The bioenergetic costs of a gene
Michael Lynch1 and Georgi K. Marinov
Department of Biology, Indiana University, Bloomington, IN 47401
Edited by W. Ford Doolittle, Dalhousie University, Halifax, Canada, and approved October 6, 2015 (received for review July 29, 2015)
Significance
A long-standing mystery in evolutionary genomics concerns the lineage-specific expansions of genome size in eukaryotes relative to prokaryotes. One argument is that the cellular complexity and elevated gene numbers in eukaryotes were impossible without a mitochondrion. However, the energetic burden of a gene is typically no greater, and generally becomes progressively smaller, in larger cells in both bacteria and eukaryotes, and this is true for costs measured at the DNA, RNA, and protein levels. These results eliminate the need to invoke an energetics barrier to genome complexity.
Abstract
An enduring mystery of evolutionary genomics concerns the mechanisms responsible for lineage-specific expansions of genome size in eukaryotes, especially in multicellular species. One idea is that all excess DNA is mutationally hazardous, but weakly enough so that genome-size expansion passively emerges in species experiencing relatively low efficiency of selection owing to small effective population sizes. Another idea is that substantial gene additions were impossible without the energetic boost provided by the colonizing mitochondrion in the eukaryotic lineage. Contrary to this latter view, analysis of cellular energetics and genomics data from a wide variety of species indicates that, relative to the lifetime ATP requirements of a cell, the costs of a gene at the DNA, RNA, and protein levels decline with cell volume in both bacteria and eukaryotes. Moreover, these costs are usually sufficiently large to be perceived by natural selection in bacterial populations, but not in eukaryotes experiencing high levels of random genetic drift. Thus, for scaling reasons that are not yet understood, by virtue of their large size alone, eukaryotic cells are subject to a broader set of opportunities for the colonization of novel genes manifesting weakly advantageous or even transiently disadvantageous phenotypic effects. These results indicate that the origin of the mitochondrion was not a prerequisite for genome-size expansion.
gene cost transcription translation cellular bioenergetics evolutionary genomics
Footnotes
1 To whom correspondence should be addressed. Email: milynch{at}indiana.edu.
Author contributions: M.L. and G.K.M. designed research, performed research, analyzed data, and wrote the paper.
The authors declare no conflict of interest.
This article is a PNAS Direct Submission.
This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1514974112/-/DCSupplemental.
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