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Ecophysiology of Acetoclastic Methanogens

  • Alfons J. M. StamsEmail author
  • Bas Teusink
  • Diana Z. Sousa
Living reference work entry
Part of the Handbook of Hydrocarbon and Lipid Microbiology book series (HHLM)

Abstract

Acetate is the most important precursor for methane in the degradation of organic matter. Only two genera of methanogenic archaea, Methanosarcina and Methanothrix (former Methanosaeta), are able to grow with acetate as sole energy and carbon source. Phylogenetically, Methanosarcina and Methanothrix both belong to the Methanosarcinales. These two genera show besides morphological differences, interesting differences in physiology. Methanosarcina is a generalist that can grow on a variety of substrates, while Methanothrix specialized in growth on acetate. The acetate metabolism shows differences in acetate activation and energy conservation. At conditions that are less favorable for acetoclastic methanogens, syntrophic acetate oxidation may occur. This, however, is not further addressed here.

Notes

Acknowledgments

This research was supported by the Soehngen Institute of Anaerobic Microbiology (SIAM) Gravitation grant (024.002.002) of the Netherlands Ministry of Education, Culture and Science and the Netherlands Organisation for Scientific Research (NWO), and by the ERC Advanced Grant Novel Anaerobes (no. 323009).

References

  1. Albers SV, Meyer BH (2011) The archaeal cell envelope. Nat Rev Microbiol 9:414–426.  https://doi.org/10.1038/nrmicro2576CrossRefPubMedGoogle Scholar
  2. Azman S, Khadem AF, Plugge CM, Stams AJM, Bec S, Zeeman G (2017) Effect of humic acid on anaerobic digestion of cellulose and xylan in completely stirred tank reactors: inhibitory effect, mitigation of the inhibition and the dynamics of the microbial communities. Appl Microbiol Biotechnol 101:889–901.  https://doi.org/10.1007/s00253-016-8010-xCrossRefPubMedGoogle Scholar
  3. Barber RD, Zhang L, Harnack M, Olson MV, Kaul R, Ingram-Smith C, Smith KS (2011) Complete genome sequence of Methanosaeta concilii, a specialist in aceticlastic methanogenesis. J Bacteriol 193:3668–3669.  https://doi.org/10.1128/JB.05031-11CrossRefPubMedPubMedCentralGoogle Scholar
  4. Barker HA (1936) Studies upon the methane-producing bacteria. Arch Mikrobiol 7:420–438.  https://doi.org/10.1007/BF00407414CrossRefGoogle Scholar
  5. Basan M (2018) Resource allocation and metabolism: the search for governing principles. Curr Opin Microbiol 45:77–83.  https://doi.org/10.1016/j.mib.2018.02.008CrossRefPubMedGoogle Scholar
  6. Benedict MN, Gonnerman MC, Metcalf WW, Price ND (2012) Genome-scale metabolic reconstruction and hypothesis testing in the methanogenic archaeon Methanosarcina acetivorans c2a. J Bacteriol 194:855–865.  https://doi.org/10.1128/JB.06040-11CrossRefPubMedPubMedCentralGoogle Scholar
  7. Berger S, Welte C, Deppenmeier U (2012) Acetate activation in Methanosaeta thermophila: characterization of the key enzymes pyrophosphatase and acetyl-CoA synthetase. Archaea 2012:315153.  https://doi.org/10.1155/2012/315153CrossRefPubMedPubMedCentralGoogle Scholar
  8. Boone DR, Kamagata Y (1998) Rejection of the species Methanothrix soehngenii and the genus MethanothrixVP as nomina confusa, and transfer of Methanothrix thermophilaVP to the genus MethanosaetaVP as Methanosaeta thermophila comb. nov. Request for an Opinion. Int J Syst Bacteriol 48:1079–1080.  https://doi.org/10.1099/ijs.0.2008/005355-0CrossRefGoogle Scholar
