Evidence for niche adaptation in the genome of the bovine pathogen Streptococcus uberis
Ward, Philip N., Holden, Matthew T. G., Leigh, James A., Lennard, Nicola, Bignell, Alexandra, Barron, Andy, Clark, Louise, Quail, Michael A., Woodward, John, Barrell, Bart G., Egan, Sharon A., Field, Terence R., Maskell, Duncan, Kehoe, Michael, Dowson, Christopher G. and Chanter, Neil (2009) Evidence for niche adaptation in the genome of the bovine pathogen Streptococcus uberis. BMC Genomics, Vol.10 . Article No. 54. ISSN 1471-2164 Official URL: http://www.biomedcentral.com/1471-2164/10/54 AbstractBackground
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.
| Item Type: | Journal Article |
|---|
| Subjects: | Q Science > QR Microbiology |
|---|
| Divisions: | Faculty of Social Sciences > Institute of Education Faculty of Science > Life Sciences (2010- ) |
|---|
| Library of Congress Subject Headings (LCSH): | Streptococcus -- Genetics, Mastitis, Genomes, Pathogenic microorganism |
|---|
| Journal or Publication Title: | BMC Genomics |
|---|
| Publisher: | BioMed Central Ltd. |
|---|
| ISSN: | 1471-2164 |
|---|
| Date: | 28 January 2009 |
|---|
| Volume: | Vol.10 |
|---|
| Page Range: | Article No. 54 |
|---|
| Status: | Peer Reviewed |
|---|
| Publication Status: | Published |
|---|
| Access rights to Published version: | Open Access |
|---|
| Funder: | Wellcome Trust (London, England) |
|---|
| References: | 1. Gottschalk M, Segura M, Xu J: Streptococcus suis infections in
humans: the Chinese experience and the situation in North
America. Anim Health Res Rev 2007, 8:29-45.
2. Bisharat N, Crook DW, Leigh J, Harding RM, Ward PN, Coffey TJ,
Maiden MC, Peto T, Jones N: Hyperinvasive neonatal group B
streptococcus has arisen from a bovine ancestor. J Clin Microbiol
2004, 42:2161-2167.
3. Bentley RW, Leigh JA, Collins MD: Intrageneric structure of
Streptococcus based on comparative analysis of small-subunit
rRNA sequences. Int J Syst Bacteriol 1991, 41:487-494.
4. Compton CW, Heuer C, Parker K, McDougall S: Epidemiology of
mastitis in pasture-grazed peripartum dairy heifers and its
effects on productivity. J Dairy Sci 2007, 90:4157-4170.
5. Olde Riekerink RG, Barkema HW, Kelton DF, Scholl DT: Incidence
rate of clinical mastitis on Canadian dairy farms. J Dairy Sci
2008, 91:1366-1377.
6. Sorensen LP, Guldbrandtsen B, Thomasen JR, Lund MS: Pathogenspecific
effects of quantitative trait loci affecting clinical mastitis
and somatic cell count in Danish Holstein cattle. J Dairy
Sci 2008, 91:2493-2500.
7. Bradley AJ, Leach KA, Breen JE, Green LE, Green MJ: Survey of the
incidence and aetiology of mastitis on dairy farms in England
and Wales. Vet Rec 2007, 160:253-257.
8. Leigh JA: Streptococcus uberis: a permanent barrier to the
control of bovine mastitis? Vet J 1999, 157:225-238.
9. Bramley AJ: Sources of Streptococcus uberis in the dairy herd.
I. Isolation from bovine faeces and from straw bedding of
cattle. J Dairy Res 1982, 49:369-373.
10. Kruze J, Bramley AJ: Sources of Streptococcus uberis in the
dairy herd. II. Evidence of colonization of the bovine intestine
by Str. uberis. J Dairy Res 1982, 49:375-379.
11. Lopez-Benavides MG, Williamson JH, Pullinger GD, Lacy-Hulbert SJ,
Cursons RT, Leigh JA: Field observations on the variation of
Streptococcus uberis populations in a pasture-based dairy
farm. J Dairy Sci 2007, 90:5558-5566.
12. Hill AW: Pathogenicity of two strains of Streptococcus uberis
infused into lactating and non-lactating bovine mammary
glands. Res Vet Sci 1988, 45:400-404.
13. Sordillo LM, Shafer-Weaver K, DeRosa D: Immunobiology of the
mammary gland. J Dairy Sci 1997, 80:1851-1865.
