期刊论文详细信息
Biotechnology for Biofuels
Mechanism, kinetics and microbiology of inhibition caused by long-chain fatty acids in anaerobic digestion of algal biomass
Jingwei Ma1  Quan-Bao Zhao1  Lieve L. M. Laurens2  Eric E. Jarvis2  Nick J. Nagle2  Shulin Chen1  Craig S. Frear1 
[1] Department of Biological Systems Engineering, Washington State University, Pullman, WA, USA
[2] National Renewable Energy Laboratory, Golden, CO, USA
关键词: Microbial community;    Kinetic model;    Calcium;    LCFA inhibition;    Anaerobic digestion;    Algae;   
Others  :  1228139
DOI  :  10.1186/s13068-015-0322-z
 received in 2015-04-10, accepted in 2015-08-21,  发布年份 2015
PDF
【 摘 要 】

Background

Oleaginous microalgae contain a high level of lipids,which can be extracted and converted to biofuel. The lipid-extracted residue can then be further utilized through anaerobic digestion to produce biogas. However, long-chain fatty acids (LCFAs) have been identified as the main inhibitory factor on microbial activity of anaerobic consortium. In this study, the mechanism of LCFA inhibition on anaerobic digestion of whole and lipid-extracted algal biomass was investigated with a range of calcium concentrations against various inoculum to substrate ratios as a means to alleviate the LCFA inhibition.

Results

Whole algal biomass of Nannochloropsis salina represents high lipid content algal biomass while lipid-extracted residue represents its low lipid counterpart. The anaerobic digestion experiments were conducted in a series of serum bottles at 35 °C for 20 days. A kinetic model, considering LCFA inhibition on hydrolysis, acidogenesis as well as methanogenesis steps, was developed from the observed phenomenon of inhibition factors as a function of the LCFA concentration and specific biomass content or calcium concentration. The results showed that inoculum to substrate ratio had a stronger effect on biogas production than calcium, and calcium had no effect on biogas production when inoculum concentration was extremely low. The microbial community analysis by high-throughput Illumina Miseq sequencing indicated that diversity of both bacterial and methanogenic communities decreased with elevation of lipid concentration. Hydrolytic bacteria and aceticlastic methanogens dominated bacterial and archaea communities, respectively, in both high and low LCFA concentration digesters.

Conclusions

This study demonstrated that inoculum concentration has a more significant effect on alleviating LCFA inhibition than calcium concentration, while calcium only played a role when inoculum concentration met a threshold level. The model revealed that each functional microbial group was subject to different levels of LCFA inhibition. Although methanogens were the most susceptible microbes to LCFA inhibition, the inhibition factor for hydrolytic bacteria was more highly affected by inoculum concentration. The microbial community analysis indicated that the bacterial community was affected more than the methanogenic community by high LCFAs concentration. Syntrophic acetogens were sensitive to high LCFA concentrations and thus showed a decreased abundance in such an environment.

【 授权许可】

   
2015 Ma et al.

【 预 览 】
附件列表
Files Size Format View
20151010001637161.pdf 2256KB PDF download
Fig.6. 28KB Image download
Fig.5. 52KB Image download
Fig.4. 148KB Image download
Fig.3. 39KB Image download
Fig.2. 42KB Image download
Fig.1. 54KB Image download
【 图 表 】

Fig.1.

Fig.2.

Fig.3.

Fig.4.

Fig.5.

Fig.6.

