Evidence for niche adaptation in the genome of the bovine pathogen Streptococcus uberis

Philip N. Ward; Matthew T. G. Holden; James A. Leigh; Nicola Lennard; Alexandra Bignell; Andy Barron; Louise Clark; Michael A. Quail; John Woodward; Bart G. Barrell; Sharon A. Egan; Terence R. Field; Duncan Maskell; Michael Kehoe; Christopher G. Dowson; Neil Chanter; Adrian M. Whatmore; Stephen D. Bentley; Julian Parkhill

doi:10.1186/1471-2164-10-54

Evidence for niche adaptation in the genome of the bovine pathogen Streptococcus uberis

Philip N. Ward, Matthew T. G. Holden^*, James A. Leigh, Nicola Lennard, Alexandra Bignell, Andy Barron, Louise Clark, Michael A. Quail, John Woodward, Bart G. Barrell, Sharon A. Egan, Terence R. Field, Duncan Maskell, Michael Kehoe, Christopher G. Dowson, Neil Chanter, Adrian M. Whatmore, Stephen D. Bentley, Julian Parkhill

^*Corresponding author for this work

Research output: Contribution to journal › Review article › peer-review

Abstract

Background: Streptococcus uberis, a Gram positive bacterial pathogen responsible for a significant proportion of bovine mastitis in commercial dairy herds, colonises multiple body sites of the cow including the gut, genital tract and mammary gland. Comparative analysis of the complete genome sequence of S. uberis strain 0140J was undertaken to help elucidate the biology of this effective bovine pathogen.

Results: The genome revealed 1,825 predicted coding sequences (CDSs) of which 62 were identified as pseudogenes or gene fragments. Comparisons with related pyogenic streptococci identified a conserved core (40%) of orthologous CDSs. Intriguingly, S. uberis 0140J displayed a lower number of mobile genetic elements when compared with other pyogenic streptococci, however bacteriophage-derived islands and a putative genomic island were identified. Comparative genomics analysis revealed most similarity to the genomes of Streptococcus agalactiae and Streptococcus equi subsp. zooepidemicus. In contrast, streptococcal orthologs were not identified for 11% of the CDSs, indicating either unique retention of ancestral sequence, or acquisition of sequence from alternative sources. Functions including transport, catabolism, regulation and CDSs encoding cell envelope proteins were over-represented in this unique gene set; a limited array of putative virulence CDSs were identified.

Conclusion: S. uberis utilises nutritional flexibility derived from a diversity of metabolic options to successfully occupy a discrete ecological niche. The features observed in S. uberis are strongly suggestive of an opportunistic pathogen adapted to challenging and changing environmental parameters.

Original language	English
Article number	54
Number of pages	17
Journal	BMC Genomics
Volume	10
DOIs	https://doi.org/10.1186/1471-2164-10-54
Publication status	Published - 28 Jan 2009

Keywords

Group-a streptococcus
Gram-positive bacteria
Group-b streptococcus
Complete nucleotide-sequence
Hyaluronic-acid capsule
Clinical mastitis
Inorganic polyphosphate
Plasminogen-activator
Repetitive structure
Maximum-likelihood

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ward2009bmcgenomics54
© 2009 Ward et al; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
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Ward, P. N., Holden, M. T. G., Leigh, J. A., Lennard, N., Bignell, A., Barron, A., Clark, L., Quail, M. A., Woodward, J., Barrell, B. G., Egan, S. A., Field, T. R., Maskell, D., Kehoe, M., Dowson, C. G., Chanter, N., Whatmore, A. M., Bentley, S. D., & Parkhill, J. (2009). Evidence for niche adaptation in the genome of the bovine pathogen Streptococcus uberis. BMC Genomics, 10, Article 54. https://doi.org/10.1186/1471-2164-10-54

