Conservative sex and the benefits of transformation in Streptococcus pneumoniae.

Conservative sex and the benefits of transformation in Streptococcus pneumoniae.
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DOI:
10.1371/journal.ppat.1003758
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发表时间:
2013
期刊:
影响因子:
6.7
通讯作者:
Rozen DE
Rozen DE
中科院分区:
医学1区
文献类型:
--
作者:
Engelmoer DJ;Donaldson I;Rozen DE

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Natural transformation has significant effects on bacterial genome evolution, but the evolutionary factors maintaining this mode of bacterial sex remain uncertain. Transformation is hypothesized to have both positive and negative evolutionary effects on bacteria. It can facilitate adaptation by combining beneficial mutations into a single individual, or reduce the mutational load by exposing deleterious alleles to natural selection. Alternatively, it may expose transformed cells to damaged or otherwise mutated environmental DNA and is energetically expensive. Here, we examine the long-term effects of transformation in the naturally competent species Streptococcus pneumoniae by evolving populations of wild-type and competence-deficient strains in chemostats for 1000 generations. Half of these populations were exposed to periodic mild stress to examine context-dependent benefits of transformation. We find that competence reduces fitness gain under benign conditions; however, these costs are reduced in the presence of periodic stress. Using whole genome re-sequencing, we show that competent populations fix fewer new mutations and that competence prevents the emergence of mutators. Our results show that during evolution in benign conditions competence helps maintain genome stability but is evolutionary costly; however, during periods of stress this same conservativism enables cells to retain fitness in the face of new mutations, showing for the first time that the benefits of transformation are context dependent. Transformation of environmental DNA can provide bacteria with a means to adapt quickly to a changing environment. While this can benefit microbes by facilitating the spread of antibiotic resistance, it can also be harmful if it causes the loss of beneficial alleles from a population. Therefore, it is unclear what evolutionary factors enable transformation to persist in bacterial populations. We used the naturally transformable opportunistic pathogen Streptococcus pneumoniae to investigate the long-term benefits of transformation. We compared the fitness of laboratory populations of S. pneumoniae after 1000 generations of evolution. Half of these populations were naturally transformable (competent) while the other half was deficient for this function. At the same time, half of the evolving populations were periodically exposed to short periods of mild stress. We find that competence reduces the average fitness gain of evolving populations, but this cost is mitigated in populations facing mild stress. Using whole genome sequencing, we discovered that functional competence reduces the total number of fixed mutations and prevents hyper-mutable cells from increasing in frequency. Our results suggest that competence in S. pneumoniae is a conservative process acting to preserve alleles, rather than an innovative one that persists because it recombines beneficial mutations.
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