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Oxic Methane Cycling: New Evidence for Methane Formation in Oxic Lake Water

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Biogenesis of Hydrocarbons

Abstract

In contrast to common belief, the potent greenhouse gas methane can be produced and emitted from oxygenated water bodies. This has been shown for both marine and freshwater systems over the last decades and has been named “the methane paradox.” The concentration of methane in anoxic sediments is orders of magnitude higher than in the oxic water layers; nevertheless, in most cases, methane from the sediment is oxidized by methanotrophic Bacteria and Archaea near the sediment. In contrast, the methane-rich oxic surface waters are in direct contact with the atmosphere and can be a significant source of atmospheric methane. Several biotic and abiotic mechanisms have been proposed to explain the “methane paradox.” These include the formation of microenvironments suitable for classical anaerobic methanogenesis as well as novel pathways. Among the latter demethylation of methylphosphonates has been proposed as an important pathway in both marine and freshwater systems. We used the meso-oligotrophic Lake Stechlin in northeastern Germany as a model system for methane-emitting freshwater lakes. We showed that oxic methane production was seasonal, occurring mostly in spring and summer. A mass balance of the methane budget suggests minimal methane input from the littoral zone to the oxic pelagic waters and that in situ biological production was the main source of methane in the oxic epi- and metalimnion. Using metagenomic and metatranscriptomic analyses, we showed that Archaea in general as well as key methanogenesis genes were entirely absent from the epi- and metalimnion of the lake. Using incubation experiments, we showed that demethylation of methylphosphonates was a potential mechanism for methane formation in oxic Lake Stechlin water, but it likely was not the most significant process based on gene counts. Addition of trimethylamine, a known precursor to methane in anoxic environments, to lake water also resulted in oxic methane formation. A survey of gene databases revealed that most genes for methanogenesis were present in Bacteria from the lake, suggesting that analogs or paralogs of missing genes may still be identified. We propose that oxic methane formation in Lake Stechlin and other aquatic systems is a result of multiple sequential and parallel pathways.

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References

  • Aben, R.C.H., Barros, N., van Donk, E., Frenken, T., Hilt, S., Kazanjian, G., et al. (2017) Cross continental increase in methane ebullition under climate change. Nat. Commun. 8:1682

    Article  Google Scholar 

  • Allgaier M, Grossart H-P (2006) Diversity and seasonal dynamics of actinobacteria populations in four lakes in northeastern Germany. Appl Environ Microbiol 72:3489–3497

    Article  CAS  Google Scholar 

  • Angel R, Claus P, Conrad R (2012) Methanogenic archaea are globally ubiquitous in aerated soils and become active under wet anoxic conditions. ISME J 6:847–862

    Article  CAS  Google Scholar 

  • Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M, Kulikov AS et al (2012) SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 19:455–477

    Article  CAS  Google Scholar 

  • Bar-Yosef Y, Sukenik A, Hadas O, Viner-Mozzini Y, Kaplan A (2010) Enslavement in the water body by toxic Aphanizomenon ovalisporum, inducing alkaline phosphatase in phytoplanktons. Curr Biol 20:1557–1561

    Article  CAS  Google Scholar 

  • 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(4):1–12. https://doi.org/10.1029/2004GB002238

    Article  Google Scholar 

  • Berg A, Lindblad P, Svensson BH (2014) Cyanobacteria as a source of hydrogen for methane formation. World J Microbiol Biotechnol 30:539–545

    Article  CAS  Google Scholar 

  • Bižić-Ionescu M, Zeder M, Ionescu D, Orlić S, Fuchs BM, Grossart H-P, Amann R (2014) Comparison of bacterial communities on limnic versus coastal marine particles reveals profound differences in colonization. Environ Microbiol 17(10):3500–3514. https://doi.org/10.1111/1462-2920.12466

    Article  Google Scholar 

  • Bodrossy L, Kovács KL, McDonald IR, Murrell JC (1999) A novel thermophilic methane-oxidising γ-proteobacterium. FEMS Microbiol Lett 170:335–341

    CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Bothe H, Distler E, Eisbrenner G (1978) Hydrogen metabolism in blue-green algae. Biochimie 60:277–289

    Article  CAS  Google Scholar 

  • Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Lozupone CA, Turnbaugh PJ et al (2011) Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. Proc Natl Acad Sci USA 108(Suppl 1):4516–4522

    Article  CAS  Google Scholar 

  • Carini P, White AE, Campbell EO, Giovannoni SJ (2014) Methane production by phosphate-starved SAR11 chemoheterotrophic marine bacteria. Nat Commun 5:1–7

