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Bacteria from natural populations transfer plasmids mostly towards their kin.

ABSTRACT: Plasmids play a key role in microbial ecology and evolution, yet the determinants of plasmid transfer rates are poorly understood. Particularly, interactions between donor hosts and potential recipients are understudied. Here, we investigate the importance of genetic similarity between naturally co-occurring Escherichia coli isolates in plasmid transfer. We uncover extensive variability, spanning over five orders of magnitude, in the ability of isolates to donate and receive two different plasmids, R1 and RP4. Overall, transfer is strongly biased towards clone-mates, but not correlated to genetic distance when donors and recipients are not clone-mates. Transfer is limited by the presence of a functional restriction-modification system in recipients, suggesting sharing of strain-specific defence systems contributes to bias towards kin. Such restriction of transfer to kin sets the stage for longer-term coevolutionary interactions leading to mutualism between plasmids and bacterial hosts in natural communities.

SUBMITTER: Dimitriu T

PROVIDER: S-EPMC6599995 | biostudies-literature | 2019 Jun

REPOSITORIES: biostudies-literature

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Bacteria from natural populations transfer plasmids mostly towards their kin.

Dimitriu Tatiana T Marchant Lauren L Buckling Angus A Raymond Ben B

Proceedings. Biological sciences 20190626 1905

Plasmids play a key role in microbial ecology and evolution, yet the determinants of plasmid transfer rates are poorly understood. Particularly, interactions between donor hosts and potential recipients are understudied. Here, we investigate the importance of genetic similarity between naturally co-occurring Escherichia coli isolates in plasmid transfer. We uncover extensive variability, spanning over five orders of magnitude, in the ability of isolates to donate and receive two different plasmi ...[more]

PMID: 31238848

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Project description:Methylation of DNA at the C-5 position of cytosine occurs in diverse organisms. This modification can increase the rate of C→T transitions at the methylated position. In Escherichia coli and related enteric bacteria, the inner C residues of the sequence CCWGG (W is A or T) are methylated by the Dcm enzyme. These sites are hot spots of mutation during rapid growth in the laboratory but not in nondividing cells, in which repair by the Vsr protein is effective. It has been suggested that hypermutation at these sites is a laboratory artifact and does not occur in nature. Many other methyltransferases, with a variety of specificities, can be found in bacteria, usually associated with restriction enzymes and confined to a subset of the population. Their methylation targets are also possible sites of hypermutation. Here, I show using whole-genome sequence data for thousands of isolates that there is indeed considerable hypermutation at Dcm sites in natural populations: their transition rate is approximately eight times the average. I also demonstrate hypermutability of targets of restriction-associated methyltransferases in several distantly related bacteria: methylation increases the transition rate by a factor ranging from 12 to 58. In addition, I demonstrate how patterns of hypermutability inferred from massive sequence data can be used to determine previously unknown methylation patterns and methyltransferase specificities.IMPORTANCE A common type of DNA modification, addition of a methyl group to cytosine (C) at carbon atom C-5, can greatly increase the rate of mutation of the C to a T. In mammals, methylation of CG sequences increases the rate of CG→TG mutations. It is unknown whether cytosine C-5 methylation increases the mutation rate in bacteria under natural conditions. I show that sites methylated by the Dcm enzyme exhibit an 8-fold increase in mutation rate in natural bacterial populations. I also show that modifications at other sites in various bacteria also increase the mutation rate, in some cases by a factor of forty or more. Finally, I demonstrate how this phenomenon can be used to infer sequence specificities of methylation enzymes.

Dataset Information

Bacteria from natural populations transfer plasmids mostly towards their kin.

Publications

Bacteria from natural populations transfer plasmids mostly towards their kin.

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