Streptococcus halichoeri: Comparative Genomics of an Emerging Pathogen

Streptococcus halichoeri is an emerging pathogen with a variety of host species and zoonotic potential. It has been isolated from grey seals and other marine mammals as well as from human infections. Beginning in 2010, two concurrent epidemics were identified in Finland, in fur animals and domestic dogs, respectively. The fur animals suffered from a new disease fur animal epidemic necrotic pyoderma (FENP) and the dogs presented with ear infections with poor treatment response. S. halichoeri was isolated in both studies, albeit among other pathogens, indicating a possible role in the disease etiologies. The aim was to find a possible common origin of the fur animal and dog isolates and study the virulence factors to assess pathogenic potential. Isolates from seal, human, dogs, and fur animals were obtained for comparison. The whole genomes were sequenced from 20 different strains using the Illumina MiSeq platform and annotated using an automatic annotation pipeline RAST. The core and pangenomes were formed by comparing the genomes against each other in an all-against-all comparison. A phylogenetic tree was constructed using the genes of the core genome. Virulence factors were assessed using the Virulence Factor Database (VFDB) concentrating on the previously confirmed streptococcal factors. A core genome was formed which encompassed approximately half of the genes in Streptococcus halichoeri. The resulting core was nearly saturated and would not change significantly by adding more genomes. The remaining genes formed the pangenome which was highly variable and would still evolve after additional genomes. The results highlight the great adaptability of this bacterium possibly explaining the ease at which it switches hosts and environments. Virulence factors were also analyzed and were found primarily in the core genome. They represented many classes and functions, but the largest single category was adhesins which again supports the marine origin of this species.

[1]  T. Sironen,et al.  Comparison of Streptococcus halichoeri isolates from canine and fur animal infections: biochemical patterns, molecular characteristics and genetic relatedness , 2020, Acta Veterinaria Scandinavica.

[2]  R. Kant Genomic insights about the Lactobacillus genus , 2018 .

[3]  J. Blom,et al.  Comparative genome analysis of 24 bovine-associated Staphylococcus isolates with special focus on the putative virulence genes , 2018, PeerJ.

[4]  I. von Ossowski,et al.  An in silico pan-genomic probe for the molecular traits behind Lactobacillus ruminis gut autochthony , 2017, PloS one.

[5]  T. Sironen,et al.  Experimental Infection of Mink Enforces the Role of Arcanobacterium phocae as Causative Agent of Fur Animal Epidemic Necrotic Pyoderma (FENP) , 2016, PloS one.

[6]  A. Tait,et al.  Identification and Analysis of Immunodominant Antigens for ELISA-Based Detection of Theileria annulata , 2016, PloS one.

[7]  Jianjun Luo,et al.  BioCircos.js: an interactive Circos JavaScript library for biological data visualization on web applications , 2016, Bioinform..

[8]  A. Whitney,et al.  Phenotypic, Genotypic, and Antimicrobial Characteristics of Streptococcus halichoeri Isolates from Humans, Proposal To Rename Streptococcus halichoeri as Streptococcus halichoeri subsp. halichoeri, and Description of Streptococcus halichoeri subsp. hominis subsp. nov., a Bacterium Associated with Hu , 2016, Journal of Clinical Microbiology.

[9]  Jian Yang,et al.  VFDB 2016: hierarchical and refined dataset for big data analysis—10 years on , 2015, Nucleic Acids Res..

[10]  R. Bolea,et al.  Isolation and Phylogenetic Characterization of Streptococcus halichoeri from a European Badger (Meles meles) with Pyogranulomatous Pleuropneumonia , 2015, Journal of Comparative Pathology.

[11]  T. Sironen,et al.  Characterization of a New Epidemic Necrotic Pyoderma in Fur Animals and Its Association with Arcanobacterium phocae Infection , 2014, PloS one.

[12]  Maria Saarela,et al.  A Comparative Pan-Genome Perspective of Niche-Adaptable Cell-Surface Protein Phenotypes in Lactobacillus rhamnosus , 2014, PloS one.

[13]  R. Foo,et al.  A Fishy Tale: a Man with Empyema Caused by Streptococcus halichoeri , 2013, Journal of Clinical Microbiology.

[14]  M. Stanhope,et al.  Genome characterization and population genetic structure of the zoonotic pathogen, Streptococcus canis , 2012, BMC Microbiology.

[15]  W. D. de Vos,et al.  Comparative genomics of Lactobacillus , 2011, Microbial biotechnology.

[16]  Joakim Lundeberg,et al.  Increased Throughput by Parallelization of Library Preparation for Massive Sequencing , 2010, PloS one.

[17]  Alexander Goesmann,et al.  EDGAR: A software framework for the comparative analysis of prokaryotic genomes , 2009, BMC Bioinformatics.

[18]  David R. Riley,et al.  Comparative genomics: the bacterial pan-genome. , 2008, Current opinion in microbiology.

[19]  Rick L. Stevens,et al.  The RAST Server: Rapid Annotations using Subsystems Technology , 2008, BMC Genomics.

[20]  S. Igimi,et al.  Deletion of peb4 gene impairs cell adhesion and biofilm formation in Campylobacter jejuni. , 2007, FEMS microbiology letters.

[21]  Gerard Talavera,et al.  Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. , 2007, Systematic biology.

[22]  Jaideep P. Sundaram,et al.  Genome analysis of multiple pathogenic isolates of Streptococcus agalactiae: implications for the microbial "pan-genome". , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[23]  P. Lawson,et al.  Streptococcus halichoeri sp. nov., isolated from grey seals (Halichoerus grypus). , 2004, International journal of systematic and evolutionary microbiology.

[24]  Robert C. Edgar,et al.  MUSCLE: multiple sequence alignment with high accuracy and high throughput. , 2004, Nucleic acids research.

[25]  N. Moran,et al.  From Gene Trees to Organismal Phylogeny in Prokaryotes:The Case of the γ-Proteobacteria , 2003, PLoS biology.

[26]  J. Satsangi,et al.  Multidrug resistance 1 gene (P-glycoprotein 170): an important determinant in gastrointestinal disease? , 2003, Gut.

[27]  Thomas L. Madden,et al.  Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. , 1997, Nucleic acids research.

[28]  L. McDaniel,et al.  Pneumococcal surface protein A (PspA) is serologically highly variable and is expressed by all clinically important capsular serotypes of Streptococcus pneumoniae , 1990, Infection and immunity.

[29]  C. Poyart,et al.  Infectious Cellulitis Caused by Streptococcus halichoeri. , 2018, Acta dermato-venereologica.

[30]  Hee-Soo Lee,et al.  First Isolation of Streptococcus halichoeri and Streptococcus phocae from a Steller Sea Lion (Eumetopias jubatus) in South Korea , 2016, Journal of wildlife diseases.

[31]  P. Bork,et al.  Quantification of insect genome divergence. , 2007, Trends in genetics : TIG.