    Article  Google Scholar 

  • Caron F, Kramer JR (1994) Formation of volatile sulfides in freshwater environments. Sci Total Environ 153:177–194

    Article  CAS  Google Scholar 

  • Carrión O, Curson ARJ, Kumaresan D, Fu Y, Lang AS, Mercadé E, Todd JD (2015) A novel pathway producing dimethylsulphide in bacteria is widespread in soil environments. Nat Commun 6:6579

    Article  Google Scholar 

  • Damm E, Helmke E, Thoms S, Schauer U, Nöthig E, Bakker K, Kiene RP (2010) Methane production in aerobic oligotrophic surface water in the central Arctic Ocean. Biogeosciences 7:1099–1108

    Article  CAS  Google Scholar 

  • Damm E, Rudels B, Schauer U, Mau S, Dieckmann G (2015) Methane excess in Arctic surface water- triggered by sea ice formation and melting. Sci Rep 5:16179

    Article  CAS  Google Scholar 

  • De Angelis MA, Lee C (1994) Methane production during zooplankton grazing on marine phytoplankton. Limnol Oceanogr 39:1298–1308

    Article  Google Scholar 

  • DelSontro T, McGinnis DF, Sobek S, Ostrovsky I, Wehrli B (2010) Extreme methane emissions from a Swiss hydropower reservoir: contribution from bubbling sediments. Environ Sci Technol 44:2419–2425

    Article  CAS  Google Scholar 

  • DelSontro T, del Giorgio PA, Prairie YT (2017) 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 1–15. https://doi.org/10.1007/s10021-017-0205-1

    Article  Google Scholar 

  • Donis D, Flury S, Stöckli A, Spangenberg JE, Vachon D, McGinnis DF (2017) Full-scale evaluation of methane production under oxic conditions in a mesotrophic lake. Nat Commun 8:1661

    Article  CAS  Google Scholar 

  • Encinas Fernández J, Peeters F, Hofmann H (2016) On the methane paradox: transport from shallow water zones rather than in situ methanogenesis is the major source of CH 4 in the open surface water of lakes. J Geophys Res Biogeosci 121:2717–2726

    Article  Google Scholar 

  • Francis DM, Martodam R (1983) In: Hilderbrand RL (ed) The role of phosphonates in living systems. CRC Press, Boca Raton

    Google Scholar 

  • Garcia SL, et al. (2015) Auxotrophy and intrapopulation complementary in the interactome of a cultivated freshwater model community. Mol. Ecol. 24:4449–4459

    Article  CAS  Google Scholar 

  • Gomez-Garcia MR, Davison M, Blain-Hartnung M, Grossman AR, Bhaya D (2011) Alternative pathways for phosphonate metabolism in thermophilic cyanobacteria from microbial mats. ISME J 5:141–149

    Article  CAS  Google Scholar 

  • Grabherr M, Haas B, Yassour M (2011) Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol 29:644–652

    Article  CAS  Google Scholar 

  • 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 108:19657–19661

    Article  CAS  Google Scholar 

  • Hofmann H (2013) Spatiotemporal distribution patterns of dissolved methane in lakes: how accurate are the current estimations of the diffusive flux path? Geophys Res Lett 40:2779–2784

    Article  CAS  Google Scholar 

  • Ionescu D, Siebert C, Polerecky L, Munwes YYY, Lott C, Häusler S, et al. (2012) Microbial and chemical characterization of underwater fresh water springs in the Dead Sea. PLoS One 7:e38319

    Article  CAS  Google Scholar 

  • Ju K-S, Gao J, Doroghazi JR, Wang K-KA, Thibodeaux CJ, Li S et al (2015) Discovery of phosphonic acid natural products by mining the genomes of 10,000 actinomycetes. Proc Natl Acad Sci 112:12175–12180

    Article  CAS  Google Scholar 

  • Karl DM, Beversdorf L, Björkman KM, Church MJ, Martinez A, Delong EF (2008) Aerobic production of methane in the sea. Nat Geosci 1:473–478

    Article  CAS  Google Scholar 

  • Keppler F, Hamilton JTG, Braß M, Röckmann T (2006) Methane emissions from terrestrial plants under aerobic conditions. Nature 439:187–191

    Article  CAS  Google Scholar 

  • Lenhart K, Bunge M, Ratering S, Neu TR, Schüttmann I, Greule M et al (2012) Evidence for methane production by saprotrophic fungi. Nat Commun 3:1046

    Article  Google Scholar 

  • Lenhart K, Klintzsch T, Langer G, Nehrke G, Bunge M, Schnell S, Keppler F (2016) Evidence for methane production by the marine algae Emiliania huxleyi. Biogeosciences 13:3163–3174

