Differential efficiency in exogenous DNA acquisition among closely related Salmonella strains: implications in bacterial speciation.

Hong-Xia Bao,Randal N Johnston,Xia Deng,Ye Feng,Le Tang,Xu-Yao Wang,Ang Li,Da-Ling Zhu,Shu-Lin Liu,Yang Li,Yong-Guo Li,Gui-Rong Liu,Lu Yu

doi:10.1186/1471-2180-14-157

Abstract

BackgroundAcquisition of exogenous genetic material is a key event in bacterial speciation. It seems reasonable to assume that recombination of the incoming DNA into genome would be more efficient with higher levels of relatedness between the DNA donor and recipient. If so, bacterial speciation would be a smooth process, leading to a continuous spectrum of genomic divergence of bacteria, which, however, is not the case as shown by recent findings. The goal of this study was todetermine if DNA transfer efficiency is correlated with the levels of sequence identity.ResultsTo compare the relative efficiency of exogenous DNA acquisition among closely related bacteria, we carried out phage-mediated transduction and plasmid-mediated transformation in representative Salmonella strains with different levels of relatedness. We found that the efficiency was remarkably variable even among genetically almost identical bacteria. Although there was a general tendency that more closely related DNA donor-recipient pairs had higher transduction efficiency, transformation efficiency exhibited over a thousand times difference among the closely related Salmonella strains.ConclusionDNA acquisition efficiency is greatly variable among bacteria that have as high as over 99% identical genetic background, suggesting that bacterial speciation involves highly complex processes affected not only by whether beneficial exogenous DNA may exist in the environment but also the “readiness” of the bacteria to accept it.

Highlights

Acquisition of exogenous genetic material is a key event in bacterial speciation
We conclude that DNA acquisition efficiency is greatly variable among bacteria that have as high as over 99% identical genetic background, which implies that bacterial speciation involves highly complex processes affected by whether beneficial exogenous DNA may exist in the environment and the “readiness” of the bacteria to accept it
A similar situation was seen with S. enteritidis LK5, whose sequence divergence is only 0.012 from S. typhimurium LT2 but its recombination frequency with LT2 was even lower than S. arizonae SARC5 with LT2, S. arizonaeis a serovar from subgroup IIIa, which is much more divergent than S. enteritidis from S. typhimurium

Summary

Introduction

Acquisition of exogenous genetic material is a key event in bacterial speciation. It seems reasonable to assume that recombination of the incoming DNA into genome would be more efficient with higher levels of relatedness between the DNA donor and recipient. Within a monophyletic Salmonella serotype, individual sub-lineages may have their own unique insertions or combinations of them, as exemplified by the DT104 phage type of S. typhimurium for their possession of three insertions ST104, ST104B and ST64B, a combination not seen in other S. typhimurium sub-lineages [16,21] All these facts suggest that, bacteria have many chances to contact exogenous DNA in the environment and may even possibly have it moved into the cell via mechanisms such as bacteriophage-mediated transduction and plasmid-mediated transformation, the recipient may or may not have it incorporated into the genome regardless of whether or not the recipient might gain better fitness to the environment by having it. In vitro recombination efficiency depends linearly on the levels of the sequence similarity of the DNA strands, whether this linearity exists in the exogenous DNA incorporation process inside a bacterial cell is unknown

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