Advertisement

Antonie van Leeuwenhoek

, Volume 112, Issue 12, pp 1801–1814 | Cite as

Microbial communities involved in the methane cycle in the near-bottom water layer and sediments of the meromictic subarctic Lake Svetloe

  • Vitaly V. KadnikovEmail author
  • Alexander S. Savvichev
  • Andrey V. Mardanov
  • Alexey V. Beletsky
  • Alexander Y. Merkel
  • Nikolai V. Ravin
  • Nikolai V. Pimenov
Original Paper

Abstract

Although arctic and subarctic lakes are important sources of methane, the emission of which will increase due to the melting of permafrost, the processes related to the methane cycle in such environments are far from being comprehensively understood. Here we studied the microbial communities in the near-bottom water layer and sediments of the meromictic subarctic Lake Svetloe using high-throughput sequencing of the 16S rRNA and methyl coenzyme M reductase subunit A genes. Hydrogenotrophic methanogens of the order Methanomicrobiales were abundant, both in the water column and in sediments, while the share of acetoclastic Methanosaetaceae decreased with the depth of sediments. Members of the Methanomassiliicoccales order were absent in the water but abundant in the deep sediments. Archaea known to perform anaerobic oxidation of methane were not found. The bacterial component of the microbial community in the bottom water layer included oxygenic (Cyanobacteria) and anoxygenic (Chlorobi) phototrophs, aerobic Type I methanotrophs, methylotrophs, syntrophs, and various organotrophs. In deeper sediments the diversity of the microbial community decreased, and it became dominated by methanogenic archaea and the members of the Bathyarchaeota, Chloroflexi and Deltaproteobacteria. This study shows that the sediments of a subarctic meromictic lake contain a taxonomically and metabolically diverse community potentially capable of complete mineralization of organic matter.

Keywords

Freshwater lake Microbial diversity sediments Methanogenesis 

Notes

Acknowledgements

The authors thank N. Kokryatskaya and A. Chupakov (Federal Research Centre for Integrated Studies of the Arctic) for their help in the sampling of primary material. This work was performed using the scientific equipment of the Core Research Facility “Bioengineering” and was partly supported by the Russian Science Foundation (Grant Number 16-14-10201). The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

Supplementary material

10482_2019_1308_MOESM1_ESM.doc (38 kb)
Supplementary material 1 (DOC 37 kb)