【 参考文献 】
  • [1]Scott SA, Davey MP, Dennis JS, Horst I, Howe CJ, Lea-Smith DJ, et al.: Biodiesel from algae: challenges and prospects. Curr Opin Biotech 2010, 21(3):277-286.
  • [2]Zhao B, Ma J, Zhao Q, Laurens L, Jarvis E, Chen S, et al.: Efficient anaerobic digestion of whole microalgae and lipid-extracted microalgae residues for methane energy production. Bioresour Technol 2014, 161:423-430.
  • [3]Sialve B, Bernet N, Bernard O: Anaerobic digestion of microalgae as a necessary step to make microalgal biodiesel sustainable. Biotechnol Adv 2009, 27(4):409-416.
  • [4]Rinzema A, Boone M, Knippenberg Kv, Lettinga G: Bactericidal effect of long chain fatty acids in anaerobic digestion. Water Environ Res 1994, 66(1):40-49.
  • [5]Pavlostathis SG, Giraldo-Gomez E: Kinetics of anaerobic treatment: a critical review. Crit Rev Environ Control 1991, 21(5–6):411-490.
  • [6]Angelidaki I, Ahring BK: Effects of free long-chain fatty acids on thermophilic anaerobic digestion. Appl Microbiol Biotechnol 1992, 37(6):808-812.
  • [7]Alves MM, Mota Vieira JA, Álvares Pereira RM, Pereira MA, Mota M: Effects of lipids and oleic acid on biomass development in anaerobic fixed-bed reactors. Part II: oleic acid toxicity and biodegradability. Water Res 2001, 35(1):264-270.
  • [8]Hanaki K, Matsuo T, Nagase M: Mechanism of inhibition caused by long-chain fatty acids in anaerobic digestion process. Biotechnol Bioeng 1981, 23(7):1591-1610.
  • [9]Lalman J, Bagley DM: Effects of C18 long chain fatty acids on glucose, butyrate and hydrogen degradation. Water Res 2002, 36(13):3307-3313.
  • [10]Lalman JA, Bagley DM: Anaerobic degradation and inhibitory effects of linoleic acid. Water Res 2000, 34(17):4220-4228.
  • [11]Pereira M, Cavaleiro A, Mota M, Alves M: Accumulation of long chain fatty acids onto anaerobic sludge under steady state and shock loading conditions: effect on acetogenic and methanogenic activity. Water Sci Technol 2003, 48(6):33-40.
  • [12]Nielsen HB, Ahring BK: Responses of the biogas process to pulses of oleate in reactors treating mixtures of cattle and pig manure. Biotechnol Bioeng 2006, 95(1):96-105.
  • [13]Wu J-T, Chiang Y-R, Huang W-Y, Jane W-N: Cytotoxic effects of free fatty acids on phytoplankton algae and cyanobacteria. Aquat Toxicol 2006, 80(4):338-345.
  • [14]Zheng CJ, Yoo J-S, Lee T-G, Cho H-Y, Kim Y-H, Kim W-G: Fatty acid synthesis is a target for antibacterial activity of unsaturated fatty acids. FEBS Lett 2005, 579(23):5157-5162.
  • [15]Desbois A, Smith V: Antibacterial free fatty acids: activities, mechanisms of action and biotechnological potential. Appl Microbiol Biotechnol 2010, 85(6):1629-1642.
  • [16]Templer J, Lalman JA, Jing N, Ndegwa PM: Influence of C18 long chain fatty acids on hydrogen metabolism. Biotechnol Prog 2006, 22(1):199-207.
  • [17]Pereira MA, Sousa DZ, Mota M, Alves MM: Mineralization of LCFA associated with anaerobic sludge: Kinetics, enhancement of methanogenic activity, and effect of VFA. Biotechnol Bioeng 2004, 88(4):502-511.
  • [18]Pereira MA, Pires OC, Mota M, Alves MM: Anaerobic biodegradation of oleic and palmitic acids: evidence of mass transfer limitations caused by long chain fatty acid accumulation onto the anaerobic sludge. Biotechnol Bioeng 2005, 92(1):15-23.
  • [19]Zonta Ž, Alves MM, Flotats X, Palatsi J: Modelling inhibitory effects of long chain fatty acids in the anaerobic digestion process. Water Res 2013, 47(3):1369-1380.
