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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.

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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.

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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).

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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.

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Correspondence to Joanna M. Wolfe.

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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

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