Bacterial community composition and fhs profiles of low- and high-ammonia biogas digesters reveal novel syntrophic acetate-oxidising bacteria

Biotechnology for Biofuels

Volumn 9, Issue 1, 2016, Pages

  Müller, Bettina ^a   Sun, Li ^a   Westerholm, Maria ^a   Schnürer, Anna ^a  

^a SWEDISH UNIVERSITY OF AGRICULTURAL SCIENCES   (Sweden)

Author keywords

Acetogens; Ammonia inhibition; Anaerobic degradation; Biogas production; Formyltetrahydrofolate synthetase; Illumina amplicon sequencing; Syntrophic acetate oxidation

Indexed keywords

ANAEROBIC DIGESTION; BACTERIA; BIOGAS; GENE ENCODING; METABOLISM; POLYMERASE CHAIN REACTION; PULP DIGESTERS;

ACETOGENS; AMMONIA INHIBITION; AMPLICONS; ANAEROBIC DEGRADATION; BIOGAS PRODUCTION; SYNTHETASES; SYNTROPHIC ACETATE OXIDATIONS;

AMMONIA;

ACETATE; AMMONIA; ANAEROBIC DIGESTION; BACTERIUM; BIODEGRADATION; BIOGAS; COMMUNITY COMPOSITION; ENZYME; MICROBIAL COMMUNITY; OXIDATION;

BACTERIA (MICROORGANISMS); CLOSTRIDIA; CLOSTRIDIALES;

EID: 84979539115     PISSN: 17546834     EISSN: None     Source Type: Journal    
DOI: 10.1186/s13068-016-0454-9     Document Type: Article

References (78)