  • [20]Fernández A, Sanchez A, Font X: Anaerobic co-digestion of a simulated organic fraction of municipal solid wastes and fats of animal and vegetable origin. Biochem Eng J 2005, 26(1):22-28.
  • [21]Palatsi J, Laureni M, Andrés M, Flotats X, Nielsen H, Angelidaki I: Strategies for recovering inhibition caused by long chain fatty acids on anaerobic thermophilic biogas reactors. Bioresour Technol 2009, 100(20):4588-4596.
  • [22]Cavaleiro A, Pereira M, Alves M: Enhancement of methane production from long chain fatty acid based effluents. Bioresour Technol 2008, 99(10):4086-4095.
  • [23]Roy F, Albagnac G, Samain E: Influence of calcium addition on growth of highly purified syntrophic cultures degrading long-chain fatty acids. Appl Environ Microbiol 1985, 49(3):702-705.
  • [24]Hatamoto M, Imachi H, Ohashi A, Harada H: Identification and cultivation of anaerobic, syntrophic long-chain fatty acid-degrading microbes from mesophilic and thermophilic methanogenic sludges. Appl Environ Microbiol 2007, 73(4):1332-1340.
  • [25]Ahn J-H, Do TH, Kim SD, Hwang S: The effect of calcium on the anaerobic digestion treating swine wastewater. Biochem Eng J 2006, 30(1):33-38.
  • [26]Koster IW, Cramer A: Inhibition of methanogenesis from acetate in granular sludge by long-chain fatty acids. Appl Environ Microbiol 1987, 53(2):403-409.
  • [27]Neves L, Oliveira R, Alves MM: Fate of LCFA in the co-digestion of cow manure, food waste and discontinuous addition of oil. Water Res 2009, 43(20):5142-5150.
  • [28]Astals S, Batstone DJ, Mata-Alvarez J, Jensen PD: Identification of synergistic impacts during anaerobic co-digestion of organic wastes. Bioresour Technol 2014, 169:421-427.
  • [29]Palatsi J, Illa J, Prenafeta-Boldú FX, Laureni M, Fernandez B, Angelidaki I, et al.: Long-chain fatty acids inhibition and adaptation process in anaerobic thermophilic digestion: batch tests, microbial community structure and mathematical modelling. Bioresour Technol 2010, 101(7):2243-2251.
  • [30]Angelidaki I, Ellegaard L, Ahring BK: A comprehensive model of anaerobic bioconversion of complex substrates to biogas. Biotechnol Bioeng 1999, 63(3):363-372.
  • [31]Wakelin NG, Forster CF: An investigation into microbial removal of fats, oils and greases. Bioresour Technol 1997, 59(1):37-43.
  • [32]Mongkolthanaruk W, Dharmsthiti S: Biodegradation of lipid-rich wastewater by a mixed bacterial consortium. Int Biodeterior Biodegrad 2002, 50(2):101-105.
  • [33]Assih EA, Ouattara AS, Thierry S, Cayol J-L, Labat M, Macarie H: Stenotrophomonas acidaminiphila sp. nov., a strictly aerobic bacterium isolated from an upflow anaerobic sludge blanket (UASB) reactor. Int J Syst Evol Microbiol 2002, 52(2):559-568.
  • [34]Zamalloa C, De Vrieze J, Boon N, Verstraete W: Anaerobic digestibility of marine microalgae Phaeodactylum tricornutum in a lab-scale anaerobic membrane bioreactor. Appl Microbiol Biotechnol 2012, 93(2):859-869.
  • [35]Labatut R, Angenent L, Scott N: Biochemical methane potential and biodegradability of complex organic substrates. Bioresour Technol 2011, 102(3):2255-2264.
  • [36]APHA: Methods for examination of water and wasterwater. 20th edition. American Public Health Association/American Water Works Association/Water Environment Federation, Washington, DC; 1998.
  • [37]Ma J, Yu L, Frear C, Zhao Q, Li X, Chen S: Kinetics of psychrophilic anaerobic sequencing batch reactor treating flushed dairy manure. Bioresour Technol 2013, 131:6-12.
  • [38]Laurens LL, Quinn M, Wychen S, Templeton D, Wolfrum E: Accurate and reliable quantification of total microalgal fuel potential as fatty acid methyl esters by in situ transesterification. Anal Bioanal Chem 2012, 403(1):167-178.
