Metagenomic analysis and functional characterization of the biogas microbiome using high throughput shotgun sequencing and a novel binning strategy

Biotechnology for Biofuels

Volumn 9, Issue 1, 2016, Pages

  Campanaro, Stefano ^a   Treu, Laura ^b   Kougias, Panagiotis G ^b   De Francisci, Davide ^b   Valle, Giorgio ^a   Angelidaki, Irini ^b  

^a UNIVERSITY OF PADOVA   (Italy)

^b TECHNICAL UNIVERSITY OF DENMARK   (Denmark)

Author keywords

Anaerobic digestion; Archaea; Bacteria; Binning; Biogas; Metagenomics; Methanogens; Microbial community structure; Next generation sequencing

Indexed keywords

BACTERIA; BINS; BIOGAS; BIOLOGY; COMPLEX NETWORKS; FATTY ACIDS; GENES; METABOLISM; METHANOGENS; MICROORGANISMS; THROUGHPUT;

ARCHAEA; BINNING; METAGENOMICS; MICROBIAL COMMUNITY STRUCTURES; NEXT-GENERATION SEQUENCING;

ANAEROBIC DIGESTION;

ANOXIC CONDITIONS; BACTERIUM; BIOGAS; COMMUNITY STRUCTURE; GENOME; METHANOGENESIS; MICROBIAL COMMUNITY; PHYLOGENY; TAXONOMY;

BACTERIA (MICROORGANISMS); UNCULTURED ARCHAEON;

EID: 84957001273     PISSN: 17546834     EISSN: None     Source Type: Journal    
DOI: 10.1186/s13068-016-0441-1     Document Type: Article

References (82)

