Phylogenetic and genomic analysis of Methanomassiliicoccales in wetlands and animal intestinal tracts reveals clade-specific habitat

FEMS Microbiology Ecology

Volumn 92, Issue 1, 2016, Pages

  Söllinger, Andrea ^a   Schwab, Clarissa ^b   Weinmaier, Thomas ^a   Loy, Alexander ^a   Tveit, Alexander T ^c   Schleper, Christa ^a   Urich, Tim ^a,d  

^a UNIVERSITY OF VIENNA   (Austria)

^b ETH ZURICH   (Switzerland)

^c UNIVERSITY OF TROMSØ   (Norway)

^d UNIVERSITY OF GREIFSWALD   (Germany)

Author keywords

Archaea; Enrichments; Metagenomics; Methanogens; Methylotrophic methanogenesis; Peat soil

Indexed keywords

ANATOMY; CARBON EMISSION; ENRICHMENT; ENZYME ACTIVITY; GENE EXPRESSION; GENETIC ANALYSIS; GENOME; GENOMICS; HABITAT SELECTION; METHANE; METHANOGENIC BACTERIUM; PEAT SOIL; PHYLOGENETICS; WETLAND;

ANIMALIA; BOVINAE; THERMOPLASMATA;

AIR POLLUTANT; METHANE; METHYL COENZYME M REDUCTASE; OXIDOREDUCTASE; RNA 16S; SOIL;

AIR POLLUTANT; ANIMAL; AUSTRIA; BIOSYNTHESIS; BOVINE; CHEMISTRY; CLASSIFICATION; DNA SEQUENCE; ECOSYSTEM; EURYARCHAEOTA; FECES; GENETICS; GENOMICS; GERMANY; HUMAN; INTESTINE FLORA; ITALY; METABOLISM; METAGENOME; MICROBIOLOGY; NUCLEOTIDE SEQUENCE; PHYLOGENY; RUMEN; SOIL; WETLAND;

AIR POLLUTANTS; ANIMALS; AUSTRIA; BASE SEQUENCE; CATTLE; ECOSYSTEM; EURYARCHAEOTA; FECES; GASTROINTESTINAL MICROBIOME; GENOMICS; GERMANY; HUMANS; ITALY; METAGENOME; METHANE; OXIDOREDUCTASES; PHYLOGENY; RNA, RIBOSOMAL, 16S; RUMEN; SEQUENCE ANALYSIS, DNA; SOIL; SOIL MICROBIOLOGY; WETLANDS;

EID: 84982134978     PISSN: 01686496     EISSN: 15746941     Source Type: Journal    
DOI: 10.1093/femsec/fiv149     Document Type: Article

References (70)

