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

Shinya Watanabe,Yusuke Sato’O,Yoshifumi Aiba,Feng-Yu Li,Tanit Boonsiri,Longzhu Cui,Bintao Cui,Kotaro Kiga,Teppei Sasahara,Xin-Ee Tan,Kanate Thitiananpakorn

doi:10.1186/s12864-018-5185-9

Abstract

BackgroundStaphylococcus 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.ResultsWe 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.ConclusionThe 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.

Highlights

Staphylococcus caprae is an animal-associated bacterium regarded as part of goats’ microflora
Our analysis revealed that the species-specific genes of S. capitis and S. caprae were typically mapped to the downstream of SCC elements, similar to that of S. aureus, S. epidermidis, and S. haemolyticus genomes [23] (Fig. 6)
The downstream regions of the Staphylococcus Cassette Chromosome mec (SCCmec) elements were divergent among species, we found that the type V SCCmec identified in the S. caprae JMUB145 genome was closely related to those of S. aureus JCSC5952 and S. pseudointermidius 06–3228 (Fig. 2) [20, 21], while type IVa SCCmec of S. caprae JMUB590 and JMUB898 was closely related to that of the S. aureus USA300 TCH1516 strain (Fig. 2) [22]

Summary

Introduction

Staphylococcus caprae is an animal-associated bacterium regarded as part of goats’ microflora. Consistent with traditional culture-based analysis, recent microbiome analysis showed that the skin of healthy humans is predominantly colonized by Propionibacterium, Corynebacterium, and Staphylococcus [3,4,5]. Most of these skin inhabitants, including coagulase-negative staphylococci (CoNS), are considered harmless to healthy humans. Detailed classification of CoNS to species levels has revealed that less frequently isolated CoNS, which are considered less virulent or of animal origin, could cause infections if the patients have underlying conditions such as indwelling foreign bodies and/or immunosuppression [8]

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Results

Conclusion