1. Holm-Nielsen JB, Al Seadi T, Oleskowicz-Popiel P. The future of anaerobic digestion and biogas utilization. Bioresour Technol. 2009;100(22):5478-84.
2. Batstone DJ, Keller J, Angelidaki I, Kalyuzhnyi S, Pavlostathis S, Rozzi A, Sanders W, Siegrist H, Vavilin V. The IWA Anaerobic Digestion Model No 1 (ADM 1). Water Sci Technol. 2002;45(10):65-73.
3. De Francisci D, 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.
4. Eikmeyer FG, Rademacher A, Hanreich A, Hennig M, Jaenicke S, Maus I, Wibberg D, Zakrzewski M, Pühler A, Klocke M. Detailed analysis of metagenome datasets obtained from biogas-producing microbial communities residing in biogas reactors does not indicate the presence of putative pathogenic microorganisms. Biotechnol Biofuels. 2013;6(1):49.
5. Schlüter A, Bekel T, Diaz NN, Dondrup M, Eichenlaub R, Gartemann K-H, Krahn I, Krause L, Krömeke H, Kruse O. The metagenome of a biogas-producing microbial community of a production-scale biogas plant fermenter analysed by the 454-pyrosequencing technology. J Biotechnol. 2008;136(1):77-90.
6. Wirth R, Kovács E, Maróti G, Bagi Z, Rákhely G, Kovács KL. Characterization of a biogas-producing microbial community by short-read next generation DNA sequencing. Biotechnol Biofuels. 2012;5(1):41.
7. Howe AC, Jansson JK, Malfatti SA, Tringe SG, Tiedje JM, Brown CT. Tackling soil diversity with the assembly of large, complex metagenomes. Proc Natl Acad Sci. 2014;111(13):4904-9.
8. Bremges A, Maus I, Belmann P, Eikmeyer F, Winkler A, Albersmeier A, Pühler A, Schlüter A, Sczyrba A. Deeply sequenced metagenome and metatranscriptome of a biogas-producing microbial community from an agricultural production-scale biogas plant. Gigascience. 2015;4:33.
9. Krause L, Diaz NN, Edwards RA, Gartemann K-H, Krömeke H, Neuweger H, Pühler A, Runte KJ, Schlüter A, Stoye J. Taxonomic composition and gene content of a methane-producing microbial community isolated from a biogas reactor. J Biotechnol. 2008;136(1):91-101.
10. Kröber M, Bekel T, Diaz NN, Goesmann A, Jaenicke S, Krause L, Miller D, Runte KJ, Viehöver P, Pühler A. Phylogenetic characterization of a biogas plant microbial community integrating clone library 16S-rDNA sequences and metagenome sequence data obtained by 454-pyrosequencing. J Biotechnol. 2009;142(1):38-49.
11. Langille MG, Zaneveld J, Caporaso JG, McDonald D, Knights D, Reyes JA, Clemente JC, Burkepile DE, Thurber RLV, Knight R. Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences. Nat Biotechnol. 2013;31(9):814-21.
12. Wommack KE, Bhavsar J, Ravel J. Metagenomics: read length matters. Appl Environ Microbiol. 2008;74(5):1453-63.
13. Kougias PG, De Francisci D, Treu L, Campanaro S, Angelidaki I. Microbial analysis in biogas reactors suffering by foaming incidents. Bioresour Technol. 2014;167:24-32.
14. Riviere D, Desvignes V, Pelletier E, Chaussonnerie S, Guermazi S, Weissenbach J, Li T, Camacho P, Sghir A. Towards the definition of a core of microorganisms involved in anaerobic digestion of sludge. ISME J. 2009;3(6):700-14.
15. Iverson V, Morris RM, Frazar CD, Berthiaume CT, Morales RL, Armbrust EV. Untangling genomes from metagenomes: revealing an uncultured class of marine Euryarchaeota. Science. 2012;335(6068):587-90.
16. Albertsen M, Hugenholtz P, Skarshewski A, Nielsen KL, Tyson GW, Nielsen PH. Genome sequences of rare, uncultured bacteria obtained by differential coverage binning of multiple metagenomes. Nat Biotechnol. 2013;31(6):533-8.
17. Nielsen HB, Almeida M, Juncker AS, Rasmussen S, Li J, Sunagawa S, Plichta DR, Gautier L, Pedersen AG, Le Chatelier E. Identification and assembly of genomes and genetic elements in complex metagenomic samples without using reference genomes. Nat Biotechnol. 2014;32(8):822-8.
18. Wang Y, Leung HC, Yiu S-M, Chin FY. MetaCluster 5.0: a two-round binning approach for metagenomic data for low-abundance species in a noisy sample. Bioinformatics. 2012;28(18):i356-62.
19. Alneberg J, Bjarnason BS, de Bruijn I, Schirmer M, Quick J, Ijaz UZ, Lahti L, Loman NJ, Andersson AF, Quince C. Binning metagenomic contigs by coverage and composition. Nat Methods. 2014;11(11):1144-6.
