Abiotic Gene Transfer: Rare or Rampant?

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, an...

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Main Authors: Kotnik, Tadej, Weaver, James C
Other Authors: Institute for Medical Engineering and Science
Format: Article
Language:English
Published: Springer US 2016
Online Access:http://hdl.handle.net/1721.1/105121
https://orcid.org/0000-0002-9016-5962
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author Kotnik, Tadej
Weaver, James C
author2 Institute for Medical Engineering and Science
author_facet Institute for Medical Engineering and Science
Kotnik, Tadej
Weaver, James C
author_sort Kotnik, Tadej
collection MIT
description 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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spelling mit-1721.1/1051212022-10-02T02:17:23Z Abiotic Gene Transfer: Rare or Rampant? Kotnik, Tadej Weaver, James C Institute for Medical Engineering and Science Harvard University--MIT Division of Health Sciences and Technology Weaver, James C 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. National Institutes of Health (U.S.) (Grant 5RO1GM63857) United States. Air Force Office of Scientific Research. Multidisciplinary University Research Initiative 2016-10-27T21:54:58Z 2017-03-01T16:14:49Z 2016-04 2016-02 2016-08-18T15:41:03Z Article http://purl.org/eprint/type/JournalArticle 0022-2631 1432-1424 http://hdl.handle.net/1721.1/105121 Kotnik, Tadej, and James C. Weaver. “Abiotic Gene Transfer: Rare or Rampant?” The Journal of Membrane Biology 249.5 (2016): 623–631. https://orcid.org/0000-0002-9016-5962 en http://dx.doi.org/10.1007/s00232-016-9897-y The Journal of Membrane Biology Article is made available in accordance with the publisher's policy and may be subject to US copyright law. Please refer to the publisher's site for terms of use. Springer Science+Business Media New York application/pdf Springer US Springer US
spellingShingle Kotnik, Tadej
Weaver, James C
Abiotic Gene Transfer: Rare or Rampant?
title Abiotic Gene Transfer: Rare or Rampant?
title_full Abiotic Gene Transfer: Rare or Rampant?
title_fullStr Abiotic Gene Transfer: Rare or Rampant?
title_full_unstemmed Abiotic Gene Transfer: Rare or Rampant?
title_short Abiotic Gene Transfer: Rare or Rampant?
title_sort abiotic gene transfer rare or rampant
url http://hdl.handle.net/1721.1/105121
https://orcid.org/0000-0002-9016-5962
work_keys_str_mv AT kotniktadej abioticgenetransferrareorrampant
AT weaverjamesc abioticgenetransferrareorrampant