Abstract
Phylogenetic studies reveal that horizontal gene transfer (HGT) plays a prominent role in evolution and genetic variability of life. Five biotic mechanisms of HGT among prokaryotic organisms have been extensively characterized: conjugation, competence, transduction, gene transfer agent particles, and transitory fusion with recombination, but it is not known whether they can account for all natural HGT. It is even less clear how HGT could have occurred before any of these mechanisms had developed. Here, we consider contemporary conditions and experiments on microorganisms to estimate possible roles of abiotic HGT—currently and throughout evolution. Candidate mechanisms include freeze-and-thaw, microbeads-agitation, and electroporation-based transformation, and we posit that these laboratory techniques have analogues in nature acting as mechanisms of abiotic HGT: freeze-and-thaw cycles in polar waters, agitation by sand at foreshores and riverbeds, and lightning-triggered electroporation in near-surface aqueous habitats. We derive conservative order-of-magnitude estimates for rates of microorganisms subjected to freeze-and-thaw cycles, sand agitation, and lightning-triggered electroporation, at 1024, 1019, and 1017 per year, respectively. Considering the yield of viable transformants, which is by far the highest in electroporation, we argue this may still favor lightning-triggered transformation over the other two mechanisms. Electroporation-based gene transfer also appears to be the most general of these abiotic candidates, and perhaps even of all known HGT mechanisms. Future studies should provide improved estimates of gene transfer rates and cell viability, currently and in the past, but to assess the importance of abiotic HGT in nature will likely require substantial progress—also in knowledge of biotic HGT.
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Acknowledgments
The work was supported by the Slovenian Research Agency Grant P2-0249 (TK), the National Institutes of Health Grant 5RO1GM63857 (JCW), and an AFOSR MURI Grant on Nanoelectropulse-Induced Electromechanical Signaling and Control of Biological Systems administered through Old Dominion University (JCW), with part of the research conducted in the LEA EBAM European Associated Laboratory (TK) and within networking efforts of the European Cooperation in Science and Technology COST actions TD1104 and TD1308 (TK). We thank P. Thomas Vernier and E. Philip Krider for valuable discussions and comments.
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Kotnik, T., Weaver, J.C. Abiotic Gene Transfer: Rare or Rampant?. J Membrane Biol 249, 623–631 (2016). https://doi.org/10.1007/s00232-016-9897-y
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DOI: https://doi.org/10.1007/s00232-016-9897-y