Genome degradation in Brucella ovis corresponds with narrowing of its host range and tissue tropism

Renee M. Tsolis; Rekha Seshadