Wide diversity of methane and short-chain alkane metabolisms in uncultured archaea (original) (raw)

References

  1. Demirel, B. & Scherer, P. The roles of acetotrophic and hydrogenotrophic methanogens during anaerobic conversion of biomass to methane: a review. Rev. Environ. Sci. Biotechnol. 7, 173–190 (2008).
    Article CAS Google Scholar
  2. Schink, B. Energetics of syntrophic cooperation in methanogenic degradation. Microbiol. Mol. Biol. Rev. 61, 262–280 (1997).
    CAS PubMed PubMed Central Google Scholar
  3. Ueno, Y., Yamada, K., Yoshida, N., Maruyama, S. & Isozaki, Y. Evidence from fluid inclusions for microbial methanogenesis in the early Archaean era. Nature 440, 516–519 (2006).
    Article CAS Google Scholar
  4. Sousa, F. L. et al. Early bioenergetic evolution.Philos. Trans. R Soc. Lond. B 368, 20130088 (2013).
    Article Google Scholar
  5. Kasting, J. F. & Siefert, J. L. Life and the evolution of Earth’s atmosphere. Science 296, 1066–1068 (2002).
    Article CAS Google Scholar
  6. Bapteste, E., Brochier, C. & Boucher, Y. Higher-level classification of the Archaea: evolution of methanogenesis and methanogens. Archaea. 1, 353–363 (2005).
    Article CAS Google Scholar
  7. Whitman, W. B., Bowen, T. L. & Boone, D. R. The Methanogenic Bacteria. Prokaryotes Vol. 3 (Springer, New York, 2006); https://doi.org/10.1007/0-387-30743-5_9
    Chapter Google Scholar
  8. Kendall, M. M. & Boone, D. R. in The Prokaryotes 244–256 (Springer, New York, 2006); https://doi.org/10.1007/0-387-30743-5_12
    Chapter Google Scholar
  9. Oren, A. in The Prokaryotes: Other Major Lineages of Bacteria and The Archaea (eds Rosenberg, E. et al.) 165–193 (Springer, New York, 2014).
  10. Borrel, G., Adam, P. S. & Gribaldo, S. Methanogenesis and the Wood-Ljungdahl pathway: an ancient, versatile, and fragile association. Genome Biol. Evol. 8, 1706–1711 (2016).
    Article CAS Google Scholar
  11. Timmers, P. H. A. et al. Reverse methanogenesis and respiration in Methanotrophic Archaea. Archaea 2017, 1654237 (2017).
    Article Google Scholar
  12. Scheller, S., Ermler, U. & Shima, S. in Anaerobic Utilization of Hydrocarbons, Oils, and Lipids (ed. Bool, M.) 1–29 (Springer, Chamonix, 2017); https://doi.org/10.1007/978-3-319-33598-8_3-1.
    Google Scholar
  13. Hallam, S. J. et al. Reverse methanogenesis: testing the hypothesis with environmental genomics. Science 305, 1457–1462 (2004).
    Article CAS Google Scholar
  14. Adam, P. S., Borrel, G., Brochier-Armanet, C. & Gribaldo, S. The growing tree of Archaea: new perspectives on their diversity, evolution and ecology. ISME. J. 11, 2407–2425 (2017).
    Article Google Scholar
  15. Spang, A., Caceres, E. F. & Ettema, T. J. G. Genomic exploration of the diversity, ecology, and evolution of the archaeal domain of life. Science 357, pii: eaaf3883 (2017).
    Article Google Scholar
  16. Borrel, G. et al. Phylogenomic data support a seventh order of methylotrophic methanogens and provide insights into the evolution of methanogenesis. Genome Biol. Evol. 5, 1769–1780 (2013).
    Article CAS Google Scholar
  17. Nobu, M. K., Narihiro, T., Kuroda, K., Mei, R. & Liu, W.-T. Chasing the elusive Euryarchaeota class WSA2: genomes reveal a uniquely fastidious methyl-reducing methanogen. ISME. J. 10, 2478–2487 (2016).
    Article CAS Google Scholar
  18. Sorokin, D. Y. et al. Discovery of extremely halophilic, methyl-reducing euryarchaea provides insights into the evolutionary origin of methanogenesis. Nat. Microbiol. 2, 17081 (2017).
    Article CAS Google Scholar
  19. Vanwonterghem, I. et al. Methylotrophic methanogenesis discovered in the novel archaeal phylum Verstraetearchaeota. Nat. Microbiol. 1, 16170 (2016).