14. Coffey TJ, Pullinger GD, Urwin R, Jolley KA, Wilson SM, Maiden MC,
Leigh JA: First insights into the evolution of Streptococcus
uberis: a multilocus sequence typing scheme that enables
investigation of its population biology. Appl Environ Microbiol
2006, 72:1420-1428.
15. Leigh JA, Ward PN, Field TR: The exploitation of the genome in
the search for determinants of virulence in Streptococcus
uberis. Vet Immunol Immunopathol 2004, 100:145-149.
16. Ferretti JJ, McShan WM, Ajdic D, Savic DJ, Savic G, Lyon K, Primeaux
C, Sezate S, Suvorov AN, Kenton S, Lai HS, Lin SP, Qian Y, Jia HG,
Najar FZ, Ren Q, Zhu H, Song L, White J, Yuan X, Clifton SW, Roe
BA, McLaughlin R: Complete genome sequence of an M1 strain
of Streptococcus pyogenes. Proc Natl Acad Sci USA 2001,
98:4658-4663.
17. Tettelin H, Masignani V, Cieslewicz MJ, Eisen JA, Peterson S, Wessels
MR, Paulsen IT, Nelson KE, Margarit I, Read TD, Madoff LC, Wolf AM,
Beanan MJ, Brinkac LM, Daugherty SC, DeBoy RT, Durkin AS, Kolonay
JF, Madupu R, Lewis MR, Radune D, Fedorova NB, Scanlan D,
Khouri H, Mulligan S, Carty HA, Cline RT, Van Aken SE, Gill J, Scarselli
M, Mora M, Iacobini ET, Brettoni C, Galli G, Mariani M, Vegni F,
Maione D, Rinaudo D, Rappuoli R, Telford JL, Kasper DL, Grandi G,
Fraser CM: Complete genome sequence and comparative
genomic analysis of an emerging human pathogen, serotype
V Streptococcus agalactiae. Proc Natl Acad Sci USA 2002,
99:12391-12396.
18. Shen K, Gladitz J, Antalis P, Dice B, Janto B, Keefe R, Hayes J, Ahmed
A, Dopico R, Ehrlich N, Jocz J, Kropp L, Yu S, Nistico L, Greenberg
DP, Barbadora K, Preston RA, Post JC, Ehrlich GD, Hu FZ: Characterization,
distribution, and expression of novel genes
among eight clinical isolates of Streptococcus pneumoniae.
Infect Immun 2006, 74:321-330.
19. Hiller NL, Janto B, Hogg JS, Boissy R, Yu S, Powell E, Keefe R, Ehrlich
NE, Shen K, Hayes J, Barbadora K, Klimke W, Dernovoy D, Tatusova
T, Parkhill J, Bentley SD, Post JC, Ehrlich GD, Hu FZ: Comparative
genomic analyses of seventeen Streptococcus pneumoniae
Additional File 1
Table Pseudogenes S1: and partial genes in the S. uberis 0140J
genome. Table S1: Table containing a list of the predicted products, systematic
IDs, and putative mutations associated with pseudogenes and partial
genes in the S. uberis 0140J genome.
Click here for file
[http://www.biomedcentral.com/content/supplementary/1471-
2164-10-54-S1.pdf]
Additional File 2
Unique CDSs compared to other sequenced streptococci. Table containing
a list of the systematic IDs and predicted products for CDSs in the S.
uberis 0140J genome that do not have reciprocal Fasta matches in S.
pyogenes Manfredo, S. equi 4047, S. zooepidemicus H70, S. thermophilus
CNRZ1066, S. suis P1/7, S. pneumoniae TIGR4, S. sanguinis
SK36, S. mutans UA159, S. agalactiae NEM316, and S.
gordonii str. Challis substr. CH1.
strains: insights into the pneumococcal supragenome. J Bacteriol
2007, 189:8186-8195.
20. Ferretti JJ, Ajdic D, McShan WM: Comparative genomics of
streptococcal species. Indian J Med Res 2004, 119(Suppl):1-6.
21. Marri PR, Hao W, Golding GB: Gene gain and gene loss in streptococcus:
is it driven by habitat? Mol Biol Evol 2006,
23:2379-2391.
22. Delorme C, Poyart C, Ehrlich SD, Renault P: Extent of horizontal
gene transfer in evolution of Streptococci of the salivarius
group. J Bacteriol 2007, 189:1330-1341.
23. Bolotin A, Quinquis B, Renault P, Sorokin A, Ehrlich SD, Kulakauskas
S, Lapidus A, Goltsman E, Mazur M, Pusch GD, Fonstein M, Overbeek
R, Kyprides N, Purnelle B, Prozzi D, Ngui K, Masuy D, Hancy F, Burteau
S, Boutry M, Delcour J, Goffeau A, Hols P: Complete
sequence and comparative genome analysis of the dairy bacterium
Streptococcus thermophilus. Nat Biotechnol 2004,
22:1554-1558.
24. Delorme C: Streptococcus thermophilus. International Journal of
Food Microbiology 126:274-277.
25. Holden MTG, Heather Z, Paillot R, Steward K, Webb K, Ainslie F,
Jourdan T, Bason N, Holroyd N, Mungall K, Quail MA, Sanders M,
Simmonds M, Willey D, Brooks K, Aanensen DM, Spratt BG, Jolley
KA, Maiden MC, Kehoe M, Chanter N, Robinson C, Maskell D,
Parkhill J, Waller AS: Genomic evidence for the evolution of
Streptococcus equi: host restriction, increased virulence and
genetic exchange with human pathogens. in press.
26. Holden MT, Scott A, Cherevach I, Chillingworth T, Churcher C,
Cronin A, Dowd L, Feltwell T, Hamlin N, Holroyd S, Jagels K, Moule
S, Mungall K, Quail MA, Price C, Rabbinowitsch E, Sharp S, Skelton J,
Whitehead S, Barrell BG, Kehoe M, Parkhill J: Complete genome
of acute rheumatic fever-associated serotype M5 Streptococcus
pyogenes strain manfredo. J Bacteriol 2007, 189:1473-1477.
27. Facklam R: What happened to the streptococci: overview of
taxonomic and nomenclature changes. Clin Microbiol Rev 2002,
15:613-630.
28. Beres SB, Musser JM: Contribution of exogenous genetic elements
to the group A Streptococcus metagenome. PLoS ONE
2007, 2:e800.
29. Tettelin H, Masignani V, Cieslewicz MJ, Donati C, Medini D, Ward
NL, Angiuoli SV, Crabtree J, Jones AL, Durkin AS, Deboy RT, Davidsen
TM, Mora M, Scarselli M, Margarit y Ros I, Peterson JD, Hauser
CR, Sundaram JP, Nelson WC, Madupu R, Brinkac LM, Dodson RJ,
Rosovitz MJ, Sullivan SA, Daugherty SC, Haft DH, Selengut J, Gwinn
ML, Zhou L, Zafar N, Khouri H, Radune D, Dimitrov G, Watkins K,
O'Connor KJ, Smith S, Utterback TR, White O, Rubens CE, Grandi
G, Madoff LC, Kasper DL, Telford JL, Wessels MR, Rappuoli R, Fraser
CM: Genome analysis of multiple pathogenic isolates of
Streptococcus agalactiae: implications for the microbial
"pan-genome". Proc Natl Acad Sci USA 2005, 102:13950-13955.
30. Cantarel BL, Coutinho PM, Rancurel C, Bernard T, Lombard V, Henrissat
B: The Carbohydrate-Active EnZymes database
(CAZy): an expert resource for Glycogenomics. Nucleic Acids
Res 2008.
31. Poolman B: Transporters and their roles in LAB cell physiology.
Antonie Van Leeuwenhoek 2002, 82:147-164.
32. Ajdic D, McShan WM, McLaughlin RE, Savic G, Chang J, Carson MB,
Primeaux C, Tian R, Kenton S, Jia H, Lin S, Qian Y, Li S, Zhu H, Najar
F, Lai H, White J, Roe BA, Ferretti JJ: Genome sequence of Streptococcus
mutans UA159, a cariogenic dental pathogen. Proc
Natl Acad Sci USA 2002, 99:14434-14439.
33. Yamamoto Y, Poyart C, Trieu-Cuot P, Lamberet G, Gruss A, Gaudu
P: Respiration metabolism of Group B Streptococcus is activated
by environmental haem and quinone and contributes
to virulence. Mol Microbiol 2005, 56:525-534.
34. Rezaiki L, Lamberet G, Derre A, Gruss A, Gaudu P: Lactococcus
lactis produces short-chain quinones that cross-feed Group
B Streptococcus to activate respiration growth. Mol Microbiol
2008, 67:947-957.
35. Ault-Riche D, Fraley CD, Tzeng CM, Kornberg A: Novel assay
reveals multiple pathways regulating stress-induced accumulations
of inorganic polyphosphate in Escherichia coli. J
Bacteriol 1998, 180:1841-1847.