1. Altschul SF, Gish W, Miller W, et al. Basic local alignment search tool. J Mol Biol 1990;215:403-10.
2. Andersen R, Chapman SJ, Artz RRE. Microbial communities in natural and disturbed peatlands: a review. Soil Biol Biochem 2013;57:979-94.
3. Aziz RK, Bartels D, Best AA, et al. The RAST Server: rapid annotations using subsystems technology. BMC Genomics 2008;9:75.
4. Bauman DE, Lock AL. Concepts in lipid digestion and metabolism in dairy cows. Proc Tri-State Dairy Nutr Conf 2006;1-14.
5. Borrel G, Harris HM, Parisot N, et al. Genome sequence of "Candidatus Methanomassiliicoccus intestinalis" Issoire-Mx1, a third Thermoplasmatales-related methanogenic archaeon from human feces. Genome Announc 2013a;1:e00453-13.
6. Borrel G, Harris HMB, Toney W, et al. Genome sequence of "Candidatus Methanomethylophilus alvus" Mx1201, a methanogenic archaeon from the human gut belonging to a seventh order of methanogens. J Bacteriol 2012;194:6944-5.
7. Borrel G, O'Toole PW, Harris HM, et al. Phylogenomic data support a seventh order of methylotrophic methanogens and provide insights into the evolution of methanogenesis. Genome Biol Evol 2013b;5:1769-80.
8. Borrel G, Parisot N, Harris HM, et al. Comparative genomics highlights the unique biology of Methanomassiliicoccales, a Thermoplasmatales-related seventh order of methanogenic archaea that encodes pyrrolysine. BMC Genomics 2014;15:679.
9. Brady A, Salzberg SL. Phymm and PhymmBL: metagenomic phylogenetic classification with interpolated Markov models. Nat Methods 2009;6:673-6.
10. Brugere JF, Borrel G, Gaci N, et al. Archaebiotics: proposed therapeutic use of archaea to prevent trimethylaminuria and cardiovascular disease. Gut Microbes 2013;5:5-10.
11. Camacho C, Coulouris G, Avagyan V, et al. BLAST+: architecture and applications. BMC Bioinformatics 2009;10:421.
12. Deng Y, Cui X, Hernández M, et al. Microbial diversity in hummock and hollow soils of three wetlands on the Qinghai-Tibetan Plateau revealed by 16S rRNA pyrosequencing. PLoS One 2014;9:e103115.
13. Dos Santos PC, Fang Z, Mason SW, et al. Distribution of nitrogen fixation and nitrogenase-like sequences amongst microbial genomes. BMC Genomics 2012;13:162.
14. Dridi B, M-L Fardeau, Ollivier B, et al. Methanomassiliicoccus luminyensis gen. nov., sp. nov., a methanogenic archaeon isolated from human faeces. Int J Syst Evol Micr 2012;62:1902-7.
15. Evans PN, Hinds LA, Sly LI, et al. Community composition and density of Methanogens in the foregut of the Tammar Wallaby (Macropus eugenii). Appl Environ Microb 2009;75:2598-602.
16. Finn RD, Bateman A, Clements J, et al. Pfam: the protein families database. Nucleic Acids Res 2013;42:D222-30.
17. Galand PE, Saarnio S, Fritze H, et al. Depth related diversity of methanogen Archaea in Finnish oligotrophic fen. FEMS Microbiol Ecol 2002;42:441-9.
18. Godon J-J, Zumstein E, Dabert P, et al. Molecular microbial diversity of an anaerobic digestor as determined by smallsubunit rDNA sequence analysis. Appl Environ Microb 1997;63:2802-13.
19. Großkopf R, Stubner S, Liesack W. Novel euryarchaeotal lineages detected on rice roots and in the anoxic bulk soil of flooded rice microcosms. Appl Environ Microb 1998;64:4983-9.
20. Gu MJ, Alam M, Kim SH, et al. Analysis of methanogenic archaeal communities of rumen fluid and rumen particles from Korean black goats. Anim Sci J 2011;82:663-72.
21. Guindon S, Gascuel O. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 2003;52:696-704.
22. Hall TA. BioEdit: a user-friendly biological sequence alignment editor and analysis programfor Windows 95/98/NT. Nucl Acid S 1999;41:95-8.
23. He S, Malfatti SA, McFarland JW, et al. Patterns in wetland microbial community composition and functional gene repertoire associated with methane emissions. mBio 2015;6:e00066-15.