1. Mackie RI, Bryant MP. Metabolic activity of fatty acid-oxidizing bacteria and the contribution of acetate, propionate, butyrate, and CO2 to methanogenesis in cattle waste at 40 and 60 °C. Appl Environ Microbiol. 1981;41:1363-73.
2. Mountfort DO, Asher RA. Changes in proportions of acetate and carbon dioxide used as methane precursors during the anaerobic digestion of bovine waste. Appl Environ Microbiol. 1978;35:648-54.
3. Zinder SH, Koch M. Non-aceticlastic methanogenesis from acetate: acetate oxidation by a thermophilic syntrophic coculture. Arch Microbiol. 1984;138:263-72.
4. Hattori S. Syntrophic acetate-oxidizing microbes in methanogenic environments. Microbes Environ. 2008;23:118-27
5. Sprott GD, Patel GB. Ammonia toxicity in pure cultures of methanogenic bacteria. Syst Appl Microbiol. 1986;7:358-63.
6. Steinhaus B, Garcis ML, Shen AQ, Angenent LT. A portable anaerobic microbioreactor reveals optimum growth conditions for the methanogen Methanosaeta concilii. Appl Environ Microbiol. 2007;73:1653-8.
7. Schnürer A, Nordberg A. Ammonia, a selective agent for methane production by syntrophic acetate oxidation at mesophilic temperature. Water Sci Technol. 2008;57:735-40.
8. Schnürer A, Zellner G, Svensson BH. Mesophilic syntrophic acetate oxidation during methane formation in biogas reactors. FEMS Microbiol Ecol. 1999;29:249-61.
9. Westerholm M, Levén L, Schnürer A. Bioaugmentation of syntrophic acetate-oxidising culture in biogas reactors exposed to increasing levels of ammonia. Appl Environ Microbiol. 2012;78:7619-25.
10. Angenent LT, Sung S, Raskin L. Methanogenic population dynamics during startup of a full-scale anaerobic sequencing batch reactor treating swine waste. Water Res. 2002;36:4648-54.
11. Shimada T, Morgenroth E, Tandukar M, Pavlostathis SG, Smith A, Raskin L, Kilian RE. Syntrophic acetate oxidation in two-phase (acid-methane) anaerobic digesters. Water Sci Technol. 2011;64:1812-20.
12. Sun L, Müller B, Westerholm M, Schnürer A. Syntrophic acetate oxidation in industrial CSTR biogas digesters. J Biotechnol. 2014;171:39-44.
13. Fotidis IA, Karakashev D, Angelidaki I. The dominant acetate degradation pathway/methanogenic composition in full-scale anaerobic digesters operating under different ammonia levels. Int J Environ Sci Technol. 2014;11:2087-94.
14. Ahring BK, Schmidt JE, Winther-Nielsen M, Macarion AJL, Conway de Macario E. Effect of the medium composition and sludge removal on the production, composition and architecture of thermophilic (55 °C) acetate-utilizing granules from an upflow anaerobic sludge blanket reactor. Appl Environ Microbiol. 1993;59:2538-44.
15. Hao L, Lü F, He P, Li L, Shao L. Predominant contribution of syntrophic acetate oxidation to thermophilic methane formation at high acetate concentrations. Environ Sci Technol. 2011;45:508-13.
16. Karakashev D, Batstone DJ, Trably E, Angelidaki I. Acetate oxidation is the dominant methanogenic pathway from acetate in the absence of Methanosaetaceae. Appl Environ Microbiol. 2006;72:5138-41.
17. Petersen SP, Ahring BK. Acetate oxidation in a thermophilic anaerobic sludge-digestor: the importance of non-acetoclastic methanogenesis from acetate. FEMS Microbiol Ecol. 1991;86:149-58.
18. Shigematsu T, Tang Y, Kobayashi T, Kawaguchi H, Morimura S, Kida K. Effect of dilution rate on metabolic pathway shift between aceticlastic and nonacetoclastic methanogenesis in chemostat cultivation. Appl Environ Microbiol. 2004;70:4048-52.
19. Mayumi D, Dolfing J, Sakata S, Maeda H, Miyagawa Y, Ikarashi M, Tamaki H, Takeuchi M, Nakatsu CH, Kamagata Y. Carbon dioxide concentration dictates alternative methanogenic pathways in oil reservoirs. Nat Commun. 2013;4:1-6.
20. Balk M, Weijma J, Stams AJM. Thermotoga lettingae sp. nov., a novel thermophilic, methanol-degrading bacterium isolated from a themophilic anaerobic reactor. Int J Syst Evol Microbiol. 2002;52:1361-8.