References

  1. Angel R, Claus P, Conrad R (2012) Methanogenic archaea are globally ubiquitous in aerated soils and become active under wet anoxic conditions. ISME J 6:847–862PubMedGoogle Scholar
  2. Bastviken D, Cole J, Pace M, Tranvik L (2004) Methane emissions from lakes: dependence of lake characteristics, two regional assessments, and a global estimate. Glob Biogeochem Cycles 18:GB4009Google Scholar
  3. Blees J, Niemann H, Wenk CB, Zopfi J, Schubert CJ, Kirf MK, Veronesi ML, Hitz C, Lehmann MF (2014) Micro-aerobic bacterial methane oxidation in the chemocline and anoxic water column of deep south-Alpine Lake Lugano (Switzerland). Limnol Oceanogr 59:311–324Google Scholar
  4. Borrel G, Jézéquel D, Biderre-Petit C, Morel-Desrosiers N, Morel J-P, Peyret P, Fonty G, Lehours A-C (2011) Production and consumption of methane in freshwater lake ecosystems. Res Microbiol 162:832–847PubMedGoogle Scholar
  5. Borrel G, Lehours AC, Crouzet O, Jézéquel D, Rockne K, Kulczak A, Duffaud E, Joblin K, Fonty G (2012) Stratification of Archaea in the deep sediments of a freshwater meromictic lake: vertical shift from methanogenic to uncultured archaeal lineages. PLoS ONE 7:e43346PubMedPubMedCentralGoogle Scholar
  6. Borrel G, Adam PS, McKay LJ, Chen LX, Sierra-García IN, Sieber CMK, Letourneur Q, Ghozlane A, Andersen GL, Li WJ, Hallam SJ, Muyzer G, de Oliveira VM, Inskeep WP, Banfield JF, Gribaldo S (2019) Wide diversity of methane and short-chain alkane metabolisms in uncultured archaea. Nat Microbiol 4(4):603–613PubMedPubMedCentralGoogle Scholar
  7. Camacho A, Walter XA, Picazo A, Zopfi J (2017) Photoferrotrophy: remains of an ancient photosynthesis in modern environments. Front Microbiol 8:323PubMedPubMedCentralGoogle Scholar
  8. Canfield DE, Rosing MT, Bjerrum C (2006) Early anaerobic metabolisms. Philos Trans R Soc Lond B Biol Sci 361:1819–1836PubMedPubMedCentralGoogle Scholar
  9. Carnevali PBM, Herbold CW, Hand KP, Priscu JC, Murray AE (2018) Distinct microbial assemblage structure and archaeal diversity in sediments of arctic thermokarst lakes differing in methane sources. Front Microbiol 9:1192Google Scholar
  10. Castelle CJ, Wrighton KC, Thomas BC, Hug LA, Brown CT, Wilkins MJ, Frischkorn KR, Tringe SG, Singh A, Markillie LM, Taylor RC, Williams KH, Banfield JF (2015) Genomic expansion of domain archaea highlights roles for organisms from new phyla in anaerobic carbon cycling. Curr Biol 25(6):690–701PubMedGoogle Scholar
  11. Castelle CJ, Brown CT, Anantharaman K, Probst AJ, Huang RH, Banfield JF (2018) Biosynthetic capacity, metabolic variety and unusual biology in the CPR and DPANN radiations. Nat Rev Microbiol 16:629–645PubMedGoogle Scholar
  12. Caumette P (1984) Distribution and characterization of phototrophic bacteria isolated from the water of Bietri Bay (Ebrie Lagoon, Ivory Coast). Can J Microbiol 30:273–284Google Scholar
  13. Chan OC, Claus P, Casper P, Ulrich A, Lueders T, Conrad R (2005) Vertical distribution of structure and function of the methanogenic archaeal community in Lake Dagow sediment. Environ Microbiol 7:1139–1149PubMedGoogle Scholar
  14. Chistoserdova L (2015) Methylotrophs in natural habitats: current insights through metagenomics. Appl Microbiol Biotechnol 99:5763–5779PubMedGoogle Scholar
  15. Concheri G, Stevanato P, Zaccone C, Shotyk W, D’Orazio V, Miano T, Piffanelli P, Rizzi V, Ferrandi C, Squartini A (2017) Rapid peat accumulation favours the occurrence of both fen and bog microbial communities within a Mediterranean, free-floating peat island. Sci Rep 7:8511PubMedPubMedCentralGoogle Scholar
  16. Conrad R (2009) The global methane cycle: recent advances in understanding the microbial processes involved. Environ Microbiol Rep 1:285–292PubMedGoogle Scholar
  17. Corinne BP, Najwa T, Hélène G, Corentin H, Didier D (2018) New insights into the pelagic microorganisms involved in the methane cycle in the meromictic Lake Pavin through metagenomics. FEMS Microbiol Ecol 95(3):fiy183Google Scholar
  18. Crevecoeur S, Vincent WF, Comte J, Matveev A, Lovejoy C (2017) Diversity and potential activity of methanotrophs in high methane-emitting permafrost thaw ponds. PLoS ONE 12(11):e0188223PubMedPubMedCentralGoogle Scholar
  19. Crowe SA, Katsev S, Leslie K, Sturm A, Magen C, Nomosatryo S, Pack MA, Kessler JD, Reeburgh WS, Roberts JA, González L, Haffner GD, Mucci A, Sundby B, Fowle DA (2011) The methane cycle in ferruginous Lake Matano. Geobiology 9(1):61–78PubMedGoogle Scholar
  20. Davis JP, Youssef NH, Elshahed MS (2009) Assessment of the diversity, abundance, and ecological distribution of members of candidate division SR1 reveals a high level of phylogenetic diversity but limited morphotypic diversity. Appl Environ Microbiol 75(12):4139–4148PubMedPubMedCentralGoogle Scholar
  21. Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26(19):2460–2461Google Scholar
  22. Ershova AA, Vorobyeva TYa, Moreva OYu, Chupakov AV, Zabelina SA, Neverova NV (2015) Hydrochemical and microbiological research of a nitrogen cycle in freshwater meromictic Lake Svetloe (the Arkhangelsk region). Reg Environ Issues 5:44–50 (in Russian) Google Scholar
  23. Ettwig KF, Butler MK, Le Paslier D, Pelletier E, Mangenot S, Kuypers MMM, Schreiber F, Dutilh BE, Zedelius J, de Beer D, Gloerich J, Wessels HJCT, van Alen T, Luesken F, Wu MV, van de Pas-Schoonen KT, Op den Camp HJM, Janssen-Megens EM, Francoijs K-J, Stunnenberg H, Weissenbach J, Jetten MSM, Strous M (2010) Nitrite-driven anaerobic methane oxidation by oxygenic bacteria. Nature 464:543–548PubMedGoogle Scholar
  24. Evans PN, Parks DH, Chadwick GL, Robbins SJ, Orphan VJ, Golding SD, Tyson GW (2015) Methane metabolism in the archaeal phylum Bathyarchaeota revealed by genome-centric metagenomics. Science 350(6259):434–438PubMedGoogle Scholar
  25. Farag IF, Davis JP, Youssef NH, Elshahed MS (2014) Global patterns of abundance, diversity and community structure of the Aminicenantes (candidate phylum OP8). PLoS ONE 9(3):e92139PubMedPubMedCentralGoogle Scholar
  26. Graef C, Hestnes AG, Svenning MM, Frenzel P (2011) The active methanotrophic community in a wetland from the High Arctic. Environ Microbiol Rep 3:466–472PubMedGoogle Scholar
  27. Grossart H-P, Frindte K, Dziallas C, Eckert W, Tang KW (2011) Microbial methane production in oxygenated water column of an oligotrophic lake. Proc Natl Acad Sci USA 108:19657–19661PubMedGoogle Scholar
  28. Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, Gascuel O (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 59(3):307–321PubMedPubMedCentralGoogle Scholar
  29. Haggblom MM, Ahn YB, Fennell DE, Kerkhof LJ, Rhee SK (2003) Anaerobic dehalogenation of organohalide contaminants in the marine environment. Adv Appl Microbiol 53:61–84PubMedGoogle Scholar
  30. He R, Wooller MJ, Pohlman JW, Quensen J, Tiedje JM, Leigh MB (2012) Diversity of active aerobic methanotrophs along depth profiles of arctic and subarctic lake water column and sediments. ISME J 6(10):1937–1948PubMedPubMedCentralGoogle Scholar
  31. He Y, Li M, Perumal V, Feng X, Fang J, Xie J, Sievert SM, Wang F (2016) Genomic and enzymatic evidence for acetogenesis among multiple lineages of the archaeal phylum Bathyarchaeota widespread in marine sediments. Nat Microbiol 1(6):16035PubMedGoogle Scholar
  32. Hegler F, Posth NR, Jiang J, Kappler A (2008) Physiology of phototrophic iron (II)-oxidizing bacteria: implications for modern and ancient environments. FEMS Microbiol Ecol 66(2):250–260PubMedGoogle Scholar
  33. Heising S, Richter L, Ludwig W, Schink B (1999) Chlorobium ferrooxidans sp. nov., a phototrophic green sulfur bacterium that oxidizes ferrous iron in coculture with a ‘Geospirillum’ sp. strain. Arch Microbiol 172:116–124PubMedGoogle Scholar
  34. Imhoff JF (2014) Biology of green sulfur bacteria. eLS.  https://doi.org/10.1002/9780470015902.a0000458.pub2 CrossRefGoogle Scholar
  35. Kadnikov VV, Mardanov AV, Beletsky AV, Shubenkova OV, Pogodaeva TV, Zemskaya TI, Ravin NV, Skrybin KG (2012) Microbial community structure in methane hydrate-bearing sediments of freshwater Lake Baikal. FEMS Microbiol Ecol 79(2):348–358PubMedGoogle Scholar
  36. Kadnikov VV, Mardanov AV, Beletsky AV, Karnachuk OV, Ravin NV (2019) Genome of the candidate phylum Aminicenantes bacterium from a deep subsurface thermal aquifer revealed its fermentative saccharolytic lifestyle. Extremophiles 23(2):189–200PubMedGoogle Scholar
  37. Kallistova A, Kadnikov V, Rusanov I, Kokryatskaya N, Beletsky A, Mardanov A, Savvichev A, Ravin N, Pimenov N (2019) Microbial communities involved in aerobic and anaerobic methane cycling in a meromictic ferruginous subarctic lake. Aquat Microb Ecol 82(1):1–18Google Scholar
  38. Kantor RS, Wrighton KC, Handley KM, Sharon I, Hug LA, Castelle CJ, Thomas BC, Banfield JF (2013) Small genomes and sparse metabolisms of sediment-associated bacteria from four candidate phyla. MBio 4(5):e00708–e00713PubMedPubMedCentralGoogle Scholar
  39. Kaster AK, Mayer-Blackwell K, Pasarelli B, Spormann AM (2014) Single cell genomic study of Dehalococcoidetes species from deep-sea sediments of the Peruvian Margin. ISME J 8(9):1831PubMedPubMedCentralGoogle Scholar
  40. Kirschke S, Bousquet P, Ciais P, Saunois M, Canadell JG, Dlugokencky EJ, Bergamaschi P, Bergmann D, Blake DR, Bruhwiler L, Cameron-Smith P, Castaldi S, Chevallier F, Feng L, Fraser A, Heimann M, Hodson EL, Houweling S, Josse B, Fraser PJ, Krummel PB, Lamarque J-F, Langenfelds RL, Quéré CL, Naik V, O’Doherty S, Palmer PI, Pison I, Plummer D, Poulter B, Prinn RG, Rigby M, Ringeval B, Santini M, Schmidt M, Shindell DT, Simpson IJ, Spahni R, Steele LP, Strode SA, Sudo K, Szopa S, van der Werf GR, Voulgarakis A, van Weele M, Weiss RF, Williams JE, Zeng G (2013) Three decades of global methane sources and sinks. Nat Geosci 6:813–823Google Scholar
  41. Kits KD, Klotz MG, Stein LY (2015) Methane oxidation coupled to nitrate reduction under hypoxia by the Gammaproteobacterium Methylomonas denitrificans, sp. nov. type strain FJG1: denitrifying metabolism in M. denitrificans FJG1. Environ Microbiol 17:3219–3232PubMedGoogle Scholar
  42. Kittelmann S, Friedrich MW (2008) Novel uncultured Chloroflexi dechlorinate perchloroethene to trans-dichloroethene in tidal flat sediments. Environ Microbiol 10(6):1557–1570PubMedGoogle Scholar
  43. Knittel K, Boetius A (2009) Anaerobic oxidation of methane: progress with an unknown process. Annu Rev Microbiol 63:311–334PubMedGoogle Scholar
  44. Kolinko S, Jogler C, Katzmann E, Wanner G, Peplies J, Schüler D (2012) Single-cell analysis reveals a novel uncultivated magnetotactic bacterium within the candidate division OP3. Environ Microbiol 14(7):1709–1721PubMedGoogle Scholar
  45. Kuever J (2014) The family syntrophaceae. In: The prokaryotes. Springer, Berlin, pp 281–288Google Scholar
  46. Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874Google Scholar
  47. Lazar CS, Baker BJ, Seitz K, Hyde AS, Dick GJ, Hinrichs KU, Teske AP (2016) Genomic evidence for distinct carbon substrate preferences and ecological niches of Bathyarchaeota in estuarine sediments. Environ Microbiol 18(4):1200–1211PubMedGoogle Scholar
  48. Lazar CS, Baker BJ, Seitz KW, Teske AP (2017) Genomic reconstruction of multiple lineages of uncultured benthic archaea suggests distinct biogeochemical roles and ecological niches. ISME J 11(5):1118–1129PubMedPubMedCentralGoogle Scholar
  49. Lee YM, Hwang K, Lee JI, Kim M, Hwang CY, Noh HJ, Choi H, Lee HK, Chun J, Hong SG, Shin SC (2018) Genomic insight into the predominance of candidate phylum Atribacteria JS1 lineage in marine sediments. Front Microbiol 9:2909PubMedPubMedCentralGoogle Scholar
  50. Lidström ME, Somers L (1984) Seasonal study of methane oxidation in Lake Washington. Appl Environ Microbiol 47:1255–1260PubMedPubMedCentralGoogle Scholar
  51. Llirós M, Casamayor EO, Borrego CM (2008) High archaeal richness in the water column of a freshwater sulfurous karstic lake along an interannual study. FEMS Microbiol Ecol 66:331–342PubMedGoogle Scholar
  52. Luton PE, Wayne JM, Sharp RJ, Riley PW (2002) The mcrA gene as an alternative to 16S rRNA in the phylogenetic analysis of methanogen populations in landfillb. Microbiology 148(11):3521–3530PubMedGoogle Scholar
  53. Ma Y, Liu F, Kong Z, Yin J, Kou W, Wu L, Ge G (2016) The distribution pattern of sediment archaea community of the Poyang Lake, the largest freshwater lake in China. Archaea 2016:9278929PubMedPubMedCentralGoogle Scholar
  54. Martinez-Cruz K, Leewis MC, Herriott IC, Sepulveda-Jauregui A, Anthony KW, Thalasso F, Leigh MB (2017) Anaerobic oxidation of methane by aerobic methanotrophs in sub-Arctic lake sediments. Sci Total Environ 607–608:23–31PubMedGoogle Scholar
  55. Matheus Carnevali PB, Herbold CW, Hand KP, Priscu JC, Murray AE (2018) Distinct microbial assemblage structure and archaeal diversity in sediments of Arctic thermokarst lakes differing in methane sources. Front Microbiol 9:1192PubMedPubMedCentralGoogle Scholar
  56. Maymó-Gatell X, Chien YT, Gossett JM, Zinder SH (1997) Isolation of a bacterium that reductively dechlorinates tetrachloroethene to ethene. Science 276(5318):1568–1571PubMedGoogle Scholar
  57. McKay LJ, Hatzenpichler R, Inskeep WP, Fields MW (2017) Occurrence and expression of novel methyl-coenzyme M reductase gene (mcrA) variants in hot spring sediments. Sci Rep 7:7252PubMedPubMedCentralGoogle Scholar
  58. Nobu MK, Dodsworth JA, Murugapiran SK, Rinke C, Gies EA, Webster G, Schwientek P, Kille P, Parkes RJ, Sass H, Jørgensen BB, Weightman AJ, Liu W-L, Hallam SJ, Tsiamis G, Woyke T, Hedlund BP (2016) Phylogeny and physiology of candidate phylum ‘Atribacteria’ (OP9/JS1) inferred from cultivation-independent genomics. ISME J 10(2):273–286PubMedGoogle Scholar
  59. Ortiz-Alvarez R, Casamayor EO (2016) High occurrence of Pacearchaeota and Woesearchaeota (Archaea superphylum DPANN) in the surface waters of oligotrophic high-altitude lakes. Environ Microbiol Rep 8(2):210–217PubMedGoogle Scholar
  60. Oswald K, Milucka J, Brand A, Hach P, Littmann S, Wehrli B, Kuypers MMM, Schubert CJ (2016) Aerobic gammaproteobacterial methanotrophs mitigate methane emissions from oxic and anoxic lake waters. Limnol Oceanogr 61:S101–S118Google Scholar
  61. Pruesse E, Peplies J, Glöckner FO (2012) SINA: accurate high-throughput multiple sequence alignment of ribosomal RNA genes. Bioinformatics 28:1823–1829PubMedPubMedCentralGoogle Scholar
  62. Restrepo-Ortiz CX, Casamayor EO (2013) Environmental distribution of two widespread uncultured freshwater Euryarchaeota clades unveiled by specific primers and quantitative PCR. Environ Microbiol Rep 5(6):861–867PubMedGoogle Scholar
  63. Rinke C, Schwientek P, Sczyrba A, Ivanova NN, Anderson IJ, Cheng JF, Darling A, Malfatti S, Swan BK, Gies EA, Dodsworth JA, Hedlund BP, Tsiamis G, Sievert SM, Liu W-T, Eisen JA, Hallam SJ, Kyrpides NC, Stepanauskas R, Rubin EM, Hugenholtz P, Woyke T (2013) Insights into the phylogeny and coding potential of microbial dark matter. Nature 499(7459):431–437PubMedGoogle Scholar
  64. Rissanen AJ, Saarenheimo J, Tiirola M, Peura S, Aalto SL, Karvinen A, Nykänen H (2018) Gammaproteobacterial methanotrophs dominate methanotrophy in aerobic and anaerobic layers of boreal lake waters. Aquat Microb Ecol 81:257–276Google Scholar
  65. Rissanen AJ, Peura S, Mpamah PA, Taipale S, Tiirola M, Biasi C, Mäki A, Nykänen H (2019) Vertical stratification of bacteria and archaea in sediments of a small boreal humic lake. FEMS Microbiol Lett 366(5):fnz044PubMedPubMedCentralGoogle Scholar
  66. Robbins SJ, Evans PN, Parks DH, Golding SD, Tyson GW (2016) Genome-centric analysis of microbial populations enriched by hydraulic fracture fluid additives in a coal bed methane production well. Front Microbiol 7:731PubMedPubMedCentralGoogle Scholar
  67. Ruuskanen MO, St Pierre KA, St Louis VL, Aris-Brosou S, Poulain AJ (2018) Physicochemical drivers of microbial community structure in sediments of Lake Hazen, Nunavut, Canada. Front Microbiol 9:1138PubMedPubMedCentralGoogle Scholar
  68. Savvichev AS, Kokryatskaya NM, Zabelina SA, Rusanov II, Zakharova EE, Veslopolova EF, Lunina ON, Patutina EO, Bumazhkin BK, Gruzdev DS, Sigalevich PA, Pimenov NV, Kuznetsov BB, Gorlenko VM (2017) Microbial processes of the carbon and sulfur cycles in an ice-covered, iron-rich meromictic Lake Svetloe (Arkhangelsk region, Russia). Environ Microbiol 19(2):659–672PubMedGoogle Scholar
  69. Schink B, Zeikus JG (1982) Microbial methanol formation-a major end product of pectin metabolism. Curr Microbiol 4:387–389Google Scholar
  70. Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ, Sahl JW, Stres B, Thallinger GG, Van Horn DJ, Weber CF (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75(23):7537–7541PubMedPubMedCentralGoogle Scholar
  71. Schuchmann K, Müller V (2016) Energetics and application of heterotrophy in acetogenic bacteria. Appl Environ Microbiol 82(14):4056–4069PubMedPubMedCentralGoogle Scholar
  72. Schulz M, Faber E, Hollerbach A, Schröder HG, Güde H (2001) The methane cycle in the epilimnion of Lake Constance. Fundam Appl Limnol 151:157–176Google Scholar
  73. Sewell HL, Kaster AK, Spormann AM (2017) Homoacetogenesis in deep-sea Chloroflexi, as inferred by single-cell genomics, provides a link to reductive dehalogenation in terrestrial Dehalococcoidetes. MBio 8(6):e02022-17PubMedPubMedCentralGoogle Scholar
  74. Steinberg LM, Regan JM (2008) Phylogenetic comparison of the methanogenic communities from an acidic, oligotrophic fen and an anaerobic digester treating municipal wastewater sludge. Appl Environ Microbiol 74:6663–6671PubMedPubMedCentralGoogle Scholar
  75. Sundh I, Bastviken D, Tranvik LJ (2005) Abundance, activity, and community structure of pelagic methane oxidizing bacteria in temperate lakes. Appl Environ Microbiol 71:6746–6752PubMedPubMedCentralGoogle Scholar
  76. Tang KW, McGinnis DF, Ionescu D, Grossart HP (2016) Methane production in oxic lake waters potentially increases aquatic methane flux to air. Environ Sci Technol Lett 3:227–233Google Scholar
  77. Taş N, Van Eekert MH, De Vos WM, Smidt H (2010) The little bacteria that can—diversity, genomics and ecophysiology of ‘Dehalococcoides’ spp. in contaminated environments. Microb Biotechnol 3(4):389–402PubMedPubMedCentralGoogle Scholar
  78. Vanwonterghem I, Evans PN, Parks DH, Jensen PD, Woodcroft BJ, Hugenholtz P, Tyson GW (2016) Methylotrophic methanogenesis discovered in the archaeal phylum Verstraetearchaeota. Nat Microbiol 1(12):16170PubMedGoogle Scholar
  79. Vetriani C, Jannasch HW, MacGregor BJ, Stahl DA, Reysenbach A-L (1999) Population structure and phylogenetic characterization of marine bentic Archaea in deep-sea sediments. Appl Environ Microbiol 65:4375–4384PubMedPubMedCentralGoogle Scholar
