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Seasonal Dynamics of Abundance, Structure, and Diversity of Methanogens and Methanotrophs in Lake Sediments

Abstract

Understanding temporal and spatial microbial community abundance and diversity variations is necessary to assess the functional roles played by microbial actors in the environment. In this study, we investigated spatial variability and temporal dynamics of two functional microbial sediment communities, methanogenic Archaea and methanotrophic bacteria, in Lake Bourget, France. Microbial communities were studied from 3 sites sampled 4 times over a year, with one core sampled at each site and date, and 5 sediment layers per core were considered. Microbial abundance in the sediment were determined using flow cytometry. Methanogens and methanotrophs community structures, diversity, and abundance were assessed using T-RFLP, sequencing, and real-time PCR targeting mcrA and pmoA genes, respectively. Changes both in structure and abundance were detected mainly at the water-sediment interface in relation to the lake seasonal oxygenation dynamics. Methanogen diversity was dominated by Methanomicrobiales (mainly Methanoregula) members, followed by Methanosarcinales and Methanobacteriales. For methanotrophs, diversity was dominated by Methylobacter in the deeper area and by Methylococcus in the shallow area. Organic matter appeared to be the main environmental parameter controlling methanogens, while oxygen availability influenced both the structure and abundance of the methanotrophic community.

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Data Availability

Sequences were deposited in GenBank under accession numbers KR011354 to KR011484 for partial mcrA gene sequences and from KR011489 to KR011714 for partial pmoA gene sequences.

References

  1. 1.

    Schmid M, De Batist M, Granin NG, Kapitanov VA, McGinnis DF, Mizandrontsev IB, Obzhirov AI, Wüest A (2007) Sources and sinks of methane in Lake Baikal: a synthesis of measurements and modeling. Limnol Oceanogr 52:1824–1837

    Article  CAS  Google Scholar 

  2. 2.

    Bastviken D, Tranvik LJ, Downing JA, Crill PM, Enrich-Prast A (2011) Freshwater methane emissions offset the continental carbon sink. Science 331:50

    PubMed  Article  CAS  Google Scholar 

  3. 3.

    Bussmann I, Damm E, Schlüter M, Wessels M (2013) Fate of methane bubbles released by pockmarks in Lake Constance. Biogeochemistry 112:613–623

    Article  CAS  Google Scholar 

  4. 4.

    Pester M, Friedrich MW, Schink B, Brune A (2004) pmoA-based analysis of methanotrophs in a littoral lake sediment reveals a diverse and stable community in a dynamic environment. Appl Environ Microbiol 70:3138–3142

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  5. 5.

    Earl J, Pickup RW, Ritchie DA, Edwards C (2005) Development of temporal temperature gradient electrophoresis for characterising methanogen diversity. Microb Ecol 50:327–336

    PubMed  Article  CAS  PubMed Central  Google Scholar 

  6. 6.

    Schwarz JIK, Eckert W, Conrad R (2008) Response of the methanogenic microbial community of a profundal lake sediment (lLake Kinneret, Israel) to algal deposition. Limnol Oceanogr 53:113–121

    Article  CAS  Google Scholar 

  7. 7.

    Brankovits D, Pohlman JW, Niemann H, Leigh MB, Leewis MC, Becker KW, Iliffe TM, Alvarez F, Lehmann MF, Phillips B (2017) Methane and dissolved organic carbon fueled microbial loop supports a tropical subterranean estuary ecosystem. Nat Commun 8:1835

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  8. 8.

    Davidson TA, Audet J, Jeppesen E, Landkildehus F, Lauridsen TL, Søndergaard M, Syväranta J (2018) Synergy between nutrients and warming enhances methane ebullition from experimental lakes. Nat Clim Chang 8:156–160

    Article  CAS  Google Scholar 

  9. 9.

    DelSontro T, delGiorgio PA, Prairie Y (2018) No longer a paradox: the interaction between physical transport and biological processes explains the spatial distribution of surface water methane within and across lakes. Ecosystems 21:1073–1087

    Article  CAS  Google Scholar 

  10. 10.

    Conrad R (2009) The global methane cycle: recent advances in understanding the microbial processes involved. Environ Microbiol Rep 1:285–292

    PubMed  Article  CAS  Google Scholar 

  11. 11.

    Siljanen HMP, Saari A, Bodrossy L, Martikainen PJ (2012) Seasonal variation in the function and diversity of methanotrophs in the littoral wetland of a boreal eutrophic lake. FEMS Microbiol Ecol 80:548–555

    PubMed  Article  CAS  Google Scholar 

  12. 12.