21. Hattori S, Kamagata Y, Hanada S, Shoun H. Thermacetogenium phaeum gen. nov., sp. nov., a strictly anaerobic, thermophilic, syntrophic acetate-oxidizing bacterium. Int J Syst Evol Microbiol. 2000;50:1601-9.
22. Schnürer A, Schink B, Svensson BH. Clostridium ultunense sp. nov., a mesophilic bacterium oxidizing acetate in syntrophic association with a hydrogenotrophic methanogenic bacterium. Int J Syst Bacteriol. 1996;46:1145-52.
23. Westerholm M, Roos S, Schnürer A. Syntrophaceticus schinkii gen. nov., sp. nov., an anaerobic, syntrophic acetate-oxidizing bacterium isolated from a mesophilic anaerobic filter. FEMS Microbiol Lett. 2010;309:100-4.
24. Westerholm M, Roos S, Schnürer A. Tepidanaerobacter acetatoxydans sp. nov., an anaerobic, syntrophic acetate-oxidizing bacterium isolated from two ammonium-enriched mesophilic methanogenic processes. Syst Appl Microbiol. 2011;34:260-6.
25. Drake HL, Küsel K, Matthies C. Acetogenic prokaryotes. 3rd ed. New York: Springer; 2006.
26. Hattori S, Galushko AS, Kamagata Y, Schink B. Operation of the CO dehydrogenase/acetyl coenzyme A pathway in both acetate oxidation and acetate formation by the syntrophically acetate-oxidizing bacterium Thermacetogenium phaeum. J Bacteriol. 2005;187:3471-6.
27. Oehler D, Poehlein A, Leimbach A, Müller N, Daniel R, Gottschalk G, Schink B. Genome-guided analysis of physiological and morphological traits of the fermentative acetate oxidizer Thermacetogenium phaeum. BMC Genomics. 2012;13:723.
28. Schnürer A, Svensson BH, Schink B. Enzyme activities in and energetics of acetate metabolism by the mesophilic syntrophically acetate-oxidizing anaerobe Clostridium ultunense. FEMS Microbiol Lett. 1997;154:331-6.
29. Müller B, Manzoor S, Niazi A, Bongcam-Rudloff E, Schnürer A. Genome-guided analysis of physiological capacities of Tepidanaerobacter acetatoxydans provides insights into environmental adaptations and syntrophic acetate oxidation. PLoS ONE. 2015;10:1-21.
30. Nobu MK, Narihiro T, Rinke C, Kamagata Y, Tringe SG, Woyke T, Liu W. Microbial dark matter ecogenomics reveals complex synergistic network in a methanogenic bioreactor. ISME J. 2015;9:1710-22.
31. Müller B, Sun L, Schnürer A. First insights into the syntrophic acetate-oxidizing bacteria - a genetic study. MicrobiologyOpen. 2012;2:35-53.
32. Leaphart AB, Lovell CR. Recovery and analysis of formyltetrahydrofolate synthetase gene sequences from natural populations of acetogenic bacteria. Appl Environ Microbiol. 2001;67:1392-5.
33. Henderson G, Naylor GE, Leahy SC, Janssen PH. Presence of novel, potentially homoacetogenic bacteria in the rumen as determined by analysis of formyltetrahydrofolate synthetase sequences from ruminants. Appl Environ Microbiol. 2010;76:2058-66.
34. Matsui H, Kojima N, Tajima K. Diversity of the formyltetrahydrofolate synthetase gene (fhs), a key enzyme for reductive acetogenesis, in the bovine rumen. Biosci Biotechnol Biochem. 2008;72:3273-6.
35. Leaphart AB, Friez MJ, Lovell CR. Formyltetrahydrofolate synthetase sequences from salt marsh plant roots reveal a diversity of acetogenic bacteria and other bacterial functional groups. Appl Environ Microbiol. 2003;69:693-6.
36. Ottesen EA, Leadbetter JR. Diversity of formyltetrahydrofolate synthetases in the guts of the wood-feeding cockroach Cryptocercus punctulatus and the omnivorous cockroach Periplaneta americana. Appl Environ Microbiol. 2010;76:4909-13.
37. Ottesen EA, Leadbetter JR. Formyltetrahydrofolate synthetase gene diversity in the guts of higher termites with different diets and lifestyles. Appl Environ Microbiol. 2011;77:3461-7.
38. Pester M, Brune A. Expression profiles of fhs (FTHFS) genes support the hypothesis that spirochaetes dominate reductive acetogenesis in the hindgut of lower termites. Environ Microbiol. 2006;8:1261-70.