24. Hoj L, Olsen RA, Torsvik VL. Archaeal communities in High Arcticwetlands at Spitsbergen, Norway (78 degrees N) as characterized by 16S rRNA gene fingerprinting. FEMS Microbiol Ecol 2005;53:89-101.
25. Huang X, Tan H, Long R, et al. Comparison of methanogen diversity of yak (Bos grunniens) and cattle (Bos taurus) from the Qinghai-Tibetan plateau, China. BMC Microbiol 2012;12:237.
26. Huang Y, Niu B, Gao Y, et al. CD-HIT Suite: a web server for clustering and comparing biological sequences. Bioinformatics 2010;26:680-82.
27. Iino T, Tamaki H, Tamazawa S, et al. Candidatus Methanogranum caenicola: a novel Methanogen from the anaerobic digested sludge, and proposal of Methanomassiliicoccaceae fam. nov and Methanomassiliicoccales ord. nov., for a Methanogenic lineage of the class thermoplasmata. Microbes Environ 2013;28:244-50.
28. IPCC. Carbon and other biogeochemical cycles. In: Ciais P, Sabine C, Bala G et al. (eds). Climate Change 2013: The Physical Science Basis. Cambridge: CUP, 2013.
29. Katoh K, Toh H. Recent developments in the MAFFTmultiple sequence alignment program. Brief Bioinform 2008;9:286-98.
30. Krzycki JA. Function of genetically encoded pyrrolysine in corrinoid-dependent methylamine methyltransferases. Curr Opin Chem Biol 2004;8:484-91.
31. Lang K, Schuldes J, Klingl A, et al. New mode of energy metabolism in the seventh order of methanogens as revealed by comparative genome analysis of "Candidatus Methanoplasma termitum". Appl Environ Microb 2015;81:1338-2352.
32. Lanzén A, Jørgensen SL, Huson DH, et al. CREST - Classification Resources for Environmental Sequence Tags. PLoS One 2012;7:e49334.
33. Laslett D, Canback B. ARAGORN, a programto detect tRNA genes and tmRNA genes in nucleotide sequences. Nucleic Acids Res 2004;32:11-16.
34. Lowe TM, Eddy SR. tRNAscan-SE: a programfor improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res 1997;25:0955-64.
35. Ludwig W, Strunk O, Westram R, et al. ARB: a software environment for sequence data. Nucleic Acids Res 2004;32:1363-71.
36. Mihajlovski A, J Doré, Levenez F, et al. Molecular evaluation of the human gut methanogenic archaeal microbiota reveals an age-associated increase of the diversity. Environ Microbiol Rep 2010;2:272-80.
37. Minh BQ, Nguyen MAT, von Haeseler A. Ultrafast approximation for phylogenetic bootstrap. Mol Biol Evol 2013;30:1188-95.
38. Mitchell AD, Chappell A, Knox K. Metabolism of betaine in the ruminant. J Anim Sci 1979;49:764-74.
39. Mondav R, Woodcroft BJ, E-H Kim, et al. Discovery of a novel methanogen prevalent in thawing permafrost. Nat Commun 2014;5:3212.
40. Moparthi VK, Hägerhäll C. The evolution of respiratory chain complex I from a smaller last common ancestor consisting of 11 protein subunits. J Mol Evol 2011;72:484-97.
41. Nercessian D, Upton M, Lloyd D, et al. Phylogenetic analysis of peat bog methanogen populations. FEMS Microbiol Lett 1999;173:425-29.
42. Oren A, Garrity GM. List of new names and new combinations previously effectively, but not validly, published. Int J Syst Evol Microbiol 2013;63:3931-34.
43. Parks DH, Imelfort M, Skennerton CT, et al. CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes. Peer J Pre Prints 2015;25:1043-55.
44. Paul K, Nonoh JO, Mikulski L, et al. "Methanoplasmatales," Thermoplasmatales-related archaea in termite guts and other environments, are the seventh order of methanogens. Appl Environ Microbiol 2012;78:8245-53.
45. Petersen SO, Højberg O, Poulsen M, et al. Methanogenic community changes, and emissions of methane and other gases, during storage of acidified and untreated pig slurry. J Appl Microbiol 2014;117:160-72.
46. Poulsen M, Schwab C, Jensen BB, et al. Methylotrophic methanogenic Thermoplasmata implicated in reduced methane emissions from bovine rumen. Nat Commun 2013;4:1428.
47. Pruesse E, Peplies J, Glöckner FO. SINA: accurate highthroughput multiple sequence alignment of ribosomal RNA genes. Bioinformatics 2012;28:1823-9.
48. Quast C, Pruesse E, Yilmaz P, et al. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res 2013;41:D590-6.
49. Saier MH, Reddy VS, Tamang DG, et al. The transporter classification database. Nucleic Acids Res 2013;42:D251-D8.
50. Sayers EW, Barrett T, Benson DA, et al. Database resources of the national center for biotechnology information. Nucleic Acids Res 2011;39:D38-51.
51. Schmidt S, Pfluger K, Kogl S, et al. The salt-induced ABC transporter Ota of the methanogenic archaeon Methanosarcina mazei Go1 is a glycine betaine transporter. FEMS Microbiol Lett 2007;277:44-9.
52. St-Pierre B, Wright A-D. Diversity of gut methanogens in herbivorous animals. Animal 2013;7:49-56.
53. Steger D, Wentrup C, Braunegger C, et al. Microorganisms with novel dissimilatory (Bi)Sulfite Reductase genes are widespread and part of the core microbiota in low-sulfate peatlands. Appl Environ Microb 2011;77:1231-42.
54. Steinberg LM, Regan JM. Phylogenetic comparison of the methanogenic communities from an acidic, oligotrophic fen and an anaerobic digester treating municipal wastewater sludge. Appl Environ Microb 2008;74:6663-71.
55. Steinberg LM, Regan JM. mcrA-targeted real-time quantitative PCR method to examine methanogen communities. Appl Environ Microb 2009;75:4435-42.
56. Sundset MA, Edwards JE, Cheng YF, et al. Rumen microbial diversity in Svalbard reindeer, with particular emphasis on methanogenic archaea. FEMS Microbiol Ecol 2009;70:553-62.
57. Tajima K, Nagamine T, Matsui H, et al. Phylogenetic analysis of archaeal 16S rRNA libraries from the rumen suggests the existence of a novel group of archaea not associated with known methanogens. FEMS Microbiol Lett 2001;200:67-72.
58. Talavera G, Castresana J. Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Syst Biol 2007;56:564-77.
59. Tveit A, Schwacke R, Svenning MM, et al. Organic carbon transformations in high-Arctic peat soils: key functions and microorganisms. ISME Journal 2012;7:299-311.
60. Tveit A, Urich T, Svenning MM. Metatranscriptomic analysis of Arctic peat soil microbiota. Appl Environ Microb 2014;80:5761-72.
61. UniProt Consortium. UniProt: a hub for protein information. Nucleic Acids Res 2015;43:D204-D12.
62. Upton M, Hill B, Edwards C, et al. Combined molecular ecological and confocal laser scanning microscopic analysis of peat bog methanogen populations. FEMS Microbiol Lett 2000;193:275-81.
63. Urich T, Lanzén A, Qi J, et al. Simultaneous assessment of soilmicrobial community structure and function through analysis of the meta-transcriptome. PLoS One 2008;3:e2527.
64. Vanderhaeghen S, Lacroix C, Schwab C. Methanogen communities in stool of humans of different age and health status and co-occurrence with bacteria. FEMS Microbiol Lett 2015;362:fnv092.
65. Watkins AJ, Roussel EG, Parkes RJ, et al. Glycine betaine as a direct substrate for methanogens (Methanococcoides spp.). Appl Environ Microb 2014;80:289-93.
66. Wright A-DG, Williams AJ, Winder B, et al. Molecular diversity of rumen methanogens from sheep in Western Australia. Appl Environ Microb 2004;70:1263-70.
67. Yarza P, Yilmaz P, Pruesse E, et al. Uniting the classification of cultured and uncultured bacteria and archaea using 16S rRNA gene sequences. Nat Rev Microbiol 2014;12:635-45.
68. Yavitt JB, Yashiro E, Cadillo-Quiroz H, et al. Methanogen diversity and community composition in peatlands of the central to northern Appalachian Mountain region, North America. Biogeochemistry 2012;109:117-31.
69. Yrjälä K, Tuomivirta T, Juottonen H, et al. CH4 production and oxidation processes in a boreal fen ecosystem after long-term water table drawdown. Global Change Biol 2011;17:1311-20.
70. Zedler JB, Kercher S. Wetland resources: status, trends, ecosystem services, and restorability. Annu Rev Env Resour 2005;30:39-74