Bacterial chromosomal mobility via lateral transduction exceeds that of classical mobile genetic elements

Suzanne Humphrey; Alfred Fillol-Salom; Nuria Quiles-Puchalt; Rodrigo Ibarra-Chávez; Andreas F. Haag; John Chen; José R. Penadés

doi:10.1038/s41467-021-26004-5

Bacterial chromosomal mobility via lateral transduction exceeds that of classical mobile genetic elements

Suzanne Humphrey, Alfred Fillol-Salom, Nuria Quiles-Puchalt, Rodrigo Ibarra-Chávez, Andreas F. Haag, John Chen, José R. Penadés^*

^*Corresponding author for this work

School of Medicine

Research output: Contribution to journal › Article › peer-review

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Abstract

It is commonly assumed that the horizontal transfer of most bacterial chromosomal genes is limited, in contrast to the frequent transfer observed for typical mobile genetic elements. However, this view has been recently challenged by the discovery of lateral transduction in Staphylococcus aureus, where temperate phages can drive the transfer of large chromosomal regions at extremely high frequencies. Here, we analyse previously published as well as new datasets to compare horizontal gene transfer rates mediated by different mechanisms in S. aureus and Salmonella enterica. We find that the horizontal transfer of core chromosomal genes via lateral transduction can be more efficient than the transfer of classical mobile genetic elements via conjugation or generalized transduction. These results raise questions about our definition of mobile genetic elements, and the potential roles played by lateral transduction in bacterial evolution.

Original language	English
Article number	6509
Number of pages	13
Journal	Nature Communications
Volume	12
DOIs	https://doi.org/10.1038/s41467-021-26004-5
Publication status	Published - 8 Nov 2021

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title = "Bacterial chromosomal mobility via lateral transduction exceeds that of classical mobile genetic elements",

abstract = "It is commonly assumed that the horizontal transfer of most bacterial chromosomal genes is limited, in contrast to the frequent transfer observed for typical mobile genetic elements. However, this view has been recently challenged by the discovery of lateral transduction in Staphylococcus aureus, where temperate phages can drive the transfer of large chromosomal regions at extremely high frequencies. Here, we analyse previously published as well as new datasets to compare horizontal gene transfer rates mediated by different mechanisms in S. aureus and Salmonella enterica. We find that the horizontal transfer of core chromosomal genes via lateral transduction can be more efficient than the transfer of classical mobile genetic elements via conjugation or generalized transduction. These results raise questions about our definition of mobile genetic elements, and the potential roles played by lateral transduction in bacterial evolution.",

author = "Suzanne Humphrey and Alfred Fillol-Salom and Nuria Quiles-Puchalt and Rodrigo Ibarra-Ch{\'a}vez and Haag, {Andreas F.} and John Chen and Penad{\'e}s, {Jos{\'e} R.}",

note = "Funding: This work was supported by grants MR/M003876/1, MR/V000772/1 and MR/S00940X/1 from the Medical Research Council (UK), BB/N002873/1, BB/V002376/1 and BB/S003835/1 from the Biotechnology and Biological Sciences Research Council (BBSRC, UK), ERC-ADG-2014 Proposal n° 670932 Dut-signal (from EU), to J.R.P; and Wellcome Trust 201531/Z/16/Z to J.R.P. ",

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AU - Humphrey, Suzanne

AU - Fillol-Salom, Alfred

AU - Quiles-Puchalt, Nuria

AU - Ibarra-Chávez, Rodrigo

AU - Haag, Andreas F.

AU - Chen, John

AU - Penadés, José R.

N1 - Funding: This work was supported by grants MR/M003876/1, MR/V000772/1 and MR/S00940X/1 from the Medical Research Council (UK), BB/N002873/1, BB/V002376/1 and BB/S003835/1 from the Biotechnology and Biological Sciences Research Council (BBSRC, UK), ERC-ADG-2014 Proposal n° 670932 Dut-signal (from EU), to J.R.P; and Wellcome Trust 201531/Z/16/Z to J.R.P.

PY - 2021/11/8

Y1 - 2021/11/8

N2 - It is commonly assumed that the horizontal transfer of most bacterial chromosomal genes is limited, in contrast to the frequent transfer observed for typical mobile genetic elements. However, this view has been recently challenged by the discovery of lateral transduction in Staphylococcus aureus, where temperate phages can drive the transfer of large chromosomal regions at extremely high frequencies. Here, we analyse previously published as well as new datasets to compare horizontal gene transfer rates mediated by different mechanisms in S. aureus and Salmonella enterica. We find that the horizontal transfer of core chromosomal genes via lateral transduction can be more efficient than the transfer of classical mobile genetic elements via conjugation or generalized transduction. These results raise questions about our definition of mobile genetic elements, and the potential roles played by lateral transduction in bacterial evolution.

AB - It is commonly assumed that the horizontal transfer of most bacterial chromosomal genes is limited, in contrast to the frequent transfer observed for typical mobile genetic elements. However, this view has been recently challenged by the discovery of lateral transduction in Staphylococcus aureus, where temperate phages can drive the transfer of large chromosomal regions at extremely high frequencies. Here, we analyse previously published as well as new datasets to compare horizontal gene transfer rates mediated by different mechanisms in S. aureus and Salmonella enterica. We find that the horizontal transfer of core chromosomal genes via lateral transduction can be more efficient than the transfer of classical mobile genetic elements via conjugation or generalized transduction. These results raise questions about our definition of mobile genetic elements, and the potential roles played by lateral transduction in bacterial evolution.

U2 - 10.1038/s41467-021-26004-5

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JO - Nature Communications

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Bacterial chromosomal mobility via lateral transduction exceeds that of classical mobile genetic elements

Abstract

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