Lateral gene transfer of streptococcal ICE element RD2 (region of difference 2) encoding secreted proteins

Sitkiewicz, Izabela; Green, Nicole M.; Guo, Nina; Mereghetti, Laurent; Musser, James M.

doi:10.1186/1471-2180-11-65

Cited by 51 publications

(51 citation statements)

References 42 publications

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“…There is strong evidence that RD2 originated in GBS and was acquired by GAS through horizontal gene transfer. It has been proposed that genes carried within RD2 might contribute to both GAS and GBS pathogenicity (28,29). Supporting this, AspA has been shown to facilitate GAS biofilm formation on salivary pellicle (25), respiratory infection, and evasion of phagocytosis (30).…”

mentioning

confidence: 61%

Structural and Functional Analysis of Cell Wall-anchored Polypeptide Adhesin BspA in Streptococcus agalactiae

Rego

Heal

Pidwill

et al. 2016

Journal of Biological Chemistry

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Streptococcus agalactiae (group B Streptococcus, GBS) is the predominant cause of early-onset infectious disease in neonates and is responsible for life-threatening infections in elderly and immunocompromised individuals. Clinical manifestations of GBS infection include sepsis, pneumonia, and meningitis. Here, we describe BspA, a deviant antigen I/II family polypeptide that confers adhesive properties linked to pathogenesis in GBS. Heterologous expression of BspA on the surface of the non-adherent bacterium Lactococcus lactis confers adherence to scavenger receptor gp340, human vaginal epithelium, and to the fungus Candida albicans. Complementary crystallographic and biophysical characterization of BspA reveal a novel ␤-sandwich adhesion domain and unique asparagine-dependent super-helical stalk. Collectively, these findings establish a new bacterial adhesin structure that has in effect been hijacked by a pathogenic Streptococcus species to provide competitive advantage in human mucosal infections. Streptococcus agalactiae (group B Streptococcus (GBS)4 ) is a commensal of the gastrointestinal tract and part of the normal microbiota of the female rectovaginal tract, where it is carried asymptomatically by ϳ10 -40% of women of childbearing age (1). However, as an opportunistic pathogen, GBS is the leading cause of neonatal meningitis and sepsis in the developed world. The predominant route by which GBS is transmitted to infants is from the mother, either during birth or following breach of the placental barrier in utero. Antenatal GBS screening strategies are therefore commonly used to identify colonized women, who then receive antimicrobial prophylaxis. Nevertheless, GBS remains a major cause of morbidity and mortality in infants worldwide (2).Because maternal GBS colonization is the primary risk factor for vertical transmission of neonatal infection (3), there has been considerable focus on the mechanisms underlying GBS colonization of the female genitourinary (GU) tract. A number of putative colonization determinants have been identified, including the following: ␣C protein, mediating entry of GBS into cervical epithelial cells (4); pili, shown to contribute to vaginal attachment (5); and Srr-1, which binds keratin-4 (5) and fibrinogen (6) on the surface of vaginal epithelium. In addition, GBS expresses numerous extracellular matrix-binding proteins, including C5a peptidase (ScpB) and FbsA, which may promote attachment to mucosal tissues of the GU tract (7).Antigen I/II (AgI/II) family polypeptide adhesins are found widely across the Streptococcus genus and have been best characterized for those streptococci indigenous to the oral cavity (8). In silico analyses have recently revealed the presence of genes encoding AgI/II family polypeptides in GBS, which we have designated here group B Streptococcus surface proteins (Bsp). These proteins conform to a conserved primary structure consisting of seven distinct regions (Fig. 1). The N-terminal region comprises a signal (leader) peptide, an N-terminal domain, and an ...