  • [39]Lourenço SO, Barbarino E, Lavín PL, Lanfer Marquez UM, Aidar E: Distribution of intracellular nitrogen in marine microalgae: calculation of new nitrogen-to-protein conversion factors. Eur J Phycol 2004, 39(1):17-32.
  • [40]Laurens LM, Dempster TA, Jones HD, Wolfrum EJ, Van Wychen S, McAllister JS, et al.: Algal biomass constituent analysis: method uncertainties and investigation of the underlying measuring chemistries. Anal Chem 2012, 84(4):1879-1887.
  • [41]Huber JA, Mark Welch DB, Morrison HG, Huse SM, Neal PR, Butterfield DA, et al.: Microbial population structures in the deep marine biosphere. Science 2007, 318(5847):97-100.
  • [42]Marteinsson VT, Runarsson A, Stefansson A, Thorsteinsson T, Johannesson T, Magnusson SH et al (2013) Microbial communities in the subglacial waters of the Vatnajokull ice cap, Iceland. ISME J. 7(2):427–437.. http://www.nature.com/ismej/journal/v7/n2/suppinfo/ismej201297s1.html webcite
  • [43]Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Huntley J, Fierer N et al (2012) Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. ISME J 6(8):1621–1624.. http://www.nature.com/ismej/journal/v6/n8/suppinfo/ismej20128s1.html webcite
  • [44]Magoč T, Salzberg SL: FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics 2011, 27(21):2957-2963.
  • [45]Wang Q, Garrity GM, Tiedje JM, Cole JR: Naïve Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 2007, 73(16):5261-5267.
  • [46]Vavilin VA, Fernandez B, Palatsi J, Flotats X: Hydrolysis kinetics in anaerobic degradation of particulate organic material: an overview. Waste Manag 2008, 28(6):939-951.
  • [47]Ramirez I, Mottet A, Carrère H, Déléris S, Vedrenne F, Steyer J-P: Modified ADM1 disintegration/hydrolysis structures for modeling batch thermophilic anaerobic digestion of thermally pretreated waste activated sludge. Water Res 2009, 43(14):3479-3492.
  • [48]Gavala H, Angelidaki I, Ahring B. Kinetics and Modeling of Anaerobic Digestion Process. In: Ahring B, Angelidaki I, Macario EC, Gavala HN, Hofman-Bang J, Macario AJL et al (2003) Biomethanation I. Advances in Biochemical Engineering/Biotechnology. Springer Berlin Heidelberg, pp 57–93
  • [49]Zhang P, Chen Y, Zhou Q, Zheng X, Zhu X, Zhao Y: Understanding short-chain fatty acids accumulation enhanced in waste activated sludge alkaline fermentation: kinetics and microbiology. Environ Sci Technol 2010, 44(24):9343-9348.
  • [50]Tartakovsky B, Mu SJ, Zeng Y, Lou SJ, Guiot SR, Wu P: Anaerobic digestion model No. 1-based distributed parameter model of an anaerobic reactor: II. Model validation. Bioresour Technol 2008, 99(9):3676-3684.
  • [51]Reichert P (1998) AQUASIM 2.0: Computer program for the identification and simulation of aquatic systems. Swiss Federal Institute for Environmental Science and Technology (EAWAG) Dubendorf, Switzerland
  • [52]Blumensaat F, Keller J: Modelling of two-stage anaerobic digestion using the IWA Anaerobic Digestion Model No. 1 (ADM1). Water Res 2005, 39(1):171-183.
  • [53]Batstone DJ, Keller J, Angelidaki I, Kalyuzhnyi SV, Pavlostathis SG, Rozzi A et al (2002) Anaerobic digestion model no.1. Scientific and Technical Report 9. International Water Association (IWA), London
  • [54]Siegrist H, Vogt D, Garcia-Heras JL, Gujer W: Mathematical Model for Meso- and Thermophilic Anaerobic Sewage Sludge Digestion. Environ Sci Technol 2002, 36(5):1113-1123.
  文献评价指标  
  下载次数:48次 浏览次数:14次