  9. Branco dos Santos F, de Vos WM, Teusink B (2013) Towards metagenome-scale models for industrial applications – the case of Lactic Acid Bacteria. Curr Opin Biotechnol 24:200–206.  https://doi.org/10.1016/j.copbio.2012.11.003CrossRefPubMedGoogle Scholar
  10. Bryant MP, Campbell LL, Reddy CA, Crabill MR (1977) Growth of Desulfovibrio in lactate or ethanol media low in sulfate in association with H2-utilizing methanogenic bacteria. Appl Environ Microbiol 33:1162–1169PubMedPubMedCentralGoogle Scholar
  11. De Vrieze J, Hennebel T, Boon N, Verstraete W (2012) Methanosarcina: the rediscovered methanogen for heavy duty biomethanation. Bioresour Technol 112:1–9.  https://doi.org/10.1016/j.biortech.2012.02.079CrossRefPubMedGoogle Scholar
  12. Deppenmeier U, Müller V (2007) Life close to the thermodynamic limit: how methanogenic archaea conserve energy. In: Richter D, Tiedge H (eds) Bioenergetics. Springer, Berlin/Heidelberg, pp 123–152.  https://doi.org/10.1007/400_2006_026CrossRefGoogle Scholar
  13. Feist AM, Scholten JCM, Palsson B, Brockman FJ, Ideker T (2006) Modeling methanogenesis with a genome-scale metabolic reconstruction of Methanosarcina barkeri. Mol Syst Biol 2.  https://doi.org/10.1038/msb4100046
  14. Ferry JG (1992) Biochemistry of methanogenesis. Crit Rev Biochem Mol Biol 27(6):473–503.  https://doi.org/10.3109/10409239209082570
  15. Ferry JG (2011) Fundamentals of methanogenic pathways that are key to the biomethanation of complex biomass. Curr Opin Biotechnol 22:351–357.  https://doi.org/10.1016/j.copbio.2011.04.011CrossRefPubMedPubMedCentralGoogle Scholar
  16. Ferry JG (2015) Acetate metabolism in anaerobes from the domain archaea. Life 5:1454–1471.  https://doi.org/10.3390/life5021454CrossRefPubMedPubMedCentralGoogle Scholar
  17. Gottstein W, Olivier BG, Bruggeman FJ, Teusink B (2016) Constraint-based stoichiometric modelling from single organisms to microbial communities. J R Soc Interface 13:20160627.  https://doi.org/10.1098/rsif.2016.0627CrossRefPubMedPubMedCentralGoogle Scholar
  18. Hanemaaijer MJ (2016) Exploring the potential of metabolic models for the study of microbial ecosystems. PhD dissertation, VU Amsterdam. ISBN: 978-94-6299-460-7Google Scholar
  19. Henson MA (2015) Genome-scale modeling of microbial metabolism with temporal and spatial resolution. Biochem Soc Trans 43:1164–1171.  https://doi.org/10.1042/BST20150146CrossRefPubMedPubMedCentralGoogle Scholar
  20. Huser BA, Wuhrmann K, Zehnder AJB (1982) Methanothrix soehngenii gen. nov., a new acetotrophic nonhydrogen-oxidizing methane bacterium. Arch Microbiol 132:1–9.  https://doi.org/10.1007/BF00690808CrossRefGoogle Scholar
  21. Jetten MSM, Stams AJM, Zehnder AJB (1990) Acetate threshold values and acetate activating enzymes in methanogenic bacteria. FEMS Microbiol Ecol 6:339–344.  https://doi.org/10.1111/j.1574-6968.1990.tb03958.xCrossRefGoogle Scholar
  22. Jetten MSM, Stams AJM, Zehnder AJB (1992) Methanogenesis from acetate: a comparison of the acetate metabolism in Methanothrix soehngenii and Methanosarcina spp. FEMS Microbiol Lett 88:181–197.  https://doi.org/10.1111/j.1574-6968.1992.tb04987.xCrossRefGoogle Scholar
  23. Kamagata Y, Kawasaki H, Oyaizu H, Nakamura K, Mikami E, Endo G, Koga Y, Yamasato K (1992) Characterization of three thermophilic strains of Methanothrix (“Methanosaeta”) thermophila sp. nov. and rejection of Methanothrix (“Methanosaeta”) thermoacetophila. Int J Syst Bacteriol 42:463–468.  https://doi.org/10.1099/00207713-42-3-463CrossRefPubMedGoogle Scholar
  24. Kreisl P, Kandler O (1986) Chemical structure of the cell wall polymer of Methanosarcina. Syst Appl Microbiol 7:293–299.  https://doi.org/10.1016/S0723-2020(86)80022-4CrossRefGoogle Scholar