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mentioning

confidence: 61%

Structural and Functional Analysis of Cell Wall-anchored Polypeptide Adhesin BspA in Streptococcus agalactiae

Rego

Heal

Pidwill

et al. 2016

Journal of Biological Chemistry

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“…In addition to CIP, RD2 encodes several proteins with predicted secretion signal sequences, among which the R28 protein that has been implicated in host-pathogen interactions (39). Interestingly, in GAS this region is present in all serotype M28 strains and in strains of other serotypes associated with maternal-fetal urogenital infections (40,41). In the case of GBS, analysis of the 373 genomes present in the NCBI database revealed 80 cip + strains mainly belonging to the hypervirulent type III ST-17, ST-23, and to the bovine ST-61-67.…”

Section: Discussionmentioning

confidence: 99%

The Group B Streptococcus–Secreted Protein CIP Interacts with C4, Preventing C3b Deposition via the Lectin and Classical Complement Pathways

Pietrocola

Rindi

Rosini³

et al. 2016

The Journal of Immunology

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The group B Streptococcus (GBS) is a leading cause of neonatal invasive disease. GBS bacteria are surrounded by a thick capsular polysaccharide that is a potent inhibitor of complement deposition via the alternative pathway. Several of its surface molecules can however activate the classical and lectin complement pathways, rendering this species still vulnerable to phagocytic killing. In this study we have identified a novel secreted protein named complement interfering protein (CIP) that downregulates complement activation via the classical and lectin pathways, but not the alternative pathway. The CIP protein showed high affinity toward C4b and inhibited its interaction with C2, presumably preventing the formation of the C4bC2a convertase. Addition of recombinant CIP to GBS cip-negative bacteria resulted in decreased deposition of C3b on their surface and in diminished phagocytic killing in a whole-blood assay. Our data reveal a novel strategy exploited by GBS to counteract innate immunity and could be valuable for the development of anti-infective agents against this important pathogen.

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“…Nevertheless, several studies showed or strongly suggested that at least some ssDNA-transferring ICEs may be capable of extrachromosomal replication as plasmid-like molecules in both Gram-positive and Gramnegative bacteria (91,95,96,97).…”

Section: Replication Of Icebs1mentioning

confidence: 99%

Biology of Three ICE Families: SXT/R391, ICE Bs1 , and ICE St1 /ICE St3

Carraro

Burrus

2014

Microbiol Spectr

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Integrative and Conjugative Elements (ICEs) are bacterial mobile genetic elements that play a key role in bacterial genomes dynamics and evolution. ICEs are widely distributed among virtually all bacterial genera. Recent extensive studies have unraveled their high diversity and complexity. The present review depicts the general conserved features of ICEs and describes more precisely three major families of ICEs that have been extensively studied in the past decade for their biology, their evolution and their impact on genomes dynamics. First, the large SXT/R391 family of ICEs disseminates antibiotic resistance genes and drives the exchange of mobilizable genomic islands (MGIs) between many enteric pathogens such as Vibrio cholerae. Second, ICEBs1 of Bacillus subtilis is the most well understood ICE of Gram-positive bacteria, notably regarding the regulation of its dissemination and its initially unforeseen extrachromosomal replication, which could be a common feature of ICEs of both Gram-positive and Gram-negative bacteria. Finally, ICESt1 and ICESt3 of Streptococcus thermophilus are the prototypes of a large family of ICEs widely distributed among various streptococci. These ICEs carry an original regulation module that associates regulators related to those of both SXT/R391 and ICEBs1. Study of ICESt1 and ICESt3 uncovered the cis-mobilization of related genomic islands (CIMEs) by a mechanism called accretion-mobilization, which likely represents a paradigm for the evolution of many ICEs and genomic islands. These three major families of ICEs give a glimpse about ICEs dynamics and their high impact on bacterial adaptation.

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Lateral gene transfer of streptococcal ICE element RD2 (region of difference 2) encoding secreted proteins

Cited by 51 publications

References 42 publications

Structural and Functional Analysis of Cell Wall-anchored Polypeptide Adhesin BspA in Streptococcus agalactiae

Structural and Functional Analysis of Cell Wall-anchored Polypeptide Adhesin BspA in Streptococcus agalactiae

The Group B Streptococcus–Secreted Protein CIP Interacts with C4, Preventing C3b Deposition via the Lectin and Classical Complement Pathways

Biology of Three ICE Families: SXT/R391, ICE Bs1 , and ICE St1 /ICE St3

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