    Article  CAS  Google Scholar 

  • Lupton FS, Marshall KC (1981) Specific adhesion of bacteria to heterocysts of Anabaena spp. and its ecological significance. Appl Environ Microbiol 42:1085–1092

    CAS  PubMed  PubMed Central  Google Scholar 

  • Magen C, Lapham LL, Pohlman JW, Marshall K, Bosman S, Casso M, Chanton JP (2014) A simple headspace equilibration method for measuring dissolved methane. Limnol Oceanogr Methods 12:637–350

    Article  Google Scholar 

  • McAullife C (1971) GC determination of solutes by multiple phase equilibration. Chem Technol 1:46–51

    Google Scholar 

  • McGinnis DF, Kirillin G, Tang KW, Flury S, Bodmer P, Engelhardt C et al (2015) Enhancing surface methane fluxes from an oligotrophic lake: exploring the microbubble hypothesis. Environ Sci Technol 49:873–880

    Article  CAS  Google Scholar 

  • Metcalf WW, Wanner BL (1993) Evidence for a fourteen-gene, phnC to phnP locus for phosphonate metabolism in Escherichia coli. Gene 129:27–32

    Article  CAS  Google Scholar 

  • Metcalf WW, Griffin BM, Cicchillo RM, Gao J, Janga SC, Cooke HA et al (2012) Synthesis of methylphosphonic acid by marine microbes: a source for methane in the aerobic ocean. Science 337(80):1104–1107

    Article  CAS  Google Scholar 

  • Murase J, Sugimoto A (2005) Inhibitory effect of light on methane oxidation in the pelagic water column of a mesotrophic lake (Lake Biwa, Japan). Limnol Oceanogr 50:1339–1343

    Article  CAS  Google Scholar 

  • Murase J, Sakai Y, Sugimoto A, Okubo K, Sakamoto M (2003) Sources of dissolved methane in Lake Biwa. Limnology 4:91–99

    Article  CAS  Google Scholar 

  • Nercessian O, Noyes E, Kalyuzhnaya MG, Lidstrom ME, Chistoserdova L (2005) Bacterial populations active in metabolism of C1 compounds in the sediment of Lake Washington, a freshwater lake. Appl Environ Microbiol 71:6885–6899

    Article  CAS  Google Scholar 

  • Ploug H (2001) Small-scale oxygen fluxes and remineralization in sinking aggregates. Limnol Oceanogr 46:1624–1631

    Article  CAS  Google Scholar 

  • Ploug H, Jorgensen B (1999) A net-jet flow system for mass transfer and microsensor studies of sinking aggregates. Mar Ecol Prog Ser 176:279–290

    Article  CAS  Google Scholar 

  • Repeta DJ, Ferrón S, Sosa OA, Johnson CG, Repeta LD, Acker M et al (2016) Marine methane paradox explained by bacterial degradation of dissolved organic matter. Nat Geosci 9:884–887

    Article  CAS  Google Scholar 

  • Rippka R, Deruelles J, Waterbury JB, Herdman M, Stanier RY (1979) Generic assignments, strain histories and properties of pure cultures of cyanobacteria. J Gen Microbiol 111:1–61

    Google Scholar 

  • Rudd JWM, Hamilton RD (1978) Methane cycling in a cutrophic shield lake and its effects on whole lake metabolism 1. Limnol Oceanogr 23:337–348

    Article  CAS  Google Scholar 

  • Schmale O, Wäge J, Mohrholz V, Wasmund N, Gräwe U, Rehder G, et al (2017) The contribution of zooplankton to methane supersaturation in the oxygenated upper waters of the central Baltic Sea. Limnol Oceanogr 63(1):412–430. https://doi.org/10.1002/lno.10640

    Article  Google Scholar 

  • Schulz M, Faber E, Hollerbach A, Schröder HG, Güde H (2001) The methane cycle in the epilimnion of Lake Constance. Fundam Appl Limnol 151:157–176

    Article  CAS  Google Scholar 

  • Scranton MI, Farrington JW (1977) Methane production in the waters off Walvis Bay. J Geophys Res 82:4947–4953

    Article  CAS  Google Scholar 

  • Selengut JD, Haft DH (2010) Unexpected abundance of coenzyme F420-dependent enzymes in Mycobacterium tuberculosis and other actinobacteria. J Bacteriol 192:5788–5798

    Article  CAS  Google Scholar 

  • Sharp CE, Stott MB, Dunfield PF (2012) Detection of autotrophic verrucomicrobial methanotrophs in a geothermal environment using stable isotope probing. Front Microbiol 3:303