  25. Kümmel A, Panke S, Heinemann M (2006) Systematic assignment of thermodynamic constraints in metabolic network models. BMC Bioinforma 7:512.  https://doi.org/10.1186/1471-2105-7-512CrossRefGoogle Scholar
  26. Laanbroek HJ, Geerligs HJ, Sijtsma VH (1984) Competition for sulfate and ethanol among Desulfobacter, Desulfobulbus, and Desulfovibrio species isolated from intertidal sediments. Appl Environ Microbiol 47:329–334PubMedPubMedCentralGoogle Scholar
  27. Li Q, Li L, Rejtar T, Lessner DJ, Karger BL et al (2006) Electron transport in the pathway of acetate conversion to methane in the marine archaeon Methanosarcina acetivorans. J Bacteriol 188:702–710.  https://doi.org/10.1128/JB.188.2.702-710.2006CrossRefPubMedPubMedCentralGoogle Scholar
  28. Lovley DR (2017) Happy together: microbial communities that hook up to swap electrons. ISME J 11:327–336.  https://doi.org/10.1038/ismej.2016.136CrossRefPubMedGoogle Scholar
  29. Martins G, Salvador AF, Pereira L, Alves MM (2018) Methane production and conductive materials: a critical review. Environ Sci Technol 52:10241–10253.  https://doi.org/10.1021/acs.est.8b01913CrossRefPubMedGoogle Scholar
  30. Morita M, Malvankar NS, Franks AE, Summers ZM, Giloteaux L, Rotaru AE et al (2011) Potential for direct interspecies electron transfer in methanogenic wastewater digester aggregates. MBio 2:e00159–00111.  https://doi.org/10.1128/mBio.00159-11CrossRefGoogle Scholar
  31. Nozhevnikova AN, Chudina VI (1985) Morphology of the thermophilic acetate bacterium Methanothrix thermoacetophila sp. nov. Microbiology 53:618–624Google Scholar
  32. Oude Elferink SJWH, Luppens SBI, Marcelis CLM, Stams AJM (1998) Kinetics of acetate oxidation by two sulfate reducers isolated from anaerobic granular sludge. Appl Environ Microbiol 64:2301–2303Google Scholar
  33. Oude Elferink SJWH, Akkermans-van Vliet WM, Bogte JJ, Stams AJM (1999) Desulfobacca acetoxidans gen. Nov. sp. nov., a novel acetate-degrading sulfate reducer isolated from sulfidogenic sludge. Int J Syst Bacteriol 49:345–350.  https://doi.org/10.1099/00207713-49-2-345CrossRefPubMedGoogle Scholar
  34. Patel GB (1984) Characterization and nutritional properties of Methanothrix concilii sp.nov., a mesophilic, aceticlastic methanogen. Can J Microbiol 30:1383–1396.  https://doi.org/10.1139/m84-221CrossRefGoogle Scholar
  35. Patel GB, Sprott GD (1990) Methanosaeta concilii gen. nov., sp. nov. (“Methanothrix concilii”) and Methanosaeta thermoacetophila nom. rev., comb. nov. Int J Syst Bacteriol 40:79–82.  https://doi.org/10.1099/00207713-40-1-79CrossRefGoogle Scholar
  36. Phelps TJ, Conrad R, Zeikus JG (1985) Sulfate-dependent interspecies H2 transfer between Methanosarcina barkeri and Desulfovibrio vulgaris during coculture metabolism of acetate or methanol. Appl Environ Microbiol 50:589–594PubMedPubMedCentralGoogle Scholar
  37. Plugge CM, Scholten JC, Culley DE, Nie L, Brockman FJ, Zhang W (2010) Global transcriptomics analysis of the Desulfovibrio vulgaris change from syntrophic growth with Methanosarcina barkeri to sulfidogenic metabolism. Microbiology 156:2746–2756.  https://doi.org/10.1099/mic.0.038539-0CrossRefPubMedGoogle Scholar
  38. Rotaru AE, Shrestha PM, Liu F, Markovaite B, Chen S, Nevin KP, Lovley DR (2014a) Direct interspecies electron transfer during syntrophic growth of Geobacter metallireducens and Methanosarcina barkeri on ethanol. Appl Environ Microbiol 80:4599–4605.  https://doi.org/10.1128/AEM.00895-14CrossRefPubMedPubMedCentralGoogle Scholar
