Abstract
Sequenced archaeal genomes are mostly smaller and more streamlined than typical bacterial genomes; however, members of the Methanosarcina genus within the Euryarchaeaota are a significant exception, with M. acetivorans being the largest archaeal genome (5.8 Mbp) sequenced thus far. This finding is partially explained by extensive gene duplication within Methanosarcina spp. Significantly, the evolutionary pressures leading to gene duplication and subsequent genome expansion have not been well investigated, especially with respect to biological methane production (methanogenesis), which is the key biological trait of these environmentally important organisms. In this study, we address this question by specifically probing the functional evolution of two methylamine-specific methyltransferase paralogs in members of the Methanosarcina genus. Using the genetically tractable strain, M. acetivorans, we first show that the two paralogs have distinct cellular functions: one being required for methanogenesis from methylamine, the other for use of methylamine as a nitrogen source. Subsequently, through comparative sequence analyses, we show that functional divergence of paralogs is primarily mediated by divergent evolution of the 5′ regulatory region, despite frequent gene conversion within the coding sequence. This unique evolutionary paradigm for functional divergence of genes post-duplication underscores a divergent role for an enzyme singularly associated with methanogenic metabolism in other aspects of cell physiology.
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Acknowledgements
The authors acknowledge the Division of Chemical Sciences, Geosciences, and Biosciences, Office of Basic Energy Sciences of the U.S. Department of Energy through Grant DE-FG02-02ER15296 (to WWM), the Carl R. Woese Institute for Genomic Biology postdoctoral fellowship (to DDN), and the Simons Foundation Life Sciences Research Foundation postdoctoral fellowship (to DDN). The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
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DDN and WWM contributed to conceptualization, data curation, formal analysis, supervision, funding acquisition, project administration, methodology, and writing. DDN performed all the experiments outlined in this work.
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Nayak, D.D., Metcalf, W.W. Methylamine-specific methyltransferase paralogs in Methanosarcina are functionally distinct despite frequent gene conversion. ISME J 13, 2173–2182 (2019). https://doi.org/10.1038/s41396-019-0428-6
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DOI: https://doi.org/10.1038/s41396-019-0428-6
