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Phylogenetic relationship and virulence inference of Streptococcus Anginosus Group: curated annotation and whole-genome comparative analysis support distinct species designation.

ABSTRACT: The Streptococcus Anginosus Group (SAG) represents three closely related species of the viridans group streptococci recognized as commensal bacteria of the oral, gastrointestinal and urogenital tracts. The SAG also cause severe invasive infections, and are pathogens during cystic fibrosis (CF) pulmonary exacerbation. Little genomic information or description of virulence mechanisms is currently available for SAG. We conducted intra and inter species whole-genome comparative analyses with 59 publically available Streptococcus genomes and seven in-house closed high quality finished SAG genomes; S. constellatus (3), S. intermedius (2), and S. anginosus (2). For each SAG species, we sequenced at least one numerically dominant strain from CF airways recovered during acute exacerbation and an invasive, non-lung isolate. We also evaluated microevolution that occurred within two isolates that were cultured from one individual one year apart.The SAG genomes were most closely related to S. gordonii and S. sanguinis, based on shared orthologs and harbor a similar number of proteins within each COG category as other Streptococcus species. Numerous characterized streptococcus virulence factor homologs were identified within the SAG genomes including; adherence, invasion, spreading factors, LPxTG cell wall proteins, and two component histidine kinases known to be involved in virulence gene regulation. Mobile elements, primarily integrative conjugative elements and bacteriophage, account for greater than 10% of the SAG genomes. S. anginosus was the most variable species sequenced in this study, yielding both the smallest and the largest SAG genomes containing multiple genomic rearrangements, insertions and deletions. In contrast, within the S. constellatus and S. intermedius species, there was extensive continuous synteny, with only slight differences in genome size between strains. Within S. constellatus we were able to determine important SNPs and changes in VNTR numbers that occurred over the course of one year.The comparative genomic analysis of the SAG clarifies the phylogenetics of these bacteria and supports the distinct species classification. Numerous potential virulence determinants were identified and provide a foundation for further studies into SAG pathogenesis. Furthermore, the data may be used to enable the development of rapid diagnostic assays and therapeutics for these pathogens.

SUBMITTER: Olson AB

PROVIDER: S-EPMC3897883 | biostudies-literature | 2013 Dec

REPOSITORIES: biostudies-literature

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Phylogenetic relationship and virulence inference of Streptococcus Anginosus Group: curated annotation and whole-genome comparative analysis support distinct species designation.

Olson Adam B AB Kent Heather H Sibley Christopher D CD Grinwis Margot E ME Mabon Philip P Ouellette Claude C Tyson Shari S Graham Morag M Tyler Shaun D SD Van Domselaar Gary G Surette Michael G MG Corbett Cindi R CR

BMC genomics 20131217

<h4>Background</h4>The Streptococcus Anginosus Group (SAG) represents three closely related species of the viridans group streptococci recognized as commensal bacteria of the oral, gastrointestinal and urogenital tracts. The SAG also cause severe invasive infections, and are pathogens during cystic fibrosis (CF) pulmonary exacerbation. Little genomic information or description of virulence mechanisms is currently available for SAG. We conducted intra and inter species whole-genome comparative an ...[more]

PMID: 24341328

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Project description:Streptococcus anginosus is an important cause of brain and liver abscesses, meningitis, appendicitis, female genital tract infection, neonatal sepsis, and bacteremia. Recent studies show that S. anginosus is responsible for around 30% of streptococci associated purulent infections of internal organs. Genome sequencing of S. anginosus identified a phage-like chromosomal island (SanCI) integrated into the DNA mismatch repair operon. In S. pyogenes, related chromosomal islands (SpyCI) integrated into the same operon confer a mutator phenotype as well as alter global gene regulation, including the increased expression of many virulence factors. We hypothesized that SanCI will also alter global transcription patterns and virulence in S. anginosus. The SanCI from strain F0211 was introduced into a SanCI-free S. anginosus strain (J4211) by natural transformation. To provide a selectable marker for transformation, gene strA, encoding a predicted transcriptional regulator, was replaced in F0211 with the gene conferring erythromycin resistance (ermB), which after transfer created strain OKSan3. A functional copy of strA was then returned to this derivative of J4211, creating strain OKSan4. RNA sequencing (RNA-seq) of strains J4211, OKSan4 and OKSan3 confirmed that the addition of the SanCI altered S. anginosus global transcription patterns with increased expression of virulence, stress response and competence factors in a growth phase dependent manner. Virulence studies using Galleria mellonella as an acute infection model showed significantly increased inflammation and mortality in larvae challenged with strains OKSan4 and OKSan3 as compare to SanCI-free strain J4211. qRT-PCR analysis supported these results, revealing that antimicrobial factors of G. mellonella were more highly expressed after infection with OKSan4 compare to J4211 infection. Further, RNA-seq suggested that SanCI-encoded gene strA may encode one of the factors responsible for altered global transcriptional changes. The result of this study along with our previous studies in S. pyogenes demonstrate that streptococcal chromosomal islands are a unique class of virulence factors that improve the fitness of their host cell by altering global transcription patterns and increasing virulence.

