Cargando…

Phylogenetic, epidemiological and functional analyses of the Streptococcus bovis/Streptococcus equinus complex through an overarching MLST scheme

BACKGROUND: The Streptococcus bovis/Streptococcus equinus complex (SBSEC) comprises seven (sub)species classified as human and animal commensals, emerging opportunistic pathogens and food fermentative organisms. Changing taxonomy, shared habitats, natural competence and evidence for horizontal gene...

Descripción completa

Detalles Bibliográficos
Autores principales: Jans, Christoph, de Wouters, Tomas, Bonfoh, Bassirou, Lacroix, Christophe, Kaindi, Dasel Wambua Mulwa, Anderegg, Janine, Böck, Désirée, Vitali, Sabrina, Schmid, Thomas, Isenring, Julia, Kurt, Fabienne, Kogi-Makau, Wambui, Meile, Leo
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4915170/
https://www.ncbi.nlm.nih.gov/pubmed/27329036
http://dx.doi.org/10.1186/s12866-016-0735-2
_version_ 1782438659390177280
author Jans, Christoph
de Wouters, Tomas
Bonfoh, Bassirou
Lacroix, Christophe
Kaindi, Dasel Wambua Mulwa
Anderegg, Janine
Böck, Désirée
Vitali, Sabrina
Schmid, Thomas
Isenring, Julia
Kurt, Fabienne
Kogi-Makau, Wambui
Meile, Leo
author_facet Jans, Christoph
de Wouters, Tomas
Bonfoh, Bassirou
Lacroix, Christophe
Kaindi, Dasel Wambua Mulwa
Anderegg, Janine
Böck, Désirée
Vitali, Sabrina
Schmid, Thomas
Isenring, Julia
Kurt, Fabienne
Kogi-Makau, Wambui
Meile, Leo
author_sort Jans, Christoph
collection PubMed
description BACKGROUND: The Streptococcus bovis/Streptococcus equinus complex (SBSEC) comprises seven (sub)species classified as human and animal commensals, emerging opportunistic pathogens and food fermentative organisms. Changing taxonomy, shared habitats, natural competence and evidence for horizontal gene transfer pose difficulties for determining their phylogeny, epidemiology and virulence mechanisms. Thus, novel phylogenetic and functional classifications are required. An SBSEC overarching multi locus sequence type (MLST) scheme targeting 10 housekeeping genes was developed, validated and combined with host-related properties of adhesion to extracellular matrix proteins (ECM), activation of the immune responses via NF-KB and survival in simulated gastric juice (SGJ). RESULTS: Commensal and pathogenic SBSEC strains (n = 74) of human, animal and food origin from Europe, Asia, America and Africa were used in the MLST scheme yielding 66 sequence types and 10 clonal complexes differentiated into distinct habitat-associated and mixed lineages. Adhesion to ECMs collagen I and mucin type II was a common characteristic (23 % of strains) followed by adhesion to fibronectin and fibrinogen (19.7 %). High adhesion abilities were found for East African dairy and human blood isolate branches whereas commensal fecal SBSEC displayed low adhesion. NF-KB activation was observed for a limited number of dairy and blood isolates suggesting the potential of some pathogenic strains for reduced immune activation. Strains from dairy MLST clades displayed the highest relative survival to SGJ independently of dairy adaptation markers lacS/lacZ. CONCLUSION: Combining phylogenetic and functional analyses via SBSEC MLST enabled the clear delineation of strain clades to unravel the complexity of this bacterial group. High adhesion values shared between certain dairy and blood strains as well as the behavior of NF-KB activation are concerning for specific lineages. They highlighted the health risk among shared lineages and establish the basis to elucidate (zoonotic-) transmission, host specificity, virulence mechanisms and enhanced risk assessment as pathobionts in an overarching One Health approach. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12866-016-0735-2) contains supplementary material, which is available to authorized users.
format Online
Article
Text
id pubmed-4915170
institution National Center for Biotechnology Information
language English
publishDate 2016
publisher BioMed Central
record_format MEDLINE/PubMed
spelling pubmed-49151702016-06-22 Phylogenetic, epidemiological and functional analyses of the Streptococcus bovis/Streptococcus equinus complex through an overarching MLST scheme Jans, Christoph de Wouters, Tomas Bonfoh, Bassirou Lacroix, Christophe Kaindi, Dasel Wambua Mulwa Anderegg, Janine Böck, Désirée Vitali, Sabrina Schmid, Thomas Isenring, Julia Kurt, Fabienne Kogi-Makau, Wambui Meile, Leo BMC Microbiol Research Article BACKGROUND: The Streptococcus bovis/Streptococcus equinus complex (SBSEC) comprises seven (sub)species classified as human and animal commensals, emerging opportunistic pathogens and food fermentative organisms. Changing taxonomy, shared habitats, natural competence and evidence for horizontal gene transfer pose difficulties for determining their phylogeny, epidemiology and virulence mechanisms. Thus, novel phylogenetic and functional classifications are required. An SBSEC overarching multi locus sequence type (MLST) scheme targeting 10 housekeeping genes was developed, validated and combined with host-related properties of adhesion to extracellular matrix proteins (ECM), activation of the immune responses via NF-KB and survival in simulated gastric juice (SGJ). RESULTS: Commensal and pathogenic SBSEC strains (n = 74) of human, animal and food origin from Europe, Asia, America and Africa were used in the MLST scheme yielding 66 sequence types and 10 clonal complexes differentiated into distinct habitat-associated and mixed lineages. Adhesion to ECMs collagen I and mucin type II was a common characteristic (23 % of strains) followed by adhesion to fibronectin and fibrinogen (19.7 %). High adhesion abilities were found for East African dairy and human blood isolate branches whereas commensal fecal SBSEC displayed low adhesion. NF-KB activation was observed for a limited number of dairy and blood isolates suggesting the potential of some pathogenic strains for reduced immune activation. Strains from dairy MLST clades displayed the highest relative survival to SGJ independently of dairy adaptation markers lacS/lacZ. CONCLUSION: Combining phylogenetic and functional analyses via SBSEC MLST enabled the clear delineation of strain clades to unravel the complexity of this bacterial group. High adhesion values shared between certain dairy and blood strains as well as the behavior of NF-KB activation are concerning for specific lineages. They highlighted the health risk among shared lineages and establish the basis to elucidate (zoonotic-) transmission, host specificity, virulence mechanisms and enhanced risk assessment as pathobionts in an overarching One Health approach. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12866-016-0735-2) contains supplementary material, which is available to authorized users. BioMed Central 2016-06-21 /pmc/articles/PMC4915170/ /pubmed/27329036 http://dx.doi.org/10.1186/s12866-016-0735-2 Text en © The Author(s). 2016 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
Jans, Christoph
de Wouters, Tomas
Bonfoh, Bassirou
Lacroix, Christophe
Kaindi, Dasel Wambua Mulwa
Anderegg, Janine
Böck, Désirée
Vitali, Sabrina
Schmid, Thomas
Isenring, Julia
Kurt, Fabienne
Kogi-Makau, Wambui
Meile, Leo
Phylogenetic, epidemiological and functional analyses of the Streptococcus bovis/Streptococcus equinus complex through an overarching MLST scheme
title Phylogenetic, epidemiological and functional analyses of the Streptococcus bovis/Streptococcus equinus complex through an overarching MLST scheme
title_full Phylogenetic, epidemiological and functional analyses of the Streptococcus bovis/Streptococcus equinus complex through an overarching MLST scheme
title_fullStr Phylogenetic, epidemiological and functional analyses of the Streptococcus bovis/Streptococcus equinus complex through an overarching MLST scheme
title_full_unstemmed Phylogenetic, epidemiological and functional analyses of the Streptococcus bovis/Streptococcus equinus complex through an overarching MLST scheme
title_short Phylogenetic, epidemiological and functional analyses of the Streptococcus bovis/Streptococcus equinus complex through an overarching MLST scheme
title_sort phylogenetic, epidemiological and functional analyses of the streptococcus bovis/streptococcus equinus complex through an overarching mlst scheme
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4915170/
https://www.ncbi.nlm.nih.gov/pubmed/27329036
http://dx.doi.org/10.1186/s12866-016-0735-2
work_keys_str_mv AT janschristoph phylogeneticepidemiologicalandfunctionalanalysesofthestreptococcusbovisstreptococcusequinuscomplexthroughanoverarchingmlstscheme
AT dewouterstomas phylogeneticepidemiologicalandfunctionalanalysesofthestreptococcusbovisstreptococcusequinuscomplexthroughanoverarchingmlstscheme
AT bonfohbassirou phylogeneticepidemiologicalandfunctionalanalysesofthestreptococcusbovisstreptococcusequinuscomplexthroughanoverarchingmlstscheme
AT lacroixchristophe phylogeneticepidemiologicalandfunctionalanalysesofthestreptococcusbovisstreptococcusequinuscomplexthroughanoverarchingmlstscheme
AT kaindidaselwambuamulwa phylogeneticepidemiologicalandfunctionalanalysesofthestreptococcusbovisstreptococcusequinuscomplexthroughanoverarchingmlstscheme
AT andereggjanine phylogeneticepidemiologicalandfunctionalanalysesofthestreptococcusbovisstreptococcusequinuscomplexthroughanoverarchingmlstscheme
AT bockdesiree phylogeneticepidemiologicalandfunctionalanalysesofthestreptococcusbovisstreptococcusequinuscomplexthroughanoverarchingmlstscheme
AT vitalisabrina phylogeneticepidemiologicalandfunctionalanalysesofthestreptococcusbovisstreptococcusequinuscomplexthroughanoverarchingmlstscheme
AT schmidthomas phylogeneticepidemiologicalandfunctionalanalysesofthestreptococcusbovisstreptococcusequinuscomplexthroughanoverarchingmlstscheme
AT isenringjulia phylogeneticepidemiologicalandfunctionalanalysesofthestreptococcusbovisstreptococcusequinuscomplexthroughanoverarchingmlstscheme
AT kurtfabienne phylogeneticepidemiologicalandfunctionalanalysesofthestreptococcusbovisstreptococcusequinuscomplexthroughanoverarchingmlstscheme
AT kogimakauwambui phylogeneticepidemiologicalandfunctionalanalysesofthestreptococcusbovisstreptococcusequinuscomplexthroughanoverarchingmlstscheme
AT meileleo phylogeneticepidemiologicalandfunctionalanalysesofthestreptococcusbovisstreptococcusequinuscomplexthroughanoverarchingmlstscheme