  80. Vuillemin A, Horn F, Friese A, Winkel M, Alawi M, Wagner D, Henny C, Orsi WD, Crowe SA, Kallmeyer J (2018) Metabolic potential of microbial communities from ferruginous sediments. Environ Microbiol 20(12):4297–4313PubMedGoogle Scholar
  81. Walker CB, de la Torre JR, Klotz MG, Urakawa H, Pinel N, Arp DJ, Brochier-Armanet C, Chain PSJ, Chan PP, Gollabgir A, Hemp J, Hьgler M, Karr EA, Kцnneke M, Shin M, Lawton TJ, Lowe T, Martens-Habbena W, Sayavedra-Soto LA, Lang D, Sievert SM, Rosenzweig AC, Manning G, Stahl DA (2010) Nitrosopumilus maritimus genome reveals unique mechanisms for nitrification and autotrophy in globally distributed marine crenarchaea. Proc Natl Acad Sci USA 107(19):8818–8823PubMedGoogle Scholar
  82. Walter KM, Smith LC, Chapin FS (2007) Methane bubbling from northern lakes: present and future contributions to the global methane budget. Philos Trans A Math Phys Eng Sci 365:1657–1676PubMedGoogle Scholar
  83. Walter XA, Picazo A, Miracle MR, Vicente E, Camacho A, Aragno M, Zopfi J (2014) Phototrophic Fe(II)-oxidation in the chemocline of a ferruginous meromictic lake. Front Microbiol 5:713PubMedPubMedCentralGoogle Scholar
  84. Wik M, Varner RK, Walter Anthony K, MacIntyre S, Bastviken D (2016) Climate-sensitive northern lakes and ponds are critical components of methane release. Nat Geosci 9:99–105Google Scholar
  85. Wilson K (2003) Preparation of genomic DNA from bacteria. In: Ausubel FM, Brent R, Kingston RE, Moore DD, Seidman JG, Smith JA, Struhl K (eds) Current protocols in molecular biology. Wiley, New York, pp 2.4.1–2.4.5Google Scholar
  86. Wurzbacher C, Fuchs A, Attermeyer K, Frindte K, Grossart HP, Hupfer M, Casper P, Monaghan MT (2017) Shifts among Eukaryota, Bacteria, and Archaea define the vertical organization of a lake sediment. Microbiome 5(1):41PubMedPubMedCentralGoogle Scholar
  87. Yamada T, Sekiguchi Y, Hanada S, Imachi H, Ohashi A, Harada H, Kamagata Y (2006) Anaerolinea thermolimosa sp. nov., Levilinea saccharolytica gen. nov., sp. nov. and Leptolinea tardivitalis gen. nov., sp. nov., novel filamentous anaerobes, and description of the new classes Anaerolineae classis nov. and Caldilineae classis nov. in the bacterial phylum Chloroflexi. Int J Syst Evol Microbiol 56(6):1331–1340PubMedGoogle Scholar
  88. Youssef NH, Rinke C, Stepanauskas R, Farag I, Woyke T, Elshahed MS (2015) Insights into the metabolism, lifestyle and putative evolutionary history of the novel archaeal phylum ‘Diapherotrites’. ISME J 9(2):447–460PubMedGoogle Scholar
  89. Yu Y, Lee C, Kim J, Hwang S (2005) Group-specific primer and probe sets to detect methanogenic communities using quantitative real-time polymerase chain reaction. Biotechnol Bioeng 89(6):670–679PubMedGoogle Scholar
  90. Yu T, Wu W, Liang W, Lever MA, Hinrichs KU, Wang F (2018) Growth of sedimentary Bathyarchaeota on lignin as an energy source. Proc Natl Acad Sci USA 115(23):6022–6027PubMedGoogle Scholar
  91. Zeleke J, Lu SL, Wang JG, Huang JX, Li B, Ogram AV, Quan ZX (2013) Methyl coenzyme M reductase A (mcrA) gene-based investigation of methanogens in the mudflat sediments of Yangtze River Estuary, China. Microb Ecol 66:257–267PubMedGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Vitaly V. Kadnikov
    • 1
    Email author
  • Alexander S. Savvichev
    • 2
  • Andrey V. Mardanov
    • 1
  • Alexey V. Beletsky
    • 1
  • Alexander Y. Merkel
    • 2
  • Nikolai V. Ravin
    • 1
  • Nikolai V. Pimenov
    • 2
  1. 1.Institute of BioengineeringResearch Center of Biotechnology of the Russian Academy of SciencesMoscowRussia
  2. 2.Winogradsky Institute of MicrobiologyResearch Center of Biotechnology of the Russian Academy of SciencesMoscowRussia

Personalised recommendations