39. Salmassi TM, Leadbetter JR. Analysis of genes of tetrahydrofolate-dependent metabolism from cultivated spirochaetes and the gut community of the termite Zootermopsis angusticollis. Microbiol. 2003;149:2529-37.
40. Hori T, Sasaki D, Haruta S, Shigematsu T, Ueno Y, Ishii M, Igarashi Y. Detection of active, potentially acetate-oxidizing syntrophs in an anaerobic digester by flux measurement and formyltetrahydrofolate synthetase (FTHFS) expression profiling. Microbiology. 2011;157:1980-9.
41. Ryan P, Forbes C, Colleran E. Investigation of the diversity of homoacetogenic bacteria in mesophilic and thermophilic anaerobic sludges using the formyltetrahydrofolate synthetase gene. Water Sci Technol. 2008;57:675-80.
42. Ryan P, Forbes C, McHugh S, O'Reilly C, Fleming GTA, Colleran E. Enrichment of acetogenic bacteria in high rate anaerobic reactors under mesophilic and thermophilic conditions. Water Res. 2010;44:4261-9.
43. Westerholm M, Müller B, Arthurson V, Schnürer A. Changes in the acetogenic population in a mesophilic anaerobic digester in response to increasing ammonia concentration. Microbes Environ. 2011;26:347-53.
44. Xu K, Liu H, Du G, Chen J. Real-time PCR assays targeting formyltetrahydrofolate synthetase gene to enumerate acetogens in natural and engineered environmants. Anaerobe. 2009;15:204-13.
45. Gagen EJ, Denman SE, Padmanabha J, Zadbuke S, Al Jassim R, Morrision M, McSweeney CS. Functional gene analysis suggests different acetogen populations in the bovine rumen and tammar wallaby forestomach. Appl Environ Microbiol. 2010;76:7785-95.
46. Westerholm M, Dolfing J, Sherry A, Gray ND, Head IM, Schnürer A. Quantification of syntrophic acetate-oxidizing microbial communities in biogas processes. Environ Microbiol Rep. 2011;3:500-5.
47. Moestedt J, Müller B, Westerholm M, Schnürer A. Ammonia threshold for inhibition of anaerobic digestion of thin stillage and the importance of organic loading rate. Microb Biotechnol. 2015. doi: 10.1111/1751-7915.12330.
48. Westerholm M, Müller B, Isaksson S, Schnürer A. Trace element and temperature effects on microbial communities and links to biogas digester performance at high ammonia levels. Biotechnol Biofuel. 2015;8:1-19.
49. Snauwaert I, Stragier P, De Vuyst L, Vandammel P. Comparative genomw analysis of Pediococcus damnosus LMG 28219, a strain well-adapted to the beer environment. BMC Genom. 2015;16:1-12.
50. Hädrich A, Heuer VB, Herrmann M, Hinrichs K, Küsel K. Origin and fate of acetate in an acidic fen. FEMS Microbiol Ecol. 2012;81:339-54.
51. Hunger S, Schmidt O, Hilgarth M, Horn MA, Kolb S, Conrad R, Drake HL. Competing formate- and carbon dioxide-utilizing prokaryotes in an anoxic methane-emitting fen soil. Appl Environ Microbiol. 2011;77:3773-85.
52. Lever MA, Heuer VB, Morono Y, Masui N, Schmidt F, Alperin MJ, Inagaki F, Hinrichs K, Teske A. Acetogenesis in deep subseafloor sediments of the Juan de Fuca Ridge flank: a synthesis of geochemical, thermodynamic, and gene-based evidence. Geomicrobiol J. 2010;27:183-211.
53. Matsui H, Yoneda S, Ban-Tokuda T, Wakita M. Diversity of the formyltetrahydrofolate synthetase (FTHFS) gene in the proximal and mid ostrich colon. Curr Microbiol. 2011;62:1-6.
54. Werner JJ, Garcia ML, Perkins SD, Yarasheski KE, Smith SR, Muegge B, Stadermann FJ, DeRito CM, Floss C, Madsen EL, et al. Microbial community dynamics and stability during an ammonia-induced shift to syntrophic acetate oxidation. Appl Environ Microbiol. 2014;80:3375-83.
55. Hahnke S, Maus I, Wibber D, Tomazetto G, Pühler A, Klocke M, Schlüter A. Complete genome sequence of the novel Porphyromonadaceae bacterium strain ING2-E5B isolated from a mesophilic lab-scale biogas reactor. J Biotechnol. 2015;193:34-6.
56. Chen S, Dong X. Proteiniphilum acetatigenes gen. nov., sp. nov., from a UASB reactor treating brewery wastewater. Int J Syst Evol Microbiol. 2005;55:2257-61.