    Article CAS Google Scholar
  20. Brugère, J. F. et al. Archaebiotics: proposed therapeutic use of archaea to prevent trimethylaminuria and cardiovascular disease. Gut Microbes 5, 5–10 (2014).
    Article Google Scholar
  21. Laso-Pérez, R. et al. Thermophilic Archaea activate butane via alkyl-coenzyme M formation. Nature 539, 396–401 (2016).
    Article Google Scholar
  22. Evans, P. N. et al. Methane metabolism in the archaeal phylum Bathyarchaeota revealed by genome-centric metagenomics. Science 350, 434–438 (2015).
    Article CAS Google Scholar
  23. Dombrowski, N., Seitz, K. W., Teske, A. P. & Baker, B. J. Genomic insights into potential interdependencies in microbial hydrocarbon and nutrient cycling in hydrothermal sediments.Microbiome 5, 106 (2017).
    Article Google Scholar
  24. McKay, L. J., & Hatzenpichler, R., Inskeep, W. P. & Fields, M. W. Occurrence and expression of novel methyl-coenzyme M reductase gene (mcrA) variants in hot spring sediments. Sci. Rep. 7, 7252 (2017).
    Article Google Scholar
  25. Hawley, E. R. et al. Metagenomes from two microbial consortia associated with Santa Barbara seep oil. Mar. Genomics 18, 97–99 (2014).
    Article Google Scholar
  26. Seitz, K. W., Lazar, C. S., Hinrichs, K.-U., Teske, A. P. & Baker, B. J. Genomic reconstruction of a novel, deeply branched sediment archaeal phylum with pathways for acetogenesis and sulfur reduction. ISME. J. 10, 1696–1705 (2016).
    Article CAS Google Scholar
  27. Mckay, L. J. et al. Co-occurring genomic capacity for anaerobic methane and dissimilatory sulfur metabolisms discovered in the Korarchaeota. Nat. Microbiol. https://doi.org/10.1038/s41564-019-0362-4 (2019).
    Article CAS Google Scholar
  28. Ermler, U., Grabarse, W., Shima, S., Goubeaud, M. & Thauer, R. K. Crystal structure of methyl-coenzyme M reductase: the key enzyme of biological methane formation. Science 278, 1457–1462 (1997).
    Article CAS Google Scholar
  29. Arshad, A. et al. A metagenomics-based metabolic model of nitrate-dependent anaerobic oxidation of methane by Methanoperedens-like archaea. Front. Microbiol. 6, 1423 (2015).
    Article Google Scholar
  30. Wegener, G., Krukenberg, V., Riedel, D., Tegetmeyer, H. E. & Boetius, A. Intercellular wiring enables electron transfer between methanotrophic archaea and bacteria. Nature 526, 587–590 (2015).
    Article CAS Google Scholar
  31. McGlynn, S. E., Chadwick, G. L., Kempes, C. P. & Orphan, V. J. Single cell activity reveals direct electron transfer in methanotrophic consortia. Nature 526, 531–535 (2015).
    Article CAS Google Scholar
  32. Meyerdierks, A. et al. Metagenome and mRNA expression analyses of anaerobic methanotrophic archaea of the ANME-1 group. Environ. Microbiol. 12, 422–439 (2010).
    Article CAS Google Scholar
  33. Grimaldi, S., Schoepp-Cothenet, B., Ceccaldi, P., Guigliarelli, B. & Magalon, A. The prokaryotic Mo/W-bisPGD enzymes family: a catalytic workhorse in bioenergetic. Biochim. Biophys. Acta Bioenerg. 1827, 1048–1085 (2013).
    Article CAS Google Scholar
  34. Jormakka, M. et al. Molecular mechanism of energy conservation in polysulfide respiration. Nat. Struct. Mol. Biol. 15, 730–737 (2008).
    Article CAS Google Scholar
  35. Hagemeier, C. H., Chistoserdova, L., Lidstrom, M. E., Thauer, R. K. & Vorholt, J. A. Characterization of a second methylene tetrahydromethanopterin dehydrogenase from Methylobacterium extorquens AM1. Eur. J. Biochem. 267, 3762–3769 (2000).
    Article CAS Google Scholar
  36. McInerney, M. J. et al. The genome of Syntrophus aciditrophicus: life at the thermodynamic limit of microbial growth. Proc. Natl Acad. Sci. USA 104, 7600–7605 (2007).
    Article Google Scholar
  37. Klenk, H.-P. et al. The complete genome sequence of the hyperthermophilic, sulphate-reducing archaeon Archaeoglobus fulgidus. Nature 390, 364–370 (1997).
