Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

Horizontal gene transfer constrains the timing of methanogen evolution

Abstract

Microbial methanogenesis may have been a major component of Earth’s carbon cycle during the Archaean eon, generating a methane greenhouse that increased global temperatures enough for a liquid hydrosphere, despite the Sun’s lower luminosity at the time. Evaluation of potential solutions to the ‘faint young Sun’ hypothesis by determining the age of microbial methanogenesis has been limited by ambiguous geochemical evidence and the absence of a diagnostic fossil record. To overcome these challenges, we use a temporal constraint: a horizontal gene transfer event from within archaeal methanogens to the ancestor of Cyanobacteria, one of the few microbial clades with recognized crown-group fossils. Results of molecular clock analyses calibrated by this horizontal-gene-transfer-propagated constraint show methanogens diverging within Euryarchaeota no later than 3.51 billion years ago, with methanogenesis itself probably evolving earlier. This timing provides independent support for scenarios wherein microbial methane production was important in maintaining temperatures on the early Earth.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

Fig. 1: Concatenated PhyloBayes gene tree of smc, scpA and scpB for Euryarchaeota, with HGT to Aquificales and Cyanobacteria.
Fig. 2: Comparisons of date estimates for Cyanobacteria, methanogenic Euryarchaeota and crown Euryarchaeota, obtained from fixed topologies.
Fig. 3: Most conservative divergence time estimates of Euryarchaeota and Cyanobacteria from composite alignment.

References

  1. 1.

    Battistuzzi, F. U., Feijao, A. & Hedges, S. B. A genomic timescale of prokaryote evolution: insights into the origin of methanogenesis, phototrophy, and the colonization of land. BMC Evol. Biol. 4, 44 (2004).

    Article  PubMed  PubMed Central  Google Scholar 

  2. 2.

    Haqq-Misra, J. D., Domagal-Goldman, S. D., Kasting, P. J. & Kasting, J. F. A revised, hazy methane greenhouse for the Archean Earth. Astrobiology 8, 1127–1137 (2008).

    CAS  Article  PubMed  Google Scholar 

  3. 3.

    Gao, B. & Gupta, R. S. Phylogenomic analysis of proteins that are distinctive of archaea and its main subgroups and the origin of methanogenesis. BMC Genom. 8, 86 (2007).

    Article  Google Scholar 

  4. 4.

    Hinrichs, K.-U. Microbial fixation of methane carbon at 2.7 Ga: was an anaerobic mechanism possible? Geochem. Geophys. Geosyst. 3, 1–10 (2002).

    Article  Google Scholar 

  5. 5.

    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).

    CAS  Article  PubMed  Google Scholar 

  6. 6.

    Marin, J., Battistuzzi, F. U., Brown, A. C. & Hedges, S. B. The timetree of prokaryotes: new insights into their evolution and speciation. Mol. Biol. Evol. 34, 437–446 (2017).

    PubMed  Google Scholar 

  7. 7.

    Battistuzzi, F. U. & Hedges, S. B. A major clade of prokaryotes with ancient adaptations to life on land. Mol. Biol. Evol. 26, 335–343 (2009).

    CAS  Article  PubMed  Google Scholar 

  8. 8.

    Sheridan, P. P., Freeman, K. H. & Brenchley, J. E. Estimated minimal divergence times of the major bacterial and archaeal phyla. Geomicrobiol. J. 20, 1–14 (2003).

    CAS  Article  Google Scholar 

  9. 9.

    Blank, C. E. Not so old archaea—the antiquity of biogeochemical processes in the archaeal domain of life. Geobiology 7, 495–514 (2009).

    CAS  Article  PubMed  Google Scholar 

  10. 10.

    Lozano-Fernandez, J., dos Reis, M., Donoghue, P. C. J. & Pisani, D. RelTime rates collapse to a strict clock when estimating the timeline of animal diversification. Genome Biol. Evol. 9, 1320–1328 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  11. 11.

    Parham, J. F. et al. Best practices for justifying fossil calibrations. Syst. Biol. 61, 346–359 (2012).

    Article  PubMed  Google Scholar 

  12. 12.

    Brocks, J. J. & Pearson, A. Building the biomarker tree of life. Rev. Mineral. Geochem. 59, 233–258 (2005).

    CAS  Article  Google Scholar 

  13. 13.

