Steady at the wheel: conservative sex and the benefits of bacterial transformation

Author:

Ambur Ole Herman1,Engelstädter Jan2,Johnsen Pål J.3,Miller Eric L.4ORCID,Rozen Daniel E.5ORCID

Affiliation:

1. Department of Life Sciences and Health, Oslo and Akershus University College of Applied Sciences, 1478 Oslo, Norway

2. School of Biological Sciences, The University of Queensland, Brisbane, QLD 4072, Australia

3. Faculty of Health Sciences, Department of Pharmacy, UiT-The Arctic University of Norway, 9037 Tromsø, Norway

4. Faculty of Life Sciences, University of Manchester, Manchester M13 9PL, UK

5. Institute of Biology, Leiden University, 2333 BE Leiden, The Netherlands

Abstract

Many bacteria are highly sexual, but the reasons for their promiscuity remain obscure. Did bacterial sex evolve to maximize diversity and facilitate adaptation in a changing world, or does it instead help to retain the bacterial functions that work right now? In other words, is bacterial sex innovative or conservative? Our aim in this review is to integrate experimental, bioinformatic and theoretical studies to critically evaluate these alternatives, with a main focus on natural genetic transformation, the bacterial equivalent of eukaryotic sexual reproduction. First, we provide a general overview of several hypotheses that have been put forward to explain the evolution of transformation. Next, we synthesize a large body of evidence highlighting the numerous passive and active barriers to transformation that have evolved to protect bacteria from foreign DNA, thereby increasing the likelihood that transformation takes place among clonemates. Our critical review of the existing literature provides support for the view that bacterial transformation is maintained as a means of genomic conservation that provides direct benefits to both individual bacterial cells and to transformable bacterial populations. We examine the generality of this view across bacteria and contrast this explanation with the different evolutionary roles proposed to maintain sex in eukaryotes.  This article is part of the themed issue ‘Weird sex: the underappreciated diversity of sexual reproduction’.

Funder

Australian Research Council

Norwegian Research Council

Biotechnology and Biological Sciences Research Council

NWO

Publisher

The Royal Society

Subject

General Agricultural and Biological Sciences,General Biochemistry, Genetics and Molecular Biology

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