@article{20b5b35fde9b4655a8d6a4aad4873ea0,

title = "Evidence for niche adaptation in the genome of the bovine pathogen Streptococcus uberis",

abstract = "Background: Streptococcus uberis, a Gram positive bacterial pathogen responsible for a significant proportion of bovine mastitis in commercial dairy herds, colonises multiple body sites of the cow including the gut, genital tract and mammary gland. Comparative analysis of the complete genome sequence of S. uberis strain 0140J was undertaken to help elucidate the biology of this effective bovine pathogen.Results: The genome revealed 1,825 predicted coding sequences (CDSs) of which 62 were identified as pseudogenes or gene fragments. Comparisons with related pyogenic streptococci identified a conserved core (40\%) of orthologous CDSs. Intriguingly, S. uberis 0140J displayed a lower number of mobile genetic elements when compared with other pyogenic streptococci, however bacteriophage-derived islands and a putative genomic island were identified. Comparative genomics analysis revealed most similarity to the genomes of Streptococcus agalactiae and Streptococcus equi subsp. zooepidemicus. In contrast, streptococcal orthologs were not identified for 11\% of the CDSs, indicating either unique retention of ancestral sequence, or acquisition of sequence from alternative sources. Functions including transport, catabolism, regulation and CDSs encoding cell envelope proteins were over-represented in this unique gene set; a limited array of putative virulence CDSs were identified.Conclusion: S. uberis utilises nutritional flexibility derived from a diversity of metabolic options to successfully occupy a discrete ecological niche. The features observed in S. uberis are strongly suggestive of an opportunistic pathogen adapted to challenging and changing environmental parameters.",

keywords = "Group-a streptococcus, Gram-positive bacteria, Group-b streptococcus, Complete nucleotide-sequence, Hyaluronic-acid capsule, Clinical mastitis, Inorganic polyphosphate, Plasminogen-activator, Repetitive structure, Maximum-likelihood",

author = "Ward, \{Philip N.\} and Holden, \{Matthew T. G.\} and Leigh, \{James A.\} and Nicola Lennard and Alexandra Bignell and Andy Barron and Louise Clark and Quail, \{Michael A.\} and John Woodward and Barrell, \{Bart G.\} and Egan, \{Sharon A.\} and Field, \{Terence R.\} and Duncan Maskell and Michael Kehoe and Dowson, \{Christopher G.\} and Neil Chanter and Whatmore, \{Adrian M.\} and Bentley, \{Stephen D.\} and Julian Parkhill",

note = "This work was supported by the Wellcome Trust.",

year = "2009",

month = jan,

day = "28",

doi = "10.1186/1471-2164-10-54",

language = "English",

volume = "10",

journal = "BMC Genomics",

issn = "1471-2164",

publisher = "BioMed Central",

}

Ward, PN, Holden, MTG, Leigh, JA, Lennard, N, Bignell, A, Barron, A, Clark, L, Quail, MA, Woodward, J, Barrell, BG, Egan, SA, Field, TR, Maskell, D, Kehoe, M, Dowson, CG, Chanter, N, Whatmore, AM, Bentley, SD & Parkhill, J 2009, 'Evidence for niche adaptation in the genome of the bovine pathogen Streptococcus uberis', BMC Genomics, vol. 10, 54. https://doi.org/10.1186/1471-2164-10-54

TY - JOUR

T1 - Evidence for niche adaptation in the genome of the bovine pathogen Streptococcus uberis

AU - Ward, Philip N.

AU - Holden, Matthew T. G.

AU - Leigh, James A.

AU - Lennard, Nicola

AU - Bignell, Alexandra

AU - Barron, Andy

AU - Clark, Louise

AU - Quail, Michael A.

AU - Woodward, John

AU - Barrell, Bart G.

AU - Egan, Sharon A.

AU - Field, Terence R.

AU - Maskell, Duncan

AU - Kehoe, Michael

AU - Dowson, Christopher G.

AU - Chanter, Neil

AU - Whatmore, Adrian M.