20. Imelfort M, Parks D, Woodcroft BJ, Dennis P, Hugenholtz P, Tyson GW. GroopM: an automated tool for the recovery of population genomes from related metagenomes. PeerJ. 2014;2:e603.
21. Kang DD, Froula J, Egan R, Wang Z. MetaBAT, an efficient tool for accurately reconstructing single genomes from complex microbial communities. PeerJ. 2015;3:e1165.
22. Galperin MY, Makarova KS, Wolf YI, Koonin EV. Expanded microbial genome coverage and improved protein family annotation in the COG database. Nucleic acids research. 2014; gku1223.
23. Kanehisa M, Goto S, Sato Y, Kawashima M, Furumichi M, Tanabe M. Data, information, knowledge and principle: back to metabolism in KEGG. Nucleic Acids Res. 2014;42(D1):D199-205.
24. Finn RD, Bateman A, Clements J, Coggill P, Eberhardt RY, Eddy SR, Heger A, Hetherington K, Holm L, Mistry J. Pfam: the protein families database. Nucleic Acids Res. 2013; gkt1223.
25. Graham DE, White RH. Elucidation of methanogenic coenzyme biosyntheses: from spectroscopy to genomics. Nat Prod Rep. 2002;19(2):133-47.
26. Drzyzga O, Bruns-Nagel D, Gorontzy T, Blotevogel K-H, Gemsa D, von Löw E. Mass balance studies with 14C-labeled 2, 4, 6-trinitrotoluene (TNT) mediated by an anaerobic Desulfovibrio species and an aerobic Serratia species. Curr Microbiol. 1998;37(6):380-6.
27. Fleischmann TJ, Walker KC, Spain JC, Hughes JB, Craig AM. Anaerobic transformation of 2, 4, 6-TNT by bovine ruminal microbes. Biochem Biophys Res Commun. 2004;314(4):957-63.
28. Lewis TA, Goszczynski S, Crawford RL, Korus RA, Admassu W. Products of Anaerobic 2, 4, 6-Trinitrotoluene (TNT) Transformation by Clostridium bifermentans. Appl Environ Microbiol. 1996;62(12):4669-74.
29. Kotrba P, Inui M, Yukawa H. Bacterial phosphotransferase system (PTS) in carbohydrate uptake and control of carbon metabolism. J Biosci Bioeng. 2001;92(6):502-17.
30. Tsapekos P, Kougias PG, Angelidaki I. Anaerobic mono- and co-digestion of mechanically pretreated meadow grass for biogas production. Energy Fuels. 2015;29(7):4005-10.
31. Werner JJ, Knights D, Garcia ML, Scalfone NB, Smith S, Yarasheski K, Cummings TA, Beers AR, Knight R, Angenent LT. Bacterial community structures are unique and resilient in full-scale bioenergy systems. Proc Natl Acad Sci. 2011;108(10):4158-63.
32. Dupont CL, Rusch DB, Yooseph S, Lombardo M-J, Richter RA, Valas R, Novotny M, Yee-Greenbaum J, Selengut JD, Haft DH. Genomic insights to SAR86, an abundant and uncultivated marine bacterial lineage. ISME J. 2012;6(6):1186-99.
33. Parks DH, Imelfort M, Skennerton CT, Hugenholtz P, Tyson GW. CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes. Genome Res. 2015;25(7):1043-55.
34. Rinke C, Schwientek P, Sczyrba A, Ivanova NN, Anderson IJ, Cheng J-F, Darling A, Malfatti S, Swan BK, Gies EA. Insights into the phylogeny and coding potential of microbial dark matter. Nature. 2013;499(7459):431-7.
35. Luo G, De Francisci D, Kougias PG, Laura T, Zhu X, Angelidaki I. New steady-state microbial community compositions and process performances in biogas reactors induced by temperature disturbances. Biotechnol Biofuels. 2015;8(1):3.
36. Abendroth C, Vilanova C, Günther T, Luschnig O, Porcar M. Eubacteria and archaea communities in seven mesophile anaerobic digester plants in Germany. Biotechnol Biofuels. 2015;8(1):1.
37. 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(20):12585-93.
38. Duda RM, da Silva Vantini J, Martins LS, de Mello Varani A, Lemos MVF, Ferro MIT, de Oliveira RA. A balanced microbiota efficiently produces methane in a novel high-rate horizontal anaerobic reactor for the treatment of swine wastewater. Bioresour Technol. 2015;197:152-60.
39. Goux X, Calusinska M, Lemaigre S, Marynowska M, Klocke M, Udelhoven T, Benizri E, Delfosse P. Microbial community dynamics in replicate anaerobic digesters exposed sequentially to increasing organic loading rate, acidosis, and process recovery. Biotechnol Biofuels. 2015;8(1):1.
