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Evolutionary Genomics of Staphylococcus aureus Reveals Insights into the Origin and Molecular Basis of Ruminant Host Adaptation

Guinane, CM; Ben Zakour, NL; Tormo-Mas, MA; Weinert, LA; Lowder, BV; Cartwright, RA; Smyth, DS; Smyth, CJ; Lindsay, JA; Gould, KA; et al. Guinane, CM; Ben Zakour, NL; Tormo-Mas, MA; Weinert, LA; Lowder, BV; Cartwright, RA; Smyth, DS; Smyth, CJ; Lindsay, JA; Gould, KA; Witney, A; Hinds, J; Bollback, JP; Rambaut, A; Penadés, JR; Fitzgerald, JR (2010) Evolutionary Genomics of Staphylococcus aureus Reveals Insights into the Origin and Molecular Basis of Ruminant Host Adaptation. GENOME BIOLOGY AND EVOLUTION, 2. 454 - 466. ISSN 1759-6653 https://doi.org/10.1093/gbe/evq031
SGUL Authors: Gould, Katherine Ann Hinds, Jason Lindsay, Jodi Anne Witney, Adam Austin

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Abstract

Phenotypic biotyping has traditionally been used to differentiate bacteria occupying distinct ecological niches such as host species. For example, the capacity of Staphylococcus aureus from sheep to coagulate ruminant plasma, reported over 60 years ago, led to the description of small ruminant and bovine S. aureus ecovars. The great majority of small ruminant isolates are represented by a single, widespread clonal complex (CC133) of S. aureus, but its evolutionary origin and the molecular basis for its host tropism remain unknown. Here, we provide evidence that the CC133 clone evolved as the result of a human to ruminant host jump followed by adaptive genome diversification. Comparative whole-genome sequencing revealed molecular evidence for host adaptation including gene decay and diversification of proteins involved in host– pathogen interactions. Importantly, several novel mobile genetic elements encoding virulence proteins with attenuated or enhanced activity in ruminants were widely distributed in CC133 isolates, suggesting a key role in its host-specific interactions. To investigate this further, we examined the activity of a novel staphylococcal pathogenicity island (SaPIov2) found in the great majority of CC133 isolates which encodes a variant of the chromosomally encoded von Willebrandbinding protein (vWbpSov2), previously demonstrated to have coagulase activity for human plasma. Remarkably, we discovered that SaPIov2 confers the ability to coagulate ruminant plasma suggesting an important role in ruminant disease pathogenesis and revealing the origin of a defining phenotype of the classical S. aureus biotyping scheme. Taken together, these data provide broad new insights into the origin and molecular basis of S. aureus ruminant host specificity.

Item Type: Article
Additional Information: © The Author(s) 2010. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/ 2.5), which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.
Keywords: Adaptation, Physiological, Animals, Base Sequence, Cattle, Comparative Genomic Hybridization, DNA, Bacterial, Ecosystem, Evolution, Molecular, Genome, Bacterial, Goats, Host-Pathogen Interactions, Humans, Interspersed Repetitive Sequences, Phylogeny, Ruminants, Sheep, Species Specificity, Staphylococcus aureus, Science & Technology, Life Sciences & Biomedicine, Evolutionary Biology, Genetics & Heredity, EVOLUTIONARY BIOLOGY, GENETICS & HEREDITY, bacteria, mobile genetic elements, genome diversification, population genetics, niche adaptation, VALENTINE LEUKOCIDIN GENES, AMINO-ACID SITES, POSITIVE SELECTION, PATHOGENICITY ISLAND, MAXIMUM-LIKELIHOOD, DELTA-TOXIN, BOVINE, VIRULENCE, RECOMBINATION, SEQUENCES, Developmental Biology, 0604 Genetics, 0603 Evolutionary Biology
SGUL Research Institute / Research Centre: Academic Structure > Infection and Immunity Research Institute (INII)
Journal or Publication Title: GENOME BIOLOGY AND EVOLUTION
ISSN: 1759-6653
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Dates:
DateEvent
9 June 2010Published
Web of Science ID: WOS:000280480000039
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URI: https://openaccess.sgul.ac.uk/id/eprint/1464
Publisher's version: https://doi.org/10.1093/gbe/evq031

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