    Rasmussen, B., Fletcher, I. R., Brocks, J. J. & Kilburn, M. R. Reassessing the first appearance of eukaryotes and cyanobacteria. Nature 455, 1101–1104 (2008).

    CAS  Article  PubMed  Google Scholar 

  14. 14.

    Hug, L. A. et al. A new view of the tree of life. Nat. Microbiol. 1, 16048 (2016).

    CAS  Article  PubMed  Google Scholar 

  15. 15.

    Da Cunha, V., Gaia, M., Gadelle, D., Nasir, A. & Forterre, P. Lokiarchaea are close relatives of Euryarchaeota, not bridging the gap between prokaryotes and eukaryotes. PLoS Genet. 13, e1006810 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  16. 16.

    Drummond, A. J., Ho, S. Y. W., Phillips, M. J. & Rambaut, A. Relaxed phylogenetics and dating with confidence. PLoS Biol. 4, e88 (2006).

    Article  PubMed  PubMed Central  Google Scholar 

  17. 17.

    Gogarten, J. P., Murphey, R. D. & Olendzenski, L. Horizontal gene transfer: pitfalls and promises. Biol. Bull. 196, 359–362 (1999).

    CAS  Article  PubMed  Google Scholar 

  18. 18.

    Huang, J., Xu, Y. & Gogarten, J. P. The presence of a haloarchaeal type tyrosyl-tRNA synthetase marks the opisthokonts as monophyletic. Mol. Biol. Evol. 22, 2142–2146 (2005).

    CAS  Article  PubMed  Google Scholar 

  19. 19.

    Petitjean, C., Moreira, D., López-García, P. & Brochier-Armanet, C. Horizontal gene transfer of a chloroplast DnaJ-Fer protein to Thaumarchaeota and the evolutionary history of the DnaK chaperone system in archaea. BMC Evol. Biol. 12, 226 (2012).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  20. 20.

    Szöllősi, G. J., Boussau, B., Abby, S. S., Tannier, E. & Daubin, V. Phylogenetic modeling of lateral gene transfer reconstructs the pattern and relative timing of speciations. Proc. Natl Acad. Sci. USA 109, 17513–17518 (2012).

    Article  PubMed  PubMed Central  Google Scholar 

  21. 21.

    Szöllősi, G. J., Tannier, E., Lartillot, N. & Daubin, V. Lateral gene transfer from the dead. Syst. Biol. 62, 386–397 (2013).

    Article  PubMed  PubMed Central  Google Scholar 

  22. 22.

    Rothman, D. H. et al. Methanogenic burst in the end-Permian carbon cycle. Proc. Natl Acad. Sci. USA 111, 5462–5467 (2014).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  23. 23.

    Sauquet, H. et al. Testing the impact of calibration on molecular divergence times using a fossil-rich group: the case of Nothofagus (Fagales). Syst. Biol. 61, 289–313 (2012).

    Article  PubMed  Google Scholar 

  24. 24.

    Schenk, J. J. Consequences of secondary calibrations on divergence time estimates. PLoS ONE 11, e0148228 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  25. 25.

    Soppa, J. Prokaryotic structural maintenance of chromosomes (SMC) proteins: distribution, phylogeny, and comparison with MukBs and additional prokaryotic and eukaryotic coiled-coil proteins. Gene 278, 253–264 (2001).

    CAS  Article  PubMed  Google Scholar 

  26. 26.

    Cobbe, N. & Heck, M. M. S. The evolution of SMC proteins: phylogenetic analysis and structural implications. Mol. Biol. Evol. 21, 332–347 (2003).

    Article  PubMed  Google Scholar 

  27. 27.

    Zheng, Y. & Wiens, J. J. Do missing data influence the accuracy of divergence-time estimation with BEAST? Mol. Phylogenet. Evol. 85, 41–49 (2015).

    Article  PubMed  Google Scholar 

  28. 28.

    Amard, B. & Bertrand-Sarfati, J. Microfossils in 2000 Ma old cherty stromatolites of the Franceville Group, Gabon. Precambrian Res. 81, 197–221 (1997).

    CAS  Article  Google Scholar 

  29. 29.

    Luo, G. et al. Rapid oxygenation of Earth’s atmosphere 2.33 billion years ago. Sci. Adv. 2, e1600134 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  30. 30.