    Fuchs A, Lyautey E, Montuelle B, Casper P (2016) Effects of increasing temperatures on methane concentrations and methanogenesis during experimental incubation of sediments from oligotrophic and mesotrophic lakes. J Geophys Res Biogeosci 121:1394–1406

    Article  CAS  Google Scholar 

  13. 13.

    Froelich PN, Klinkhammer GP, Bender ML, Luedtke NA, Heath GR, Cullen D, Dauphin P, Hammond D, Hartman B, Maynard V (1979) Early oxidation of organic matter in pelagic sediments of the eastern equatorial Atlantic: suboxic diagenesis. Geochim Cosmochim Acta 43:1075–1090

    Article  CAS  Google Scholar 

  14. 14.

    Chaudhary PP, Brablcová L, Buriánková I, Rulík M (2013) Molecular diversity and tools for deciphering the methanogen community structure and diversity in freshwater sediments. Appl Microbiol Biotechnol 97:7553–7562

    PubMed  Article  CAS  Google Scholar 

  15. 15.

    Chowdhury TR, Dick RP (2013) Ecology of aerobic methanotrophs in controlling methane fluxes from wetlands. Appl Soil Ecol 65:8–22

    Article  Google Scholar 

  16. 16.

    Thomas C, Frossard V, Perga ME, Tofield-Pasche N, Hofmann H, Dubois N, Belkina N, Zobkova M, Robert S, Lyautey E (2019) Lateral variations and vertical structure of the microbial methane cycle in the sediment of Lake Onego (Russia). Inland Waters 9:205–226

    Article  CAS  Google Scholar 

  17. 17.

    Karlsson J, Giesler R, Persson J, Lundin E (2013) High emission of carbon dioxide and methane during ice thaw in high latitude lakes. Geophys Res Lett 40:1–5

    Article  Google Scholar 

  18. 18.

    Fernandez JE, Peeters F, Hofmann H (2014) Importance of the autumn overturn and anoxic conditions in the hypolimnion for the annual methane emissions from a temperate lake. Environ Sci Technol 48:7297–7304

    Article  CAS  Google Scholar 

  19. 19.

    Conrad R (2007) Microbial ecology of methanogens and methanotrophs. Adv Agron 96:1–63

    Article  CAS  Google Scholar 

  20. 20.

    Evans PN, Boyd JA, Leu AO, Woodcroft BJ, Parks DH, Hugenholtz P, Tyson GW (2019) An evolving view of methane metabolism in the Archaea. Nat Rev Microbiol 17:219–232

    PubMed  Article  CAS  Google Scholar 

  21. 21.

    Semrau JD, DiSpirito AA, Yoon S (2010) Methanotrophs and copper. FEMS Microbiol Rev 34:496–531

    PubMed  Article  CAS  Google Scholar 

  22. 22.

    Bosse U, Frenzel P, Conrad R (1993) Inhibition of methane oxidation by ammonium in the surface layer of a littoral sediment. FEMS Microbiol Ecol 13:123–134

    Article  CAS  Google Scholar 

  23. 23.

    Bastviken D, Jörgen Ejlertsson J, Tranvik L (2002) Measurement of methane oxidation in lakes: a comparison of methods. Environ Sci Technol 36:3354–3361

    PubMed  Article  CAS  Google Scholar 

  24. 24.

    Duc NT, Crill P, Bastviken D (2010) Implications of temperature and sediment characteristics on methane formation and oxidation in lake sediments. Biogeochemistry 100:185–196

    Article  CAS  Google Scholar 

  25. 25.

    Murase J, Frenzel P (2008) Selective grazing of methanotrophs by protozoa in a rice field soil. FEMS Microbiol Ecol 65:408–414

    PubMed  Article  CAS  Google Scholar 

  26. 26.

    Lehours AC, Bardot C, Thenot A, Debroas D, Fonty G (2005) Anaerobic microbial communities in Lake Pavin, a unique meromictic lake in France. Appl Environ Microbiol 71:7389–7400

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  27. 27.

    Bastviken D, Cole JJ, Pace ML, Van de Bogert MC (2008) Fates of methane from different lake habitats: connecting whole-lake budgets and CH4 emissions. J Geophys Res 113:G02024

    Google Scholar 

  28. 28.