57. Schaal KP, Yassin AF, Stackebrandt E. The family Actinomycetaceae: the genera Actinomyces, Actinobaculum, Arcanobacterium, Varibaculum, and Mobiluncus. In: Balows A, Truper HG, Dworkin M, Harder W, Schleifer KH, editors. The prokaryotes: a handbook on the biology of bacteria. 2nd ed. Berlin: Springer; 2006. p. 430-537.
58. Bouanane-Darenfed A, Fardeau ML, Grégoire P, Joseph M, Kebbouche-Gana S, Benayad T, Hacene H, Cayol JL, Ollivier B. Caldicoprobacter algeriensis sp. nov. a new thermophilic anaerobic, xylanolytic bacterium isolated from an Algerian hot spring. Curr Microbiol. 2011;62:826-32.
59. Bouanane-Darenfed A, Ben Hania W, Hacene H, Cayol JL, Ollivier B, Fardeau ML. Caldicoprobacter guelmensis sp. nov., a thermophilic, anaerobic, xylanolytic bacterium isolated from a hot spring. Int J Syst Evol Microbiol. 2013;63:2049-53.
60. Hammes WP, Hertel C. Genus I. Lactobacillus Beijerink. 2nd ed. New York: Springer; 1901. p. 2009.
61. Francisci DD, Kougias PG, Treu L, Campanaro S, Angelidaki I. Microbial diversity and dynamicity of biogas reactors due to radical changes of feedstock composition. Bioresour Technol. 2015;176:56-64.
62. Sträuber H, Lucas R, Kleinsteuber S. Metabolic and microbial community dynamics during the anaerobic digestion of maize silage in a two-phase process. Bioenerg Biofuel. 2016;100:479-91.
63. Park D, Lee WJ, Jang I, Lee W. Got Lactobacillus? Commensals power growth. Cell Host Microbe. 2015;18:388-90.
64. Bassani I, Kougias PG, Treu L, Angelidaki I. Biogas upgrading via hydrogenotrophic methanogenesis in two-stage continuous stirred tank reactors at mesophilic and thermophilic conditions. Environ Sci Technol. 2015;49:12585-93.
65. Lee S, Park J, Kim SH, Yu BJ, Yoon J, Park H. Evidence off syntrophic acetate oxidation by Spirochaetes during anaerobic methane production. Bioresour Technol. 2015;190:543-9.
66. Levén L, Eriksson A, Schnürer A. Effect of process temperature on bacterial and archaeal communities in two methanogenic bioreactors treating organic household waste. FEMS Microbiol Ecol. 2007;59:683-93.
67. Rozen S, Skaletsky H. Primer3 on the WWW for general users and for biologist programmers. Methods Mol Biol. 2000;132:365-86
68. Katoh K, Kuma K, Toh H, Miyata T. MAFFT version 5: improvement in accuracy of multiple sequence alignment. Nucliec Acids Res. 2005;33:511-8.
69. Guindon S, Gascuel O. A simple, fast and accurate algorithm to estimate large phylogenies by maximum Likelihood. Syst Biol. 2003;52:696-704.
70. Hugerth LW, Wefer HA, Lundin S, Jakobsson HE, Lindberg M, Rodin S, Engstrand L, Andersson AF. DegePrime, a program for degenerate primer design for broad-taxonomic range PCR in microbial ecology studies. Appl Environ Microbiol. 2014;80:5116-23.
71. Martin M. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet.journal. 2011;17:10-2.
72. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Pena AG, Goodrich JK, Gordon JI, et al. QIIME allows analysis of high-throughput community sequencing data. Nat Methods. 2010;7:335-6.
73. Rideout JR, He Y, Navas-Molina JA, Walters WA, Ursell LK, Gibbons SM, Chase J, McDonald D, Gonzalez A, Robbins-Pianka A, et al. Subsampled open-reference clustering creates consistent, comprehensive OTU definitions and scales to billions of sequences. PeerJ. 2014;2:e545.
74. Edgar RC. Search and clustering orders of magnitude faster than BLAST. Bioinformatics. 2010;26:2460-1.
75. Caporaso JG, Bittinger K, Bushman FD, DeSantis TZ, Andersen GL, Knight R. PyNAST: a flexible tool for aligning sequences to a template alignment. Bioinformatics. 2010;26:266-7.
76. Haas BJ, Gevers D, Earl AM, Feldgarden M, Ward DV, Giannoukos G, Ciulla D, Tabbaa D, Highlander SK, Sodergren E. Chimeric 16S rRNA sequence formation and detection in Sanger and 454-pyrosequenced PCR amplicons. Genome Res. 2011;21:494-504.
77. 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;73:5261-7.
78. Price MN, Dehal PS, Arkin AP. FastTree 2 - approximately maximum-likelihood trees for large alignments. PLoS One. 2010;5:e9490.