Biosynthesis of the Unique Wall Teichoic Acid of <named-content content-type="genus-species">Staphylococcus aureus</named-content> Lineage ST395

ABSTRACT The major clonal lineages of the human pathogen Staphylococcus aureus produce cell wall-anchored anionic poly-ribitol-phosphate (RboP) wall teichoic acids (WTA) substituted with d-Alanine and N-acetyl-d-glucosamine. The phylogenetically isolated S. aureus ST395 lineage has recently been fou...

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Autores principales:	Volker Winstel, Patricia Sanchez-Carballo, Otto Holst, Guoqing Xia, Andreas Peschel
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2014
Materias:	Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/ed9d9f9fb13349fdb721ece6c551d151
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spelling	oai:doaj.org-article:ed9d9f9fb13349fdb721ece6c551d1512021-11-15T15:45:12ZBiosynthesis of the Unique Wall Teichoic Acid of <named-content content-type="genus-species">Staphylococcus aureus</named-content> Lineage ST39510.1128/mBio.00869-142150-7511https://doaj.org/article/ed9d9f9fb13349fdb721ece6c551d1512014-05-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00869-14https://doaj.org/toc/2150-7511ABSTRACT The major clonal lineages of the human pathogen Staphylococcus aureus produce cell wall-anchored anionic poly-ribitol-phosphate (RboP) wall teichoic acids (WTA) substituted with d-Alanine and N-acetyl-d-glucosamine. The phylogenetically isolated S. aureus ST395 lineage has recently been found to produce a unique poly-glycerol-phosphate (GroP) WTA glycosylated with N-acetyl-d-galactosamine (GalNAc). ST395 clones bear putative WTA biosynthesis genes on a novel genetic element probably acquired from coagulase-negative staphylococci (CoNS). We elucidated the ST395 WTA biosynthesis pathway and identified three novel WTA biosynthetic genes, including those encoding an α-O-GalNAc transferase TagN, a nucleotide sugar epimerase TagV probably required for generation of the activated sugar donor substrate for TagN, and an unusually short GroP WTA polymerase TagF. By using a panel of mutants derived from ST395, the GalNAc residues carried by GroP WTA were found to be required for infection by the ST395-specific bacteriophage Φ187 and to play a crucial role in horizontal gene transfer of S. aureus pathogenicity islands (SaPIs). Notably, ectopic expression of ST395 WTA biosynthesis genes rendered normal S. aureus susceptible to Φ187 and enabled Φ187-mediated SaPI transfer from ST395 to regular S. aureus. We provide evidence that exchange of WTA genes and their combination in variable, mosaic-like gene clusters have shaped the evolution of staphylococci and their capacities to undergo horizontal gene transfer events. IMPORTANCE The structural highly diverse wall teichoic acids (WTA) are cell wall-anchored glycopolymers produced by most Gram-positive bacteria. While most of the dominant Staphylococcus aureus lineages produce poly-ribitol-phosphate WTA, the recently described ST395 lineage produces a distinct poly-glycerol-phosphate WTA type resembling the WTA backbone of coagulase-negative staphylococci (CoNS). Here, we analyzed the ST395 WTA biosynthesis pathway and found new types of WTA biosynthesis genes along with an evolutionary link between ST395 and CoNS, from which the ST395 WTA genes probably originate. The elucidation of ST395 WTA biosynthesis will help to understand how Gram-positive bacteria produce highly variable WTA types and elucidate functional consequences of WTA variation.Volker WinstelPatricia Sanchez-CarballoOtto HolstGuoqing XiaAndreas PeschelAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 5, Iss 2 (2014)
institution	DOAJ
collection	DOAJ
language	EN
topic	Microbiology QR1-502
spellingShingle	Microbiology QR1-502 Volker Winstel Patricia Sanchez-Carballo Otto Holst Guoqing Xia Andreas Peschel Biosynthesis of the Unique Wall Teichoic Acid of <named-content content-type="genus-species">Staphylococcus aureus</named-content> Lineage ST395
description	ABSTRACT The major clonal lineages of the human pathogen Staphylococcus aureus produce cell wall-anchored anionic poly-ribitol-phosphate (RboP) wall teichoic acids (WTA) substituted with d-Alanine and N-acetyl-d-glucosamine. The phylogenetically isolated S. aureus ST395 lineage has recently been found to produce a unique poly-glycerol-phosphate (GroP) WTA glycosylated with N-acetyl-d-galactosamine (GalNAc). ST395 clones bear putative WTA biosynthesis genes on a novel genetic element probably acquired from coagulase-negative staphylococci (CoNS). We elucidated the ST395 WTA biosynthesis pathway and identified three novel WTA biosynthetic genes, including those encoding an α-O-GalNAc transferase TagN, a nucleotide sugar epimerase TagV probably required for generation of the activated sugar donor substrate for TagN, and an unusually short GroP WTA polymerase TagF. By using a panel of mutants derived from ST395, the GalNAc residues carried by GroP WTA were found to be required for infection by the ST395-specific bacteriophage Φ187 and to play a crucial role in horizontal gene transfer of S. aureus pathogenicity islands (SaPIs). Notably, ectopic expression of ST395 WTA biosynthesis genes rendered normal S. aureus susceptible to Φ187 and enabled Φ187-mediated SaPI transfer from ST395 to regular S. aureus. We provide evidence that exchange of WTA genes and their combination in variable, mosaic-like gene clusters have shaped the evolution of staphylococci and their capacities to undergo horizontal gene transfer events. IMPORTANCE The structural highly diverse wall teichoic acids (WTA) are cell wall-anchored glycopolymers produced by most Gram-positive bacteria. While most of the dominant Staphylococcus aureus lineages produce poly-ribitol-phosphate WTA, the recently described ST395 lineage produces a distinct poly-glycerol-phosphate WTA type resembling the WTA backbone of coagulase-negative staphylococci (CoNS). Here, we analyzed the ST395 WTA biosynthesis pathway and found new types of WTA biosynthesis genes along with an evolutionary link between ST395 and CoNS, from which the ST395 WTA genes probably originate. The elucidation of ST395 WTA biosynthesis will help to understand how Gram-positive bacteria produce highly variable WTA types and elucidate functional consequences of WTA variation.
format	article
author	Volker Winstel Patricia Sanchez-Carballo Otto Holst Guoqing Xia Andreas Peschel
author_facet	Volker Winstel Patricia Sanchez-Carballo Otto Holst Guoqing Xia Andreas Peschel
author_sort	Volker Winstel
title	Biosynthesis of the Unique Wall Teichoic Acid of <named-content content-type="genus-species">Staphylococcus aureus</named-content> Lineage ST395
title_short	Biosynthesis of the Unique Wall Teichoic Acid of <named-content content-type="genus-species">Staphylococcus aureus</named-content> Lineage ST395
title_full	Biosynthesis of the Unique Wall Teichoic Acid of <named-content content-type="genus-species">Staphylococcus aureus</named-content> Lineage ST395
title_fullStr	Biosynthesis of the Unique Wall Teichoic Acid of <named-content content-type="genus-species">Staphylococcus aureus</named-content> Lineage ST395
title_full_unstemmed	Biosynthesis of the Unique Wall Teichoic Acid of <named-content content-type="genus-species">Staphylococcus aureus</named-content> Lineage ST395
title_sort	biosynthesis of the unique wall teichoic acid of <named-content content-type="genus-species">staphylococcus aureus</named-content> lineage st395
publisher	American Society for Microbiology
publishDate	2014
url	https://doaj.org/article/ed9d9f9fb13349fdb721ece6c551d151
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Biosynthesis of the Unique Wall Teichoic Acid of <named-content content-type="genus-species">Staphylococcus aureus</named-content> Lineage ST395

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