P, Macarie H, Garcia JL, Ollivier B., Int. J. Syst. Evol. Microbiol. 52(Pt 4), 2002
PMID: 12148631
Microbial biochemistry, physiology, and biotechnology of hyperthermophilic Thermotoga species.
Conners SB, Mongodin EF, Johnson MR, Montero CI, Nelson KE, Kelly RM., FEMS Microbiol. Rev. 30(6), 2006
PMID: 17064285
Hydrogen transfer between methanogens and fermentative heterotrophs in hyperthermophilic cocultures.
Muralidharan V, Rinker KD, Hirsh IS, Bouwer EJ, Kelly RM., Biotechnol. Bioeng. 56(3), 1997
PMID: 18636642
Conversion processes in anaerobic digestion
Gujer W, Zehnder AJ., 1983
Kinetics of anaerobic treatment—a critical review
Pavlostathis SG, Giraldo-Gomez E., 1991
Acetate oxidation is the dominant methanogenic pathway from acetate in the absence of Methanosaetaceae.
Karakashev D, Batstone DJ, Trably E, Angelidaki I., Appl. Environ. Microbiol. 72(7), 2006
PMID: 16820524
Microbial community dynamics in replicate anaerobic digesters exposed sequentially to increasing organic loading rate, acidosis, and process recovery.
Goux X, Calusinska M, Lemaigre S, Marynowska M, Klocke M, Udelhoven T, Benizri E, Delfosse P., Biotechnol Biofuels 8(), 2015
PMID: 26288654
The development of artificial media for marine algae.
PROVASOLI L, MCLAUGHLIN JJ, DROOP MR., Arch Mikrobiol 25(4), 1957
PMID: 13403656
Trophic diversity in a Mediterranean food web-Stable isotope analysis of an ant community of an organic citrus grove
Platner C, Piñol J, Sanders D, Espadaler X., 2012
A simple method for the isolation and purification of total lipides from animal tissues.
FOLCH J, LEES M, SLOANE STANLEY GH., J. Biol. Chem. 226(1), 1957
PMID: 13428781
Colorimetric method for determination of sugars and related substances
DuBois M, Giles KA, Hamilton JK, Rebers PA, Smith F., 1956
Anaerobic co-digestion of pig manure and crude glycerol at mesophilic conditions: biogas and digestate.
Astals S, Nolla-Ardevol V, Mata-Alvarez J., Bioresour. Technol. 110(), 2012
PMID: 22341889
Organic and volatile acids
Clescerl LS, Greenberg AE, Eaton AD., 1999
DNA recovery from soils of diverse composition.
Zhou J, Bruns MA, Tiedje JM., Appl. Environ. Microbiol. 62(2), 1996
PMID: 8593035
Evaluation of general 16S ribosomal RNA gene PCR primers for classical and next-generation sequencing-based diversity studies.
Klindworth A, Pruesse E, Schweer T, Peplies J, Quast C, Horn M, Glockner FO., Nucleic Acids Res. 41(1), 2012
PMID: 22933715
Taxonomic analysis of the microbial community in stored sugar beets using high-throughput sequencing of different marker genes.
Liebe S, Wibberg D, Winkler A, Puhler A, Schluter A, Varrelmann M., FEMS Microbiol. Ecol. 92(2), 2016
PMID: 26738557
FLASH: fast length adjustment of short reads to improve genome assemblies.
Magoc T, Salzberg SL., Bioinformatics 27(21), 2011
PMID: 21903629
Search and clustering orders of magnitude faster than BLAST.
Edgar RC., Bioinformatics 26(19), 2010
PMID: 20709691
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