  39. Rotaru AE, Shrestha PM, Liu FH, Shrestha M, Shrestha D et al (2014b) A new model for electron flow during anaerobic digestion: direct interspecies electron transfer to Methanosaeta for the reduction of carbon dioxide to methane. Energy Environ Sci 7:408–415.  https://doi.org/10.1039/C3EE42189ACrossRefGoogle Scholar
  40. Schlegel K, Müller V (2013) Evolution of Na+ and H+ bioenergetics in methanogenic archaea. Biochem Soc Trans 41:421–426.  https://doi.org/10.1042/BST20120294CrossRefPubMedGoogle Scholar
  41. Schnellen CGTP (1947) Onderzoekingen over de methaangisting. PhD dissertation, DelftGoogle Scholar
  42. Schnürer A, Zellner G, Svensson BH (1999) Mesophilic syntrophic acetate oxidation during methane formation in biogas reactors. FEMS Microbiol Ecol 29:249–261.  https://doi.org/10.1111/j.1574-6941.1999.tb00616.xCrossRefGoogle Scholar
  43. Scholten JC, Culley DE, Brockman FJ, Wu G, Zhang W (2007) Evolution of the syntrophic interaction between Desulfovibrio vulgaris and Methanosarcina barkeri: involvement of an ancient horizontal gene transfer. Biochem Biophys Res Commun 352:48–54.  https://doi.org/10.1016/j.bbrc.2006.10.164CrossRefPubMedGoogle Scholar
  44. Schönheit P, Kristjansson JK, Thauer RK (1982) Kinetic mechanism for the ability of sulfate reducers to out-compete methanogens for acetate. Arch Microbiol 132:285–288.  https://doi.org/10.1007/BF00407967CrossRefGoogle Scholar
  45. Shapiro B, Hoehler TM, Jin Q (2018) Integrating genome-scale metabolic models into the prediction of microbial kinetics in natural environments. Geochim Cosmochim Acta 242:102–122.  https://doi.org/10.1016/j.gca.2018.08.047CrossRefGoogle Scholar
  46. Shrestha PM, Rotaru AE, Aklujkar M, Liu F, Shrestha M, Summers ZM et al (2013) Syntrophic growth with direct interspecies electron transfer as the primary mechanism for energy exchange. Environ Microbiol Rep 5:904–910.  https://doi.org/10.1111/1758-2229.12093CrossRefPubMedGoogle Scholar
  47. Silva SA, Salvador AF, Cavaleiro AJ, Pereira MA, Stams AJM, Alves MM, Sousa DZ (2016) Toxicity of long chain fatty acids towards acetate conversion by Methanosaeta concilii and Methanosarcina mazei. Microb Biotechnol 9:514–518.  https://doi.org/10.1111/1751-7915.12365CrossRefPubMedPubMedCentralGoogle Scholar
  48. Smith KS, Ingram-Smith C (2011) Methanosaeta, the forgotten methanogen? Trends Microbiol 15:150–155.  https://doi.org/10.1016/j.tim.2007.02.002CrossRefGoogle Scholar
  49. Söhngen N (1906) The formation and disappearance of hydrogen and methane under the influence of organic life. PhD dissertation, DelftGoogle Scholar
  50. Sousa DZ, Alves JI, Alves MM, Smidt H, Stams AJM (2009) Effect of sulfate on methanogenic communities that degrade unsaturated and saturated long-chain fatty acids (LCFA). Environ Microbiol 11:68–80.  https://doi.org/10.1111/j.1462-2920.2008.01740.xCrossRefPubMedGoogle Scholar
  51. Stams AJM, Plugge CM (2009) Electron transfer in syntrophic communities of anaerobic bacteria and archaea. Nat Rev Microbiol 7:568–577.  https://doi.org/10.1038/nrmicro2166CrossRefPubMedGoogle Scholar
  52. Stams AJM, Plugge CM, de Bok FAM, van Houten BHGW, Lens P, Dijkman H, Weijma J (2005) Metabolic interactions in methanogenic and sulfate-reducing bioreactors. Water Sci Technol 52:13–20.  https://doi.org/10.2166/wst.2005.0493CrossRefPubMedGoogle Scholar
  53. Thauer RK, Jungermann K, Decker K (1977) Energy conservation in chemotrophic anaerobic bacteria. Bacteriol Rev 41:100–180PubMedPubMedCentralGoogle Scholar
  54. Tindall BJ (2008) Rejection of the genus name Methanothrix with the species Methanothrix soehngenii Huser et al.. 1983 and transfer of Methanothrix thermophila Kamagata et al. 1992 to the genus Methanosaeta as Methanosaeta thermophila comb. nov. Opinion 75. Int J Syst Evol Microbiol 58:1753–1754.  https://doi.org/10.1099/ijs.0.2008/005355-0CrossRefGoogle Scholar
