Wall teichoic acid structure governs horizontal gene transfer between major bacterial pathogens

Volker Winstel; Chunguang Liang; Patricia Sanchez-Carballo; Matthias Steglich; Marta Munar; Barbara M. Broker; Jose R. Penadés; Ulrich Nübel; Otto Holst; Thomas Dandekar; Andreas Peschel; Guoqing Xia

doi:10.1038/ncomms3345

Wall teichoic acid structure governs horizontal gene transfer between major bacterial pathogens

Volker Winstel, Chunguang Liang, Patricia Sanchez-Carballo, Matthias Steglich, Marta Munar, Barbara M. Broker, Jose R. Penadés, Ulrich Nübel, Otto Holst, Thomas Dandekar, Andreas Peschel, Guoqing Xia

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Abstract

Mobile genetic elements (MGEs) encoding virulence and resistance genes are widespread in bacterial pathogens, but it has remained unclear how they occasionally jump to new host species. Staphylococcus aureus clones exchange MGEs such as S. aureus pathogenicity islands (SaPIs) with high frequency via helper phages. Here we report that the S. aureus ST395 lineage is refractory to horizontal gene transfer (HGT) with typical S. aureus but exchanges SaPIs with other species and genera including Staphylococcus epidermidis and Listeria monocytogenes. ST395 produces an unusual wall teichoic acid (WTA) resembling that of its HGT partner species. Notably, distantly related bacterial species and genera undergo efficient HGT with typical S. aureus upon ectopic expression of S. aureus WTA. Combined with genomic analyses, these results indicate that a 'glycocode' of WTA structures and WTA-binding helper phages permits HGT even across long phylogenetic distances thereby shaping the evolution of Gram-positive pathogens. © 2013 Macmillan Publishers Limited.

Original language	English
Article number	2345
Journal	Nature Communications
Volume	4
DOIs	https://doi.org/10.1038/ncomms3345
Publication status	Published - 2013

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title = "Wall teichoic acid structure governs horizontal gene transfer between major bacterial pathogens",

abstract = "Mobile genetic elements (MGEs) encoding virulence and resistance genes are widespread in bacterial pathogens, but it has remained unclear how they occasionally jump to new host species. Staphylococcus aureus clones exchange MGEs such as S. aureus pathogenicity islands (SaPIs) with high frequency via helper phages. Here we report that the S. aureus ST395 lineage is refractory to horizontal gene transfer (HGT) with typical S. aureus but exchanges SaPIs with other species and genera including Staphylococcus epidermidis and Listeria monocytogenes. ST395 produces an unusual wall teichoic acid (WTA) resembling that of its HGT partner species. Notably, distantly related bacterial species and genera undergo efficient HGT with typical S. aureus upon ectopic expression of S. aureus WTA. Combined with genomic analyses, these results indicate that a 'glycocode' of WTA structures and WTA-binding helper phages permits HGT even across long phylogenetic distances thereby shaping the evolution of Gram-positive pathogens. {\textcopyright} 2013 Macmillan Publishers Limited.",

author = "Volker Winstel and Chunguang Liang and Patricia Sanchez-Carballo and Matthias Steglich and Marta Munar and Broker, {Barbara M.} and Penad{\'e}s, {Jose R.} and Ulrich N{\"u}bel and Otto Holst and Thomas Dandekar and Andreas Peschel and Guoqing Xia",

year = "2013",

doi = "10.1038/ncomms3345",

language = "English",

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journal = "Nature Communications",

issn = "2041-1723",

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TY - JOUR

T1 - Wall teichoic acid structure governs horizontal gene transfer between major bacterial pathogens

AU - Winstel, Volker

AU - Liang, Chunguang

AU - Sanchez-Carballo, Patricia

AU - Steglich, Matthias

AU - Munar, Marta

AU - Broker, Barbara M.

AU - Penadés, Jose R.

AU - Nübel, Ulrich

AU - Holst, Otto

AU - Dandekar, Thomas

AU - Peschel, Andreas

AU - Xia, Guoqing

PY - 2013

Y1 - 2013

N2 - Mobile genetic elements (MGEs) encoding virulence and resistance genes are widespread in bacterial pathogens, but it has remained unclear how they occasionally jump to new host species. Staphylococcus aureus clones exchange MGEs such as S. aureus pathogenicity islands (SaPIs) with high frequency via helper phages. Here we report that the S. aureus ST395 lineage is refractory to horizontal gene transfer (HGT) with typical S. aureus but exchanges SaPIs with other species and genera including Staphylococcus epidermidis and Listeria monocytogenes. ST395 produces an unusual wall teichoic acid (WTA) resembling that of its HGT partner species. Notably, distantly related bacterial species and genera undergo efficient HGT with typical S. aureus upon ectopic expression of S. aureus WTA. Combined with genomic analyses, these results indicate that a 'glycocode' of WTA structures and WTA-binding helper phages permits HGT even across long phylogenetic distances thereby shaping the evolution of Gram-positive pathogens. © 2013 Macmillan Publishers Limited.

AB - Mobile genetic elements (MGEs) encoding virulence and resistance genes are widespread in bacterial pathogens, but it has remained unclear how they occasionally jump to new host species. Staphylococcus aureus clones exchange MGEs such as S. aureus pathogenicity islands (SaPIs) with high frequency via helper phages. Here we report that the S. aureus ST395 lineage is refractory to horizontal gene transfer (HGT) with typical S. aureus but exchanges SaPIs with other species and genera including Staphylococcus epidermidis and Listeria monocytogenes. ST395 produces an unusual wall teichoic acid (WTA) resembling that of its HGT partner species. Notably, distantly related bacterial species and genera undergo efficient HGT with typical S. aureus upon ectopic expression of S. aureus WTA. Combined with genomic analyses, these results indicate that a 'glycocode' of WTA structures and WTA-binding helper phages permits HGT even across long phylogenetic distances thereby shaping the evolution of Gram-positive pathogens. © 2013 Macmillan Publishers Limited.

U2 - 10.1038/ncomms3345

DO - 10.1038/ncomms3345

M3 - Article

C2 - 23965785

SN - 2041-1723

VL - 4

JO - Nature Communications

JF - Nature Communications

M1 - 2345

ER -

Wall teichoic acid structure governs horizontal gene transfer between major bacterial pathogens

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