AU - Bentley, Stephen D.

AU - Parkhill, Julian

N1 - This work was supported by the Wellcome Trust.

PY - 2009/1/28

Y1 - 2009/1/28

N2 - Background: Streptococcus uberis, a Gram positive bacterial pathogen responsible for a significant proportion of bovine mastitis in commercial dairy herds, colonises multiple body sites of the cow including the gut, genital tract and mammary gland. Comparative analysis of the complete genome sequence of S. uberis strain 0140J was undertaken to help elucidate the biology of this effective bovine pathogen.Results: The genome revealed 1,825 predicted coding sequences (CDSs) of which 62 were identified as pseudogenes or gene fragments. Comparisons with related pyogenic streptococci identified a conserved core (40%) of orthologous CDSs. Intriguingly, S. uberis 0140J displayed a lower number of mobile genetic elements when compared with other pyogenic streptococci, however bacteriophage-derived islands and a putative genomic island were identified. Comparative genomics analysis revealed most similarity to the genomes of Streptococcus agalactiae and Streptococcus equi subsp. zooepidemicus. In contrast, streptococcal orthologs were not identified for 11% of the CDSs, indicating either unique retention of ancestral sequence, or acquisition of sequence from alternative sources. Functions including transport, catabolism, regulation and CDSs encoding cell envelope proteins were over-represented in this unique gene set; a limited array of putative virulence CDSs were identified.Conclusion: S. uberis utilises nutritional flexibility derived from a diversity of metabolic options to successfully occupy a discrete ecological niche. The features observed in S. uberis are strongly suggestive of an opportunistic pathogen adapted to challenging and changing environmental parameters.

AB - Background: Streptococcus uberis, a Gram positive bacterial pathogen responsible for a significant proportion of bovine mastitis in commercial dairy herds, colonises multiple body sites of the cow including the gut, genital tract and mammary gland. Comparative analysis of the complete genome sequence of S. uberis strain 0140J was undertaken to help elucidate the biology of this effective bovine pathogen.Results: The genome revealed 1,825 predicted coding sequences (CDSs) of which 62 were identified as pseudogenes or gene fragments. Comparisons with related pyogenic streptococci identified a conserved core (40%) of orthologous CDSs. Intriguingly, S. uberis 0140J displayed a lower number of mobile genetic elements when compared with other pyogenic streptococci, however bacteriophage-derived islands and a putative genomic island were identified. Comparative genomics analysis revealed most similarity to the genomes of Streptococcus agalactiae and Streptococcus equi subsp. zooepidemicus. In contrast, streptococcal orthologs were not identified for 11% of the CDSs, indicating either unique retention of ancestral sequence, or acquisition of sequence from alternative sources. Functions including transport, catabolism, regulation and CDSs encoding cell envelope proteins were over-represented in this unique gene set; a limited array of putative virulence CDSs were identified.Conclusion: S. uberis utilises nutritional flexibility derived from a diversity of metabolic options to successfully occupy a discrete ecological niche. The features observed in S. uberis are strongly suggestive of an opportunistic pathogen adapted to challenging and changing environmental parameters.

KW - Group-a streptococcus

KW - Gram-positive bacteria

KW - Group-b streptococcus

KW - Complete nucleotide-sequence

KW - Hyaluronic-acid capsule

KW - Clinical mastitis

KW - Inorganic polyphosphate

KW - Plasminogen-activator

KW - Repetitive structure

KW - Maximum-likelihood

UR - https://www.scopus.com/pages/publications/62749122218

U2 - 10.1186/1471-2164-10-54

DO - 10.1186/1471-2164-10-54

M3 - Review article

SN - 1471-2164

VL - 10

JO - BMC Genomics

JF - BMC Genomics

M1 - 54

ER -

Evidence for niche adaptation in the genome of the bovine pathogen Streptococcus uberis

Abstract

Keywords

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