    Valley, J. W. et al. Hadean age for a post-magma-ocean zircon confirmed by atom-probe tomography. Nat. Geosci. 7, 219–223 (2014).

    CAS  Article  Google Scholar 

  31. 31.

    Tomitani, A., Knoll, A. H., Cavanaugh, C. M. & Ohno, T. The evolutionary diversification of cyanobacteria: molecular–phylogenetic and paleontological perspectives. Proc. Natl Acad. Sci. USA 103, 5442–5447 (2006).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  32. 32.

    Butterfield, N. J. Proterozoic photosynthesis—a critical review. Palaeontology 58, 953–972 (2015).

    Article  Google Scholar 

  33. 33.

    Horodyski, R. J. & Donaldson, J. A. Microfossils from the Middle Proterozoic Dismal Lakes Group, Arctic Canada. Precambrian Res. 11, 125–159 (1980).

    Article  Google Scholar 

  34. 34.

    Duchêne, S., Lanfear, R. & Ho, S. Y. W. The impact of calibration and clock-model choice on molecular estimates of divergence times. Mol. Phylogenet. Evol. 78, 277–289 (2014).

    Article  PubMed  Google Scholar 

  35. 35.

    Toussaint, E. F. & Condamine, F. L. To what extent do new fossil discoveries change our understanding of clade evolution? A cautionary tale from burying beetles (Coleoptera: Nicrophorus). Biol. J. Linn. Soc. 117, 686–704 (2016).

    Article  Google Scholar 

  36. 36.

    Shih, P. M., Hemp, J., Ward, L. M., Matzke, N. J. & Fischer, W. W. Crown group Oxyphotobacteria postdate the rise of oxygen. Geobiology 15, 19–29 (2017).

    CAS  Article  PubMed  Google Scholar 

  37. 37.

    Evans, P. N. et al. Methane metabolism in the archaeal phylum Bathyarchaeota revealed by genome-centric metagenomics. Science 350, 434–438 (2015).

    CAS  Article  PubMed  Google Scholar 

  38. 38.

    Vanwonterghem, I. et al. Methylotrophic methanogenesis discovered in the archaeal phylum Verstraetearchaeota. Nat. Microbiol. 1, 16170 (2016).

    CAS  Article  PubMed  Google Scholar 

  39. 39.

    Barker, J. F. & Fritz, P. Carbon isotope fractionation during microbial methane oxidation. Nature 293, 289–291 (1981).

    CAS  Article  Google Scholar 

  40. 40.

    Reeburgh, W. S. Oceanic methane biogeochemistry. Chem. Rev. 107, 486–513 (2007).

    CAS  Article  PubMed  Google Scholar 

  41. 41.

    Holler, T. et al. Substantial 13C/12C and D/H fractionation during anaerobic oxidation of methane by marine consortia enriched in vitro. Environ. Microbiol. Rep. 1, 370–376 (2009).

    CAS  Article  PubMed  Google Scholar 

  42. 42.

    Suda, K. et al. Origin of methane in serpentinite-hosted hydrothermal systems: The CH4–H2–H2O hydrogen isotope systematics of the Hakuba Happo hot spring. Earth Planet. Sci. Lett. 386, 112–125 (2014).

    CAS  Article  Google Scholar 

  43. 43.

    Blank, C. E. Phylogenomic dating—the relative antiquity of archaeal metabolic and physiological traits. Astrobiology 9, 193–219 (2009).

    CAS  Article  PubMed  Google Scholar 

  44. 44.

    David, L. A. & Alm, E. J. Rapid evolutionary innovation during an Archaean genetic expansion. Nature 469, 93–96 (2011).

    CAS  Article  PubMed  Google Scholar 

  45. 45.

    Shih, P. M. & Matzke, N. J. Primary endosymbiosis events date to the later Proterozoic with cross-calibrated phylogenetic dating of duplicated ATPase proteins. Proc. Natl Acad. Sci. USA 110, 12355–12360 (2013).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  46. 46.

    Harmon, L. J. et al. Arbor: comparative analysis workflows for the tree of life. PLoS Curr. 5, https://doi.org/10.1371/currents.tol.099161de5eabdee073fd3d21a44518dc (2013).

  47. 47.

    Uyeda, J. C., Harmon, L. J. & Blank, C. E. A comprehensive study of cyanobacterial morphological and ecological evolutionary dynamics through deep geologic time. PLoS ONE 11, e0162539 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  48. 48.