    Article CAS Google Scholar
  38. Milkov, A. V. Molecular and stable isotope compositions of natural gas hydrates: a revised global dataset and basic interpretations in the context of geological settings. Org. Geochem. 36, 681–702 (2005).
    Article CAS Google Scholar
  39. Meredith, W., Kelland, S. J. & Jones, D. M. Influence of biodegradation on crude oil acidity and carboxylic acid composition. Org. Geochem. 31, 1059–1073 (2000).
    Article CAS Google Scholar
  40. Sieber, J. R., McInerney, M. J. & Gunsalus, R. P. Genomic insights into syntrophy: the paradigm for anaerobic metabolic cooperation. Annu. Rev. Microbiol. 66, 429–452 (2012).
    Article CAS Google Scholar
  41. Zengler, K., Richnow, H. H., Rosselló-Mora R., Michaelis, W. & Widdel, F. Methane formation from long-chain alkanes by anaerobic microorganisms. Nature 401, 266–269, https://doi.org/10.1038/45777 (1999).
    Article CAS PubMed Google Scholar
  42. Stams, A. J. M., Sousa, D. Z., Kleerebezem, R. & Plugge, C. M. Role of syntrophic microbial communities in high-rate methanogenic bioreactors. Water Sci. Technol. 66, 353–363 (2012).
    Article Google Scholar
  43. Gao, B. & Gupta, R. S. Phylogenomic analysis of proteins that are distinctive of Archaea and its main subgroups and the origin of methanogenesis. BMC Genomics 8, 86 (2007).
    Article Google Scholar
  44. Kaster, A. K. More than 200 genes required for methane formation from H2 and CO2 and energy conservation are present in Methanothermobacter marburgensis and Methanothermobacter thermautotrophicus. Archaea 2011, 973848 (2011).
    Article Google Scholar
  45. Nayak, D. D., Mahanta, N., Mitchell, D. A. & Metcalf, W. W. Post-translational thioamidation of methyl-coenzyme M reductase, a key enzyme in methanogenic and methanotrophic archaea. eLife 6, e29218 (2017).
    Article Google Scholar
  46. Lyu, Z. et al. Mmp10 is required for post-translational methylation of arginine at the active site of methyl-coenzyme M reductase. Preprint at BioRxiv https://doi.org/10.1101/211441 (2017).
  47. Sarmiento, F., Mrázek, J. & Whitman, W. B. Genome-scale analysis of gene function in the hydrogenotrophic methanogenic archaeon Methanococcus maripaludis. Proc. Natl Acad. Sci. USA 110, 4726–4731 (2013).
    Article CAS Google Scholar
  48. Wagner, T., Kahnt, J., Ermler, U. & Shima, S. Didehydroaspartate modification in methyl-coenzyme M reductase catalyzing methane formation. Angew. Chemie - Int. Ed. 55, 10630–10633 (2016).
    Google Scholar
  49. Borrel, G. et al. Comparative genomics highlights the unique biology of Methanomassiliicoccales, a Thermoplasmatales-related seventh order of methanogenic archaea that encodes pyrrolysine. BMC Genomics 15, 679 (2014).
    Article Google Scholar
  50. Zheng, K., Ngo, P. D., Owens, V. L., Yang, X. & Mansoorabadi, S. O. The biosynthetic pathway of coenzyme F430 in methanogenic and methanotrophic archaea. Science 354, 339–342 (2016).
    Article CAS Google Scholar
  51. Prakash, D., Wu, Y., Suh, S. J. & Duin, E. C. Elucidating the process of activation of methyl-coenzyme M reductase. J. Bacteriol. 196, 2491–2498 (2014).
    Article Google Scholar
  52. Li, J. et al. Global mapping transcriptional start sites revealed both transcriptional and post-transcriptional regulation of cold adaptation in the methanogenic archaeon Methanolobus psychrophilus. Sci. Rep. 5, 9209 (2015).
    Article CAS Google Scholar
  53. Raymann, K., Brochier-Armanet, C. & Gribaldo, S. The two-domain tree of life is linked to a new root for the Archaea. Proc. Natl Acad. Sci. USA 112, 6670–6675 (2015).
    Article CAS Google Scholar
  54. Weiss, M. C. et al. The physiology and habitat of the last universal common ancestor. Nat. Microbiol. 1, 16116 (2016).
    Article CAS Google Scholar
  55. Adam, P. S., Borrel, G. & Gribaldo, S. Evolutionary history of carbon monoxide dehydrogenase/acetyl-CoA synthase, one of the oldest enzymatic complexes. Proc. Natl Acad. Sci. USA 115, E5837 (2018).
    Article Google Scholar
  56. McGlynn, S. E. Energy metabolism during anaerobic methane oxidation in ANME Archaea. Microbes Environ. 32, 5–13 (2017).
    Article Google Scholar
  57. Katoh, K. & Standley, D. M. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol. Biol. Evol. 30, 772–780 (2013).
    Article CAS Google Scholar
  58. Criscuolo, A. & Gribaldo, S. BMGE (block mapping and gathering with entropy): a new software for selection of phylogenetic informative regions from multiple sequence alignments. BMC Evol. Biol. 10, 210 (2010).
    Article Google Scholar
  59. Nguyen, L. T., Schmidt, H. A., Von Haeseler, A. & Minh, B. Q. IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol. Biol. Evol. 32, 268–274 (2015).
    Article CAS Google Scholar
  60. Nurk, S., Meleshko, D., Korobeynikov, A. & Pevzner, P. A. MetaSPAdes: a new versatile metagenomic assembler. Genome Res. 27, 824–834 (2017).
    Article CAS Google Scholar
  61. Peng, Y., Leung, H. C. M., Yiu, S.-M. & Chin, F. Y. L. IDBA-UD: a de novo assembler for single-cell and metagenomic sequencing data with highly uneven depth. Bioinformatics 28, 1420–1428 (2012).
    Article CAS Google Scholar
  62. Kang, D. D., Froula, J., Egan, R. & Wang, Z. MetaBAT, an efficient tool for accurately reconstructing single genomes from complex microbial communities. Peer J. 3, e1165 (2015).
    Article Google Scholar
  63. Wu, Y. W., Simmons, B. A. & Singer, S. W. MaxBin 2.0: an automated binning algorithm to recover genomes from multiple metagenomic datasets. Bioinformatics 32, 605–607 (2015).
    Article Google Scholar
  64. Alneberg, J. et al. Binning metagenomic contigs by coverage and composition. Nat. Methods 11, 1144–1146 (2014).
    Article CAS Google Scholar
  65. Sieber, C. M. K. et al. Recovery of genomes from metagenomes via a dereplication, aggregation, and scoring strategy. Nat. Microbiol. 3, 836–843 (2018).
  66. Parks, D. H., Imelfort, M., Skennerton, C. T., Hugenholtz, P. & Tyson, G. W. CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes. Genome Res. 25, 1043–1055 (2015).
    Article CAS Google Scholar
  67. Darling, A. E. et al. PhyloSift: phylogenetic analysis of genomes and metagenomes. Peer J. 2, e243 (2014).
    Article Google Scholar
  68. Kobert, K., Salichos, L., Rokas, A. & Stamatakis, A. Computing the internode certainty and related measures from partial gene trees. Mol. Biol. Evol. 33, 1606–1617 (2016).
    Article CAS Google Scholar
  69. Stamatakis, A. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22, 2688–2690 (2006).
    Article CAS Google Scholar
  70. Lartillot, N., Lepage, T. & Blanquart, S. PhyloBayes 3: a Bayesian software package for phylogenetic reconstruction and molecular dating. Bioinformatics 25, 2286–2288 (2009).
    Article CAS Google Scholar
  71. Hyatt, D. et al. Prodigal: prokaryotic gene recognition and translation initiation site identification. BMC Bioinformatics 11, 119 (2010).
    Article Google Scholar
  72. Aziz, R. K. et al. The RAST server: rapid annotations using subsystems technology. BMC Genomics 9, 75 (2008).
    Article Google Scholar
  73. Oberto, J. SyntTax: a web server linking synteny to prokaryotic taxonomy. BMC Bioinformatics 14, 4 (2013).
    Article Google Scholar
  74. Marchler-Bauer, A. et al. CDD: NCBI’s conserved domain database. Nucleic Acids Res. 43, D222–D226 (2015).
    Article CAS Google Scholar
  75. Abby, S. S., Néron, B., Ménager, H., Touchon, M. & Rocha, E. P. A. MacSyFinder: a program to mine genomes for molecular systems with an application to CRISPR-Cas systems.PLoS One 9, e110726(2014).
    Article Google Scholar
  76. Kahnt, J. et al. Post-translational modifications in the active site region of methyl-coenzyme M reductase from methanogenic and methanotrophic archaea. FEBS. J. 274, 4913–4921 (2007).
    Article CAS Google Scholar

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