36. Kim KS, Rao NN, Fraley CD, Kornberg A: Inorganic polyphosphate
is essential for long-term survival and virulence factors
in Shigella and Salmonella spp. Proc Natl Acad Sci USA 2002,
99:7675-7680.
37. Jahid IK, Silva AJ, Benitez JA: Polyphosphate stores enhance the
ability of Vibrio cholerae to overcome environmental
stresses in a low-phosphate environment. Appl Environ Microbiol
2006, 72:7043-7049.
38. McMeechan A, Lovell MA, Cogan TA, Marston KL, Humphrey TJ, Barrow
PA: Inactivation of ppk differentially affects virulence and
disrupts ATP homeostasis in Salmonella enterica serovars
Typhimurium and Gallinarum. Res Microbiol 2007, 158:79-85.
39. Candon HL, Allan BJ, Fraley CD, Gaynor EC: Polyphosphate
kinase 1 is a pathogenesis determinant in Campylobacter
jejuni. J Bacteriol 2007, 189:8099-8108.
40. Heir E, Sundheim G, Holck AL: The Staphylococcus qacH gene
product: a new member of the SMR family encoding multidrug
resistance. FEMS Microbiol Lett 1998, 163:49-56.
41. Wirawan RE, Swanson KM, Kleffmann T, Jack RW, Tagg JR: Uberolysin:
a novel cyclic bacteriocin produced by Streptococcus
uberis. Microbiology 2007, 153:1619-1630.
42. Wirawan RE, Klesse NA, Jack RW, Tagg JR: Molecular and genetic
characterization of a novel nisin variant produced by Streptococcus
uberis. Appl Environ Microbiol 2006, 72:1148-1156.
43. Heng NC, Burtenshaw GA, Jack RW, Tagg JR: Ubericin A, a class
IIa bacteriocin produced by Streptococcus uberis. Appl Environ
Microbiol 2007, 73:7763-7766.
44. Holden MTG, Feil EJ, Lindsay JA, Peacock SJ, Day NPJ, Enright MC,
Foster TJ, Moore CE, Hurst L, Atkin R, Barron A, Bason N, Bentley
SD, Chillingworth C, Chillingworth T, Churcher C, Clark L, Corton
C, Cronin A, Doggett J, Dowd L, Feltwell T, Hance Z, Harris B,
Hauser H, Holroyd S, Jagels K, James KD, Lennard N, Line A, Mayes
R, Moule S, Mungall K, Ormond D, Quail MA, Rabbinowitsch E,
Rutherford K, Sanders M, Sharp S, Simmonds M, Stevens K, Whitehead
S, Barrell BG, Spratt BG, Parkhill J: Complete genomes of
two clinical Staphylococcus aureus strains: Evidence for the
rapid evolution of virulence and drug resistance. Proc Natl
Acad Sci USA 2004, 101:9786-9791.
45. Lerat E, Ochman H: Recognizing the pseudogenes in bacterial
genomes. Nucleic Acids Res 2005, 33:3125-3132.
46. Christie J, McNab R, Jenkinson HF: Expression of fibronectinbinding
protein FbpA modulates adhesion in Streptococcus
gordonii. Microbiology 2002, 148:1615-1625.
47. Comfort D, Clubb RT: A comparative genome analysis identifies
distinct sorting pathways in gram-positive bacteria. Infect
Immun 2004, 72:2710-2722.
48. Dramsi S, Trieu-Cuot P, Bierne H: Sorting sortases: a nomenclature
proposal for the various sortases of Gram-positive bacteria.
Res Microbiol 2005, 156:289-297.
49. Pallen MJ, Lam AC, Antonio M, Dunbar K: An embarrassment of
sortases – a richness of substrates? Trends Microbiol 2001,
9:97-102.
50. Mazmanian SK, Liu G, Ton-That H, Schneewind O: Staphylococcus
aureus sortase, an enzyme that anchors surface proteins to
the cell wall. Science 1999, 285:760-763.
51. Schneewind O, Mihaylova-Petkov D, Model P: Cell wall sorting signals
in surface proteins of gram-positive bacteria. Embo J
1993, 12:4803-4811.
52. Moshynskyy I, Jiang M, Fontaine MC, Perez-Casal J, Babiuk LA, Potter
AA: Characterization of a bovine lactoferrin binding protein
of Streptococcus uberis. Microb Pathog 2003, 35:203-215.