40. Langer SG, Ahmed S, Einfalt D, Bengelsdorf FR, Kazda M. Functionally redundant but dissimilar microbial communities within biogas reactors treating maize silage in co-fermentation with sugar beet silage. Microb Biotechnol. 2015;8(5):828-36.
41. Krakat N, Schmidt S, Scherer P. Potential impact of process parameters upon the bacterial diversity in the mesophilic anaerobic digestion of beet silage. Bioresour Technol. 2011;102(10):5692-701.
42. Xafenias N, Mapelli V. Performance and bacterial enrichment of bioelectrochemical systems during methane and acetate production. Int J Hydrogen Energy. 2014;39(36):21864-75.
43. Sousa DZ, Alves JI, Alves MM, Smidt H, Stams AJ. Effect of sulfate on methanogenic communities that degrade unsaturated and saturated long-chain fatty acids (LCFA). Environ Microbiol. 2009;11(1):68-80.
44. Sousa DZ, Smidt H, Alves MM, Stams AJ. Ecophysiology of syntrophic communities that degrade saturated and unsaturated long-chain fatty acids. FEMS Microbiol Ecol. 2009;68(3):257-72.
45. Handley KM, Wrighton KC, Piceno YM, Andersen GL, DeSantis TZ, Williams KH, Wilkins MJ, N'Guessan AL, Peacock A, Bargar J. High-density PhyloChip profiling of stimulated aquifer microbial communities reveals a complex response to acetate amendment. FEMS Microbiol Ecol. 2012;81(1):188-204.
46. Pope PB, Vivekanand V, Eijsink VG, Horn SJ. Microbial community structure in a biogas digester utilizing the marine energy crop Saccharina latissima. 3 Biotech. 2013;3(5):407-14.
47. Solli L, Håvelsrud OE, Horn SJ, Rike AG. A metagenomic study of the microbial communities in four parallel biogas reactors. Biotechnol Biofuels. 2014;7(1):1-15.
48. Krakat N, Westphal A, Satke K, Schmidt S, Scherer P. The microcosm of a biogas fermenter: comparison of moderate hyperthermophilic (60 C) with thermophilic (55 C) conditions. Eng Life Sci. 2010;10(6):520-7.
49. Lebuhn M, Hanreich A, Klocke M, Schlüter A, Bauer C, Pérez CM. Towards molecular biomarkers for biogas production from lignocellulose-rich substrates. Anaerobe. 2014;29:10-21.
50. Weiss A, Jérôme V, Freitag R, Mayer HK. Diversity of the resident microbiota in a thermophilic municipal biogas plant. Appl Microbiol Biotechnol. 2008;81(1):163-73.
51. Maus I, Cibis KG, Wibberg D, Winkler A, Stolze Y, König H, Pühler A, Schlüter A. Complete genome sequence of the strain Defluviitoga tunisiensis L3, isolated from a thermophilic, production-scale biogas plant. J Biotechnol. 2015;203:17-8.
52. Wang W, Xie L, Luo G, Zhou Q, Angelidaki I. Performance and microbial community analysis of the anaerobic reactor with coke oven gas biomethanation and in situ biogas upgrading. Bioresour Technol. 2013;146:234-9.
53. Rademacher A, Zakrzewski M, Schlüter A, Schönberg M, Szczepanowski R, Goesmann A, Pühler A, Klocke M. Characterization of microbial biofilms in a thermophilic biogas system by high-throughput metagenome sequencing. FEMS Microbiol Ecol. 2012;79(3):785-99.
54. Zakrzewski M, Goesmann A, Jaenicke S, Jünemann S, Eikmeyer F, Szczepanowski R, Al-Soud WA, Sørensen S, Pühler A, Schlüter A. Profiling of the metabolically active community from a production-scale biogas plant by means of high-throughput metatranscriptome sequencing. J Biotechnol. 2012;158(4):248-58.
55. Hess M, Sczyrba A, Egan R, Kim T-W, Chokhawala H, Schroth G, Luo S, Clark DS, Chen F, Zhang T. Metagenomic discovery of biomass-degrading genes and genomes from cow rumen. Science. 2011;331(6016):463-7.
56. Koeck DE, Wibberg D, Maus I, Winkler A, Albersmeier A, Zverlov VV, Liebl W, Pühler A, Schwarz WH, Schlüter A. Complete genome sequence of the cellulolytic thermophile Ruminoclostridium cellulosi wild-type strain DG5 isolated from a thermophilic biogas plant. J Biotechnol. 2014;188:136-7.
57. Müller V. Energy conservation in acetogenic bacteria. Appl Environ Microbiol. 2003;69(11):6345-53.
58. Zinder SH, Koch M. Non-aceticlastic methanogenesis from acetate: acetate oxidation by a thermophilic syntrophic coculture. Arch Microbiol. 1984;138(3):263-72.
59. Barker HA. On the biochemistry of the methane fermentation. Archiv für Mikrobiologie. 1936;7(1-5):404-19.