    Schulz S, Conrad R (1995) Effect of algal deposition on acetate and methane concentration in the profundal sediment of a deep lake (Lake Constance). FEMS Microbiol Ecol 16:251–259

    Article  CAS  Google Scholar 

  29. 29.

    Billard E, Domaizon I, Tissot N, Arnaud F, Lyautey E (2015) Multi-scale phylogenetic heterogeneity of archaea, bacteria, methanogens and methanotrophs in lake sediments. Hydrobiologia 751:159–173

    Article  Google Scholar 

  30. 30.

    Jacquet S, Barbet D, Cachera S, Caudron A, Colon M, Girel C, Guillard J, Hébert A, Kerrien F, Laine L, Lazzarotto J, Moille JP, Paolini G, Perga M, Perney P, Rimet F (2012) Suivi environnemental des eaux du lac du Bourget pour l’année 2011. Rapport INRA-CISALB-CALB

  31. 31.

    Jacquet S, Domaizon I, Anneville O (2014) The need for ecological monitoring of freshwaters in a changing world: a case studies of Lakes Annecy, Bourget and Geneva. Environ Monit Assess 186:3455–3476

    PubMed  Article  Google Scholar 

  32. 32.

    Brandl H, Hanselmann KW, Bachoffen R (1993) In situ stimulation of bacterial sulfate reduction in sulfate-limited freshwater sediments. FEMS Microbiol Lett 74:21–32

    Article  Google Scholar 

  33. 33.

    Duhamel S, Jacquet S (2006) Flow cytometry analysis of bacteria- and virus- like particles in lake sediments. J Microbiol Methods 64:316–332

    PubMed  Article  CAS  Google Scholar 

  34. 34.

    Lueders T, Friedrich MW (2003) Evaluation of PCR amplification bias by terminal restriction fragment length polymorphism analysis of small-subunit rRNA and mcrA genes by using defined template mixtures of methanogenic pure cultures and soil DNA extracts. Appl Environ Microbiol 69:320–326

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  35. 35.

    Costello AM, Lidstrom ME (1999) Molecular characterization of functional and phylogenetic genes from natural populations of methanotrophs in lake sediments. Appl Environ Microbiol 65:5066–5074

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  36. 36.

    Hales BA, Edwards C, Ritchie DA, Hall G, Pickup RW, Saunders JR (1996) Isolation and identification of methanogen-specific DNA from blanket bog peat by PCR amplification and sequence analysis. Appl Environ Microbiol 62:668–675

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  37. 37.

    Bourne DG, McDonald IR, Murrell JC (2001) Comparison of pmoA PCR primer sets as tools for investigating methanotroph diversity in three Danish soils. Appl Environ Microbiol 67:3802–3809

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  38. 38.

    Freitag TE, Prosser JI (2009) Correlation of methane production and functional gene transcriptional activity in a peat soil. Appl Environ Microbiol 75:6679–6687

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  39. 39.

    Stolyar S, Costello AM, Peeples TL, Lidstrom ME (1999) Role of multiple gene copies in particulate methane monooxygenase activity in the methane-oxidizing bacterium Methylococcus capsulatus Bath. Microbiology 145:1235–1244

    PubMed  Article  CAS  Google Scholar 

  40. 40.

    Clarke KR, Warwick RM (2001) Change in marine communities: an approach to statistical analysis and interpretation2nd edn. PRIMER-E, Plymouth

    Google Scholar 

  41. 41.

    Fish JA, Chai B, Wang Q, Sun Y, Brown CT, Tiedje JM, Cole JR (2013) FunGene: the functional gene pipeline and repository. Front Microbiol 4:291

    PubMed  PubMed Central  Article  Google Scholar 

  42. 42.

    Daebeler A, Gansen M, Frenzel P (2013) Methyl fluoride affects methanogenesis rather than community composition of methanogenic Archaea in a rice field soil. PLoS One 8:e53656

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  43. 43.

    Degelmann DM, Borken W, Drake HL, Kolb S (2010) Different atmospheric methane-oxidizing communities in European beech and Norway spruce soils. Appl Environ Microbiol 76:3228–3235

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  44. 44.

    Schloss PD, Handelsman J (2005) Introducing DOTUR, a computer program for defining operational taxonomic units and estimating species richness. Appl Environ Microbiol 71:1501–1506

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  45. 45.

    Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  46. 46.

    Junier P, Junier T, Witzel KP (2008) TRiFLe, a program for in silico terminal restriction fragment length polymorphism analysis with user-defined sequences sets. Appl Environ Microbiol 74:6452–6456

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  47. 47.