    Edgar, R. C. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32, 1792–1797 (2004).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  49. 49.

    Melby, T. E., Ciampaglio, C. N., Briscoe, G. & Erickson, H. P. The symmetrical structure of structural maintenance of chromosomes (SMC) and MukB proteins: long, antiparallel coiled coils, folded at a flexible hinge. J. Cell Biol. 142, 1595–1604 (1998).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  50. 50.

    Penn, O. et al. GUIDANCE: a web server for assessing alignment confidence scores. Nucleic Acids Res. 38, W23–W28 (2010).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  51. 51.

    Tan, G. et al. Current methods for automated filtering of multiple sequence alignments frequently worsen single-gene phylogenetic inference. Syst. Biol. 64, 778–791 (2015).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  52. 52.

    Stamatakis, A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30, 1312–1313 (2014).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  53. 53.

    Le, S. Q., Dang, C. C. & Gascuel, O. Modeling protein evolution with several amino acid replacement matrices depending on site rates. Mol. Biol. Evol. 29, 2921–2936 (2012).

    CAS  Article  PubMed  Google Scholar 

  54. 54.

    Kück, P. & Meusemann, K. FASconCAT: convenient handling of data matrices. Mol. Phylogenet. Evol. 56, 1115–1118 (2010).

    Article  PubMed  Google Scholar 

  55. 55.

    Lartillot, N., Rodrigue, N., Stubbs, D. & Richer, J. PhyloBayes MPI: phylogenetic reconstruction with infinite mixtures of profiles in a parallel environment. Syst. Biol. 62, 611–615 (2013).

    CAS  Article  PubMed  Google Scholar 

  56. 56.

    Quang, L. S., Gascuel, O. & Lartillot, N. Empirical profile mixture models for phylogenetic reconstruction. Bioinformatics 24, 2317–2323 (2008).

    CAS  Article  Google Scholar 

  57. 57.

    Schirrmeister, B. E., de Vos, J. M., Antonelli, A. & Bagheri, H. C. Evolution of multicellularity coincided with increased diversification of cyanobacteria and the Great Oxidation Event. Proc. Natl Acad. Sci. USA 110, 1791–1796 (2013).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  58. 58.

    Schirrmeister, B. E., Gugger, M. & Donoghue, P. C. J. Cyanobacteria and the Great Oxidation Event: evidence from genes and fossils. Palaeontology 58, 769–785 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  59. 59.

    Schirrmeister, B. E., Sanchez-Baracaldo, P. & Wacey, D. Cyanobacterial evolution during the Precambrian. Int. J. Astrobiol. 15, 1–18 (2016).

    Article  Google Scholar 

  60. 60.

    Yang, Z. & Rannala, B. Bayesian estimation of species divergence times under a molecular clock using multiple fossil calibrations with soft bounds. Mol. Biol. Evol. 23, 212–226 (2006).

    CAS  Article  PubMed  Google Scholar 

  61. 61.

    Warnock, R. C. M., Yang, Z. & Donoghue, P. C. J. Exploring uncertainty in the calibration of the molecular clock. Biol. Lett. 8, 156–159 (2012).

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

We thank D. Pisani and M. dos Reis for improving the manuscript with their helpful comments; D. Gruen, C. Magnabosco, D. Rothman and B. Schirrmeister for discussions; and G. Shomo for assistance with the Engaging Cluster at the Massachusetts Green High Performance Computing Center. We acknowledge support from the Simons Foundation Collaboration on the Origin of Life (number 339603 to G.P.F. and NSF EAR-1615426 to G.P.F. and J.M.W).

Author information

Affiliations

Authors

Contributions

J.M.W. and G.P.F. designed the research and performed the data analysis. J.M.W. drafted the manuscript with assistance from G.P.F.

Corresponding author

Correspondence to Joanna M. Wolfe.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Publisher’s note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

Supplementary Information

Supplementary Methods, Supplementary Figs. 1–8, Supplementary Tables 1–4, Supplementary References

Life Sciences Reporting Summary

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Wolfe, J.M., Fournier, G.P. Horizontal gene transfer constrains the timing of methanogen evolution. Nat Ecol Evol 2, 897–903 (2018). https://doi.org/10.1038/s41559-018-0513-7

Download citation

Further reading

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing