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Complete genome sequencing of three human clinical isolates of Staphylococcus caprae reveals virulence factors similar to those of S. epidermidis and S. capitis

BACKGROUND: Staphylococcus caprae is an animal-associated bacterium regarded as part of goats’ microflora. Recently, S. caprae has been reported to cause human nosocomial infections such as bacteremia and bone and joint infections. However, the mechanisms responsible for the development of nosocomia...

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Autores principales: Watanabe, Shinya, Aiba, Yoshifumi, Tan, Xin-Ee, Li, Feng-Yu, Boonsiri, Tanit, Thitiananpakorn, Kanate, Cui, Bintao, Sato’o, Yusuke, Kiga, Kotaro, Sasahara, Teppei, Cui, Longzhu
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6225691/
https://www.ncbi.nlm.nih.gov/pubmed/30409159
http://dx.doi.org/10.1186/s12864-018-5185-9
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author Watanabe, Shinya
Aiba, Yoshifumi
Tan, Xin-Ee
Li, Feng-Yu
Boonsiri, Tanit
Thitiananpakorn, Kanate
Cui, Bintao
Sato’o, Yusuke
Kiga, Kotaro
Sasahara, Teppei
Cui, Longzhu
author_facet Watanabe, Shinya
Aiba, Yoshifumi
Tan, Xin-Ee
Li, Feng-Yu
Boonsiri, Tanit
Thitiananpakorn, Kanate
Cui, Bintao
Sato’o, Yusuke
Kiga, Kotaro
Sasahara, Teppei
Cui, Longzhu
author_sort Watanabe, Shinya
collection PubMed
description BACKGROUND: Staphylococcus caprae is an animal-associated bacterium regarded as part of goats’ microflora. Recently, S. caprae has been reported to cause human nosocomial infections such as bacteremia and bone and joint infections. However, the mechanisms responsible for the development of nosocomial infections remain largely unknown. Moreover, the complete genome sequence of S. caprae has not been determined. RESULTS: We determined the complete genome sequences of three methicillin-resistant S. caprae strains isolated from humans and compared these sequences with the genomes of S. epidermidis and S. capitis, both of which are closely related to S. caprae and are inhabitants of human skin capable of causing opportunistic infections. The genomes showed that S. caprae JMUB145, JMUB590, and JMUB898 strains contained circular chromosomes of 2,618,380, 2,629,173, and 2,598,513 bp, respectively. JMUB145 carried type V SCCmec, while JMUB590 and JMUB898 had type IVa SCCmec. A genome-wide phylogenetic SNP tree constructed using 83 complete genome sequences of 24 Staphylococcus species and 2 S. caprae draft genome sequences confirmed that S. caprae is most closely related to S. epidermidis and S. capitis. Comparative complete genome analysis of eight S. epidermidis, three S. capitis and three S. caprae strains revealed that they shared similar virulence factors represented by biofilm formation genes. These factors include wall teichoic acid synthesis genes, poly-gamma-DL-glutamic acid capsule synthesis genes, and other genes encoding nonproteinaceous adhesins. The 17 proteinases/adhesins and extracellular proteins known to be associated with biofilm formation in S. epidermidis were also conserved in these three species, and their biofilm formation could be detected in vitro. Moreover, two virulence-associated gene clusters, the type VII secretion system and capsular polysaccharide biosynthesis gene clusters, identified in S. aureus were present in S. caprae but not in S. epidermidis and S. capitis genomes. CONCLUSION: The complete genome sequences of three methicillin-resistant S. caprae isolates from humans were determined for the first time. Comparative genome analysis revealed that S. caprae is closely related to S. epidermidis and S. capitis at the species level, especially in the ability to form biofilms, which may lead to increased virulence during the development of S. caprae infections. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12864-018-5185-9) contains supplementary material, which is available to authorized users.