    Article  Google Scholar 

  • Srivastava A, McMahon KD, Stepanauskas R, Grossart HP (2015) De novo synthesis and functional analysis of the phosphatase-encoding gene acI-B of uncultured actinobacteria from Lake Stechlin (NE Germany). Int Microbiol 18:39–47

    PubMed  Google Scholar 

  • Stefels J (2000) Physiological aspects of the production and conversion of DMSP in marine algae and higher plants. In, Journal of Sea Research, pp. 183–197

    Article  CAS  Google Scholar 

  • Stewart FJ, Ottesen EA, DeLong EF (2010) Development and quantitative analyses of a universal rRNA-subtraction protocol for microbial metatranscriptomics. ISME J 4:896–907

    Article  CAS  Google Scholar 

  • Tallant TC, Krzycki JA (1997) Methylthiol:coenzyme M methyltransferase from Methanosarcina barkeri, an enzyme of methanogenesis from dimethylsulfide and methylmercaptopropionate. J Bacteriol 179:6902–6911

    Article  CAS  Google Scholar 

  • Tang K, Dam H, Visscher P, Fenn T (1999) Dimethylsulfoniopropionate (DMSP) in marine copepods and its relation with diets and salinity. Mar Ecol Prog Ser 179:71–79

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Tang KW, McGinnis DF, Ionescu D, Grossart H-P (2016) Methane production in oxic lake waters potentially increases aquatic methane flux to air. Environ Sci Technol Lett 3:227–233

    Article  CAS  Google Scholar 

  • Thompson LR, Sanders JG, McDonald D, Amir A, Ladau J, Locey KJ et al (2017) A communal catalogue reveals Earth’s multiscale microbial diversity. Nature 551:457–463

    Article  CAS  Google Scholar 

  • Vila-Costa M, Simo R, Harada H, Gasol JM, Slezak D, Kiene RP (2006) Dimethylsulfoniopropionate uptake by marine phytoplankton. Science 314(80):652–654

    Article  Google Scholar 

  • Visscher PT, Taylor BF (1993) A new mechanism for the aerobic catabolism of dimethyl sulfide. Appl Environ Microbiol 59:3784–3789

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wackett LP, Wanner BL, Venditti CP, Walsh CT (1987) Involvement of the phosphate regulon and the psiD locus in carbon-phosphorus lyase activity of Escherichia coli K-12. J Bacteriol 169:1753–1756

    Article  CAS  Google Scholar 

  • Wang Q, Dore JE, McDermott TR (2017) Methylphosphonate metabolism by Pseudomonas sp. populations contributes to the methane oversaturation paradox in an oxic freshwater lake. Environ Microbiol 19(6):2366–2378. https://doi.org/10.1111/1462-2920.13747

    Article  CAS  Google Scholar 

  • Wilke A, Bischof J, Gerlach W, Glass E, Harrison T, Keegan KP et al (2016) The MG-RAST metagenomics database and portal in 2015. Nucleic Acids Res 44:D590–D594

    Article  CAS  Google Scholar 

  • Yao M, Henny C, Maresca JA (2016) Freshwater bacteria release methane as a by-product of phosphorus acquisition. Appl Environ Microbiol 82:6994–7003

    Article  CAS  Google Scholar 

  • Yoch D (2001) Dimethylsulfide (DMS) production from dimethylsulfoniopropionate by freshwater river sediments: phylogeny of gram-positive DMS-producing isolates. FEMS Microbiol Ecol 37:31–37

    Article  CAS  Google Scholar 

  • Yu X, Doroghazi JR, Janga SC, Zhang JK, Circello B, Griffin BM et al (2013) Diversity and abundance of phosphonate biosynthetic genes in nature. Proc Natl Acad Sci USA 110:20759–20764

    Article  CAS  Google Scholar 

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Acknowledgments

We thank the Neuglobsow lake lab team for providing O2 and temperature profiler data measured from July 2014 to November 2015. MBI, DI, and HPG were supported by the DFG Aquameth project (GR1540/21-1).

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Correspondence to Mina Bižić-Ionescu or Hans-Peter Grossart .

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Bižić-Ionescu, M., Ionescu, D., Günthel, M., Tang, K.W., Grossart, HP. (2019). Oxic Methane Cycling: New Evidence for Methane Formation in Oxic Lake Water. In: Stams, A., Sousa, D. (eds) Biogenesis of Hydrocarbons. Handbook of Hydrocarbon and Lipid Microbiology . Springer, Cham. https://doi.org/10.1007/978-3-319-78108-2_10

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