    Deutzmann JS, Stief P, Brandes J, Schink B (2014) Anaerobic methane oxidation in a deep lake. Proc Natl Acad Sci U S A 111:18273–18278

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  48. 48.

    Rissanen AJ, Karvinen A, Nykänen H, Peura S, Tiirola M, Mäki A, Kankaala P (2017) Effects of alternative electron acceptors on the activity and community structure of methane-producing and consuming microbes in the sediments of two shallow boreal lakes. FEMS Microbiol Ecol 93:fix078

    Article  CAS  Google Scholar 

  49. 49.

    Weber HS, Habicht KS, Thamdrup B (2017) Anaerobic methanotrophic Archaea of the ANME-2d cluster are active in a low-sulfate, iron-rich freshwater sediment. Front Microbiol 8:619

    PubMed  PubMed Central  Google Scholar 

  50. 50.

    Martinez-Cruz K, Sepulveda-Jauregui A, Casper P, Anthony KW, Smemo KA, Thalasso F (2018) Ubiquitous and significant anaerobic oxidation of methane in freshwater lake sediments. Water Res 144:332–340

    PubMed  Article  CAS  Google Scholar 

  51. 51.

    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:e43346

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  52. 52.

    Zhang S, Guo C, Wang C, Gu J, Wang P, Hui Y, Han B (2014) Detection of methane biogenesis in a shallow urban lake in summer. J Soils Sediments 14:1004–1012

    Article  CAS  Google Scholar 

  53. 53.

    Borrel G, Jézéquel D, Biderre-Petit C, Morel-Desrosiers N, Morel JP, Peyret P, Fonty G, Lehours AC (2011) Production and consumption of methane in freshwater lake ecosystems. Res Microbiol 162:832–847

    PubMed  Article  CAS  Google Scholar 

  54. 54.

    Schwarz JIK, Eckert W, Conrad R (2007) Community structure of Archaea and Bacteria in a profundal lake sediment Lake Kinneret (Israel). Syst Appl Microbiol 30:239–254

    PubMed  Article  CAS  Google Scholar 

  55. 55.

    Berberich ME, Beaulieu JJ, Hamilton TL, Waldo S, Buffam I (2019) Spatial variability of sediment methane production and methanogen communities within a eutrophic reservoir: importance of organic matter source and quantity. Limnol Oceanogr. https://doi.org/10.1002/lno.11392

  56. 56.

    Yang Y, Chen J, Tong T, Xie S, Liu Y (2020) Influences of eutrophication on methanogenesis pathways and methanogenic microbial community structures in freshwater lakes. Environ Pollut 260:114106. https://doi.org/10.1016/j.envpol.2020.114106

    Article  PubMed  CAS  Google Scholar 

  57. 57.

    Angel R, Matthies D, Conrad R (2011) Activation of methanogenesis in arid biological soil crusts despite the presence of oxygen. PLoS One 6:e20453

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  58. 58.

    Grossart HP, Frindte K, Dziallas C, Eckert W, Tang KW (2011) Microbial methane production in oxygenated water column of an oligotrophic lake. Proc Natl Acad Sci 108:19657–19661

    PubMed  PubMed Central  Article  Google Scholar 

  59. 59.

    Bogard MJ, del Giorgio PA, Boutet L, Garcia-Chaves MC, Prairie YT, Merante A, Derry AM (2014) Oxic water column methanogenesis as a major component of aquatic CH4 fluxes. Nat Commun 5:5350

    PubMed  Article  CAS  Google Scholar 

  60. 60.

    Tang KW, McGinnis DF, Frindte K, Brüchert V, Grossart HP (2014) Paradox reconsidered: methane oversaturation in well-oxygenated lake waters. Limnol Oceanogr 59:275–284

    Article  Google Scholar 

  61. 61.

    Bertolet BL, West WE, Armitage DW, Jones SE (2019) Organic matter supply and bacterial community composition predict methanogenesis rates in temperate lake sediments. Limnol Oceanogr Lett 4:164–172

    Article  CAS  Google Scholar 

  62. 62.

    Praetzel LSE, Plenter N, Schilling S, Schmiedeskamp M, Broll G, Knorr K-H (2019) Organic matter and sediment properties determine in-lake variability of sediment CO2 and CH4 production and emissions of a small and shallow lake. Biogeosci Discuss. https://doi.org/10.5194/bg-2019-284 in review, 2019

  63. 63.