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spelling pubmed-62256912018-11-19 Complete genome sequencing of three human clinical isolates of Staphylococcus caprae reveals virulence factors similar to those of S. epidermidis and S. capitis Watanabe, Shinya Aiba, Yoshifumi Tan, Xin-Ee Li, Feng-Yu Boonsiri, Tanit Thitiananpakorn, Kanate Cui, Bintao Sato’o, Yusuke Kiga, Kotaro Sasahara, Teppei Cui, Longzhu BMC Genomics Research Article BACKGROUND: Staphylococcus caprae is an animal-associated bacterium regarded as part of goats’ microflora. Recently, S. caprae has been reported to cause human nosocomial infections such as bacteremia and bone and joint infections. However, the mechanisms responsible for the development of nosocomial infections remain largely unknown. Moreover, the complete genome sequence of S. caprae has not been determined. RESULTS: We determined the complete genome sequences of three methicillin-resistant S. caprae strains isolated from humans and compared these sequences with the genomes of S. epidermidis and S. capitis, both of which are closely related to S. caprae and are inhabitants of human skin capable of causing opportunistic infections. The genomes showed that S. caprae JMUB145, JMUB590, and JMUB898 strains contained circular chromosomes of 2,618,380, 2,629,173, and 2,598,513 bp, respectively. JMUB145 carried type V SCCmec, while JMUB590 and JMUB898 had type IVa SCCmec. A genome-wide phylogenetic SNP tree constructed using 83 complete genome sequences of 24 Staphylococcus species and 2 S. caprae draft genome sequences confirmed that S. caprae is most closely related to S. epidermidis and S. capitis. Comparative complete genome analysis of eight S. epidermidis, three S. capitis and three S. caprae strains revealed that they shared similar virulence factors represented by biofilm formation genes. These factors include wall teichoic acid synthesis genes, poly-gamma-DL-glutamic acid capsule synthesis genes, and other genes encoding nonproteinaceous adhesins. The 17 proteinases/adhesins and extracellular proteins known to be associated with biofilm formation in S. epidermidis were also conserved in these three species, and their biofilm formation could be detected in vitro. Moreover, two virulence-associated gene clusters, the type VII secretion system and capsular polysaccharide biosynthesis gene clusters, identified in S. aureus were present in S. caprae but not in S. epidermidis and S. capitis genomes. CONCLUSION: The complete genome sequences of three methicillin-resistant S. caprae isolates from humans were determined for the first time. Comparative genome analysis revealed that S. caprae is closely related to S. epidermidis and S. capitis at the species level, especially in the ability to form biofilms, which may lead to increased virulence during the development of S. caprae infections. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12864-018-5185-9) contains supplementary material, which is available to authorized users. BioMed Central 2018-11-08 /pmc/articles/PMC6225691/ /pubmed/30409159 http://dx.doi.org/10.1186/s12864-018-5185-9 Text en © The Author(s). 2018 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research Article
Watanabe, Shinya
Aiba, Yoshifumi
Tan, Xin-Ee
Li, Feng-Yu
Boonsiri, Tanit
Thitiananpakorn, Kanate
Cui, Bintao
Sato’o, Yusuke
Kiga, Kotaro
Sasahara, Teppei
Cui, Longzhu
Complete genome sequencing of three human clinical isolates of Staphylococcus caprae reveals virulence factors similar to those of S. epidermidis and S. capitis
title Complete genome sequencing of three human clinical isolates of Staphylococcus caprae reveals virulence factors similar to those of S. epidermidis and S. capitis
title_full Complete genome sequencing of three human clinical isolates of Staphylococcus caprae reveals virulence factors similar to those of S. epidermidis and S. capitis
title_fullStr Complete genome sequencing of three human clinical isolates of Staphylococcus caprae reveals virulence factors similar to those of S. epidermidis and S. capitis
title_full_unstemmed Complete genome sequencing of three human clinical isolates of Staphylococcus caprae reveals virulence factors similar to those of S. epidermidis and S. capitis
title_short Complete genome sequencing of three human clinical isolates of Staphylococcus caprae reveals virulence factors similar to those of S. epidermidis and S. capitis
title_sort complete genome sequencing of three human clinical isolates of staphylococcus caprae reveals virulence factors similar to those of s. epidermidis and s. capitis
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6225691/
https://www.ncbi.nlm.nih.gov/pubmed/30409159
http://dx.doi.org/10.1186/s12864-018-5185-9
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