Project description:The ITS2 gene class shows a high sequence divergence among its members that have complicated its annotation and its use for reconstructing phylogenies at a higher taxonomical level (beyond species and genus). Several alignment strategies have been implemented to improve the ITS2 annotation quality and its use for phylogenetic inferences. Although, alignment based methods have been exploited to the top of its complexity to tackle both issues, no alignment-free approaches have been able to successfully address both topics. By contrast, the use of simple alignment-free classifiers, like the topological indices (TIs) containing information about the sequence and structure of ITS2, may reveal to be a useful approach for the gene prediction and for assessing the phylogenetic relationships of the ITS2 class in eukaryotes. Thus, we used the TI2BioP (Topological Indices to BioPolymers) methodology [1], [2], freely available at http://ti2biop.sourceforge.net/ to calculate two different TIs. One class was derived from the ITS2 artificial 2D structures generated from DNA strings and the other from the secondary structure inferred from RNA folding algorithms. Two alignment-free models based on Artificial Neural Networks were developed for the ITS2 class prediction using the two classes of TIs referred above. Both models showed similar performances on the training and the test sets reaching values above 95% in the overall classification. Due to the importance of the ITS2 region for fungi identification, a novel ITS2 genomic sequence was isolated from Petrakia sp. This sequence and the test set were used to comparatively evaluate the conventional classification models based on multiple sequence alignments like Hidden Markov based approaches, revealing the success of our models to identify novel ITS2 members. The isolated sequence was assessed using traditional and alignment-free based techniques applied to phylogenetic inference to complement the taxonomy of the Petrakia sp. fungal isolate.

Project description:Cystic fibrosis (CF) airways harbour complex and dynamic polymicrobial communities that include many oral bacteria. Despite increased knowledge of CF airway microbiomes the interaction between established CF pathogens and other resident microbes and resulting impact on disease progression is poorly understood. Previous studies have demonstrated that oral commensal streptococci of the Anginosus group (AGS) can establish chronic pulmonary infections and become numerically dominant in CF sputa indicating that they play an important role in CF microbiome dynamics. In this study a strain of Pseudomonas aeruginosa (DWW2) of the mucoid alginate overproducing phenotype associated with chronic CF airway infection and a strain of the oral commensal AGS species Streptococcus anginosus (3a) from CF sputum were investigated for their ability to co-exist and their responses to biofilm co-culture. Bacteria in biofilms were quantified, pyocyanin expression by DWW2 was measured and the effect of AGS strain 3a on reversion of DWW2 to a non-mucoidal phenotype investigated. The virulence of DWW2, 3a and colony variant phenotypes of DWW2 in mono- and co-culture were compared in a Galleria mellonella infection model. Co-culture biofilms were formed in normoxic, hypercapnic (10% CO2) and anoxic atmospheres with the streptococcus increasing in number in co-culture, indicating that these bacteria would be able to co-exist and thrive within the heterogeneous microenvironments of the CF airway. The streptococcus caused increased pyocyanin expression by DWW2 and colony variants by stimulating reversion of the mucoid phenotype to the high pyocyanin expressing non-mucoid phenotype. The latter was highly virulent in the infection model with greater virulence when in co-culture with the streptococcus. The results of this study demonstrate that the oral commensal S. anginosus benefits from interaction with P. aeruginosa of the CF associated mucoid phenotype and modulates the behaviour of the pseudomonad in ways that may be clinically relevant.

Dataset Information

Phylogenetic relationship and virulence inference of Streptococcus Anginosus Group: curated annotation and whole-genome comparative analysis support distinct species designation.

Publications

Phylogenetic relationship and virulence inference of Streptococcus Anginosus Group: curated annotation and whole-genome comparative analysis support distinct species designation.

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