  55. Tindall BJ (2014) The genus name Methanothrix Huser et al. 1983 and the species combination Methanothrix soehngenii Huser et al. 1983 do not contravene Rule 31a and are not to be considered as rejected names, the genus name Methanosaeta Patel and Sprott 1990 refers to the same taxon as Methanothrix soehngenii Huser et al. 1983 and the species combination Methanothrix thermophila Kamagata et al. 1992 is rejected: supplementary information to Opinion 75. Judicial Commission of the International Committee on Systematics of Prokaryotes. Int J Syst Evol Microbiol 64:3597–3598.  https://doi.org/10.1099/ijs.0.069252-0CrossRefPubMedGoogle Scholar
  56. Touzel JP, Prensier G, Roustan JL, Thomas I, Dubourguier HC, Albagnac G (1988) Description of a new strain of Methanothrix soehngenii and rejection of Methanothrix concilii as a synonym of Methanothrix soehngenii. Int J Syst Bacteriol 38:30–36.  https://doi.org/10.1099/00207713-38-1-30CrossRefGoogle Scholar
  57. ‘t Zandt MH, van den Bosch TJM, Rijkers R, van Kessel MAHJ, Jetten MSM, Welte CU (2018) Co-cultivation of the strictly anaerobic methanogen Methanosarcina barkeri with aerobic methanotrophs in an oxygen-limited membrane bioreactor. Appl Microbiol Biotechnol 102(13):5685–5694.  https://doi.org/10.1007/s00253-018-9038-x
  58. Visser A, Beeksma I, van der Zee A, Stams AJM, Lettinga G (1993) Anaerobic degradation of volatile fatty acids at different sulfate concentrations. Appl Microbiol Biotechnol 40:549–556.  https://doi.org/10.1007/BF00175747CrossRefGoogle Scholar
  59. Wang M, Tomb JF, Ferry JG (2011) Electron transport in acetate-grown Methanosarcina acetivorans. BMC Microbiol 11:165.  https://doi.org/10.1186/1471-2180-11-165CrossRefPubMedPubMedCentralGoogle Scholar
  60. Wang LY, Nevin KP, Woodard TL, Mu BZ, Lovley DR (2016) Expanding the diet for DIET: electron donors supporting direct interspecies electron transfer (DIET) in defined co-cultures. Front Microbiol 7:236.  https://doi.org/10.3389/fmicb.2016.00236CrossRefPubMedPubMedCentralGoogle Scholar
  61. Welte C, Deppenmeier U (2011) Membrane-bound electron transport in Methanosaeta thermophila. J Bacteriol 193:2868–2870.  https://doi.org/10.1128/JB.00162-11CrossRefPubMedPubMedCentralGoogle Scholar
  62. Welte C, Deppenmeier U (2014) Bioenergetics and anaerobic respiratory chains of aceticlastic methanogens. Biochim Biophys Acta 1837:1130–1147.  https://doi.org/10.1016/j.bbabio.2013.12.002CrossRefPubMedGoogle Scholar
  63. Zhu J, Zheng H, Ai G, Zhang G, Liu D, Liu X, Dong X (2012) The genome characteristics and predicted function of methyl-group oxidation pathway in the obligate aceticlastic methanogens, Methanosaeta spp. PLoS One 7(5):e36756.  https://doi.org/10.1371/journal.pone.0036756CrossRefPubMedPubMedCentralGoogle Scholar
  64. Zinder SH, Koch M (1984) Non-aceticlastic methanogenesis from acetate: acetate oxidation by a thermophilic syntrophic coculture. Arch Microbiol 138:263–272.  https://doi.org/10.1007/BF00402133CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Alfons J. M. Stams
    • 1
    • 2
    Email author
  • Bas Teusink
    • 3
  • Diana Z. Sousa
    • 1
  1. 1.Laboratory of MicrobiologyWageningen University and ResearchWageningenThe Netherlands
  2. 2.Centre of Biological Engineering, University of MinhoBragaPortugal
  3. 3.Laboratory of Systems BioinformaticsFree University of AmsterdamAmsterdamThe Netherlands

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