53. Whatmore AM: Streptococcus pyogenes sclB encodes a putative
hypervariable surface protein with a collagen-like repetitive
structure. Microbiology 2001, 147:419-429.
54. Hagiwara S, Kawai K, Anri A, Nagahata H: Lactoferrin concentrations
in milk from normal and subclinical mastitic cows. J Vet
Med Sci 2003, 65:319-323.
55. Harmon RJ, Schanbacher FL, Ferguson LC, Smith KL: Changes in
lactoferrin, immunoglobulin G, bovine serum albumin, and
alpha-lactalbumin during acute experimental and natural
coliform mastitis in cows. Infect Immun 1976, 13:533-542.
56. Todhunter DA, Smith KL, Schoenberger PS: In vitro growth of
mastitis-associated streptococci in bovine mammary secretions.
J Dairy Sci 1985, 68:2337-2346.
57. Almeida RA, Luther DA, Park HM, Oliver SP: Identification, isolation,
and partial characterization of a novel Streptococcus
uberis adhesion molecule (SUAM). Vet Microbiol 2006,
115:183-191.
58. Fang W, Oliver SP: Identification of lactoferrin-binding proteins
in bovine mastitis-causing Streptococcus uberis. FEMS
Microbiol Lett 1999, 176:91-96.
59. Fang W, Almeida RA, Oliver SP: Effects of lactoferrin and milk on
adherence of Streptococcus uberis to bovine mammary epithelial
cells. Am J Vet Res 2000, 61:275-279.
60. Chen CC, Cleary PP: Complete nucleotide sequence of the
streptococcal C5a peptidase gene of Streptococcus pyogenes.
J Biol Chem 1990, 265:3161-3167.
61. Hollingshead SK, Fischetti VA, Scott JR: Complete nucleotide
sequence of type 6 M protein of the group A Streptococcus.
Repetitive structure and membrane anchor. J Biol Chem 1986,
261:1677-1686.
62. Martin PR, Hoiby EA: Streptococcal serogroup A epidemic in
Norway 1987–1988. Scand J Infect Dis 1990, 22:421-429.
63. Cho KH, Caparon MG: Patterns of virulence gene expression
differ between biofilm and tissue communities of Streptococcus
pyogenes. Mol Microbiol 2005, 57:1545-1556.
64. Ward PN, Field TR, Ditcham WG, Maguin E, Leigh JA: Identification
and disruption of two discrete loci encoding hyaluronic acid
capsule biosynthesis genes hasA, hasB, and hasC in Streptococcus
uberis. Infect Immun 2001, 69:392-399.
65. Dougherty BA, Rijn I van de: Molecular characterization of hasA
from an operon required for hyaluronic acid synthesis in
group A streptococci. J Biol Chem 1994, 269:169-175.
66. Ashbaugh CD, Alberti S, Wessels MR: Molecular analysis of the
capsule gene region of group A Streptococcus: the hasAB
genes are sufficient for capsule expression. J Bacteriol 1998,
180:4955-4959.
67. Field TR, Ward PN, Pedersen LH, Leigh JA: The hyaluronic acid
capsule of Streptococcus uberis is not required for the development
of infection and clinical mastitis. Infect Immun 2003,
71:132-139.
68. Rosey EL, Lincoln RA, Ward PN, Yancey RJ Jr, Leigh JA: PauA: a
novel plasminogen activator from Streptococcus uberis. FEMS
Microbiol Lett 1999, 178:27-33.
69. Ward PN, Leigh JA: Characterization of PauB, a novel broadspectrum
plasminogen activator from Streptococcus uberis. J
Bacteriol 2002, 184:119-125.
70. Malke H, Steiner K, Gase K, Frank C: Expression and regulation
of the streptokinase gene. Methods 2000, 21:111-124.
71. Mechold U, Steiner K, Vettermann S, Malke H: Genetic organization
of the streptokinase region of the Streptococcus equisimilis
H46A chromosome. Mol Gen Genet 1993, 241:129-140.
72. Canchaya C, Desiere F, McShan WM, Ferretti JJ, Parkhill J, Brussow
H: Genome analysis of an inducible prophage and prophage
remnants integrated in the Streptococcus pyogenes strain
SF370. Virology 2002, 302:245-258.
73. Banks DJ, Porcella SF, Barbian KD, Beres SB, Philips LE, Voyich JM,
DeLeo |
|---|
Data sourced from Thomson Reuters' Web of Knowledge Request changes to a record Repository Staff Only: item control page
|