    Rahalkar M, Deutzmann J, Schink B, Bussmann I (2009) Abundance and activity of methanotrophic bacteria in littoral and profundal sediments of Lake Constance (Germany). Appl Environ Microbiol 75:119–126

    PubMed  Article  CAS  Google Scholar 

  64. 64.

    Deutzmann JS, Wörner S, Schink B (2011) Activity and diversity of methanotrophic Bacteria at methane seeps in Eastern Lake Constance sediments. Appl Environ Microbiol 77:2573–2581

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  65. 65.

    Roslev P, King GM (1996) Regulation of methane oxidation in a freshwater wetland by water table changes and anoxia. FEMS Microbiol Ecol 19:105–115

    Article  CAS  Google Scholar 

  66. 66.

    Rahalkar M, Schink B (2007) Comparison of aerobic methanotrophic communities in littoral and profundal sediments of Lake Constance by a molecular approach. Appl Environ Microbiol 73:4389–4394

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  67. 67.

    Shrestha M, Abraham WR, Shrestha PM, Noll M, Conrad R (2008) Activity and composition of methanotrophic bacterial communities in planted rice soil studied by flux measurements, analyses of pmoA gene and stable isotope probing of phospholipid fatty acids. Environ Microbiol 10:400–412

    PubMed  Article  CAS  Google Scholar 

  68. 68.

    Ma K, Lu Y (2011) Regulation of microbial methane production and oxidation by intermittent drainage in rice field soil. FEMS Microbiol Ecol 75:446–456

    PubMed  Article  CAS  Google Scholar 

  69. 69.

    Ma K, Conrad R, Lu Y (2013) Dry/wet cycles change the activity and population dynamics of methanotrophs in rice field soil. Appl Environ Microbiol 79:4932–4939

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  70. 70.

    Sobek S, Durisch-Kaiser E, Zurbrügg R, Wongfun N, Wessels M, Pasche N, Wehrli B (2009) Organic carbon burial efficiency in lake sediments controlled by oxygen exposure time and sediment source. Limnol Oceanogr 54:2243–2254

    Article  Google Scholar 

  71. 71.

    Krause S, Lüke C, Frenzel P (2010) Succession of methanotrophs in oxygen–methane counter-gradients of flooded rice paddies. ISME J 4:1603–1607

    PubMed  Article  Google Scholar 

  72. 72.

    Biderre-Petit C, Jézéquel D, Dugat-Bony E, Lopes F, Kuever J, Borrel G, Viollier E, Fonty G, Peyret P (2011) Identification of microbial communities involved in the methane cycle of a freshwater meromictic lake. FEMS Microbiol Ecol 77:533–545

    PubMed  Article  CAS  Google Scholar 

  73. 73.

    Lew S, Glińska-Lewczukb K (2018) Environmental controls on the abundance of methanotrophs and methanogens in peat bog lakes. Sci Total Environ 645:1201–1211

    PubMed  Article  CAS  Google Scholar 

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Acknowledgments

We thank Emmanuel Mallet and Jean-Philippe Jenny for field assistance, as well as Annie Millery and Cécile Pignol for sediment characterization analyses. We utilized the database from the observatory on perialpine lakes (reference article: https://doi.org/10.4081/jlimnol.2020.1944) as the source of complementary data on Lake Bourget; we thank OLA (Observatory on LAkes), © OLA-IS, AnaEE-France, INRAE Thonon-les-Bains, CISALB, and IS OLA Data (https://doi.org/10.15454/VBWYWG).

Funding

Elodie Billard was supported by a Ph.D. fellowship from the French Ministère de l’Enseignement Supérieur et de la Recherche.

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E. Lyautey, E. Billard, and I. Domaizon conceived and designed the study; E. Billard, N. Tissot and S. Jacquet performed the experiments and analyzed the samples; E. Billard and N. Tissot conducted the bioinformatic and biostatistical analyses; E. Lyautey, E. Billard and I. Domaizon drafted the manuscript.

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Correspondence to Emilie Lyautey.

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Lyautey, E., Billard, E., Tissot, N. et al. Seasonal Dynamics of Abundance, Structure, and Diversity of Methanogens and Methanotrophs in Lake Sediments. Microb Ecol 82, 559–571 (2021). https://doi.org/10.1007/s00248-021-01689-9

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Keywords

  • Archaea
  • Bacteria
  • Methane cycle
  • Benthic habitat