60. Ahring B, Schmidt J, Winther-Nielsen M, Macario A, de Macario EC. Effect of medium composition and sludge removal on the production, composition, and architecture of thermophilic (55 degrees C) acetate-utilizing granules from an upflow anaerobic sludge blanket reactor. Appl Environ Microbiol. 1993;59(8):2538-45.
61. Petersen SP, Ahring BK. Acetate oxidation in a thermophilic anaerobic sewage-sludge digestor: the importance of non-aceticlastic methanogenesis from acetate. FEMS Microbiol Ecol. 1991;9(2):149-57.
62. Fotidis IA, Karakashev D, Kotsopoulos TA, Martzopoulos GG, Angelidaki I. Effect of ammonium and acetate on methanogenic pathway and methanogenic community composition. FEMS Microbiol Ecol. 2013;83(1):38-48.
63. 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(7):5138-41.
64. Schnürer A, Zellner G, Svensson BH. Mesophilic syntrophic acetate oxidation during methane formation in biogas reactors. FEMS Microbiol Ecol. 1999;29(3):249-61.
65. Chovatia M, Sikorski J, Schröder M, Lapidus A, Nolan M, Tice H, Del Rio TG, Copeland A, Cheng J-F, Lucas S. Complete genome sequence of Thermanaerovibrio acidaminovorans type strain (Su883T). Stand Genomic Sci. 2009;1(3):254.
66. Lang K, Schuldes J, Klingl A, Poehlein A, Daniel R, Brune A. New Mode of Energy Metabolism in the Seventh Order of Methanogens as Revealed by Comparative Genome Analysis of "Candidatus Methanoplasma termitum". Appl Environ Microbiol. 2015;81(4):1338-52.
67. Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics. 2014;30:2114.
68. Magoč T, Salzberg SL. FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics. 2011;27(21):2957-63.
69. Hyatt D, LoCascio PF, Hauser LJ, Uberbacher EC. Gene and translation initiation site prediction in metagenomic sequences. Bioinformatics. 2012;28(17):2223-30.
70. Xie C, Mao X, Huang J, Ding Y, Wu J, Dong S, Kong L, Gao G, Li C-Y, Wei L. KOBAS 2.0: a web server for annotation and identification of enriched pathways and diseases. Nucleic Acids Res. 2011;39(suppl 2):W316-22.
71. Overbeek R, Olson R, Pusch GD, Olsen GJ, Davis JJ, Disz T, Edwards RA, Gerdes S, Parrello B, Shukla M. The SEED and the Rapid Annotation of microbial genomes using Subsystems Technology (RAST). Nucleic Acids Res. 2014;42(D1):D206-14.
72. Moriya Y, Itoh M, Okuda S, Yoshizawa AC, Kanehisa M. KAAS: an automatic genome annotation and pathway reconstruction server. Nucleic Acids Res. 2007;35(suppl 2):W182-5.
73. Meyer F, Paarmann D, D'Souza M, Olson R, Glass EM, Kubal M, Paczian T, Rodriguez A, Stevens R, Wilke A. The metagenomics RAST server-a public resource for the automatic phylogenetic and functional analysis of metagenomes. BMC Bioinform. 2008;9(1):386.
74. Ondov BD, Bergman NH, Phillippy AM. Interactive metagenomic visualization in a Web browser. BMC Bioinform. 2011;12(1):385.
75. Segata N, Börnigen D, Morgan XC, Huttenhower C. PhyloPhlAn is a new method for improved phylogenetic and taxonomic placement of microbes. Nat Commun. 2013;4:2304.
76. Patil KR, Haider P, Pope PB, Turnbaugh PJ, Morrison M, Scheffer T, McHardy AC. Taxonomic metagenome sequence assignment with structured output models. Nat Methods. 2011;8(3):191-2.
77. Treu L, Toniolo C, Nadai C, Sardu A, Giacomini A, Corich V, Campanaro S. The impact of genomic variability on gene expression in environmental Saccharomyces cerevisiae strains. Environ Microbiol. 2014;16(5):1378-97.
78. Langmead B, Salzberg SL. Fast gapped-read alignment with Bowtie 2. Nat Methods. 2012;9(4):357-9.
79. Quinlan AR, Hall IM. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics. 2010;26(6):841-2.
80. Finn RD, Clements J, Eddy SR. HMMER web server: interactive sequence similarity searching. Nucleic Acids Res. 2011;39:W29.
81. Wang Q, Garrity GM, Tiedje JM, Cole JR. Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol. 2007;73(16):5261-7.
82. Saeed A, Sharov V, White J, Li J, Liang W, Bhagabati N, Braisted J, Klapa M, Currier T, Thiagarajan M. TM4: a free, open-source system for microarray data management and analysis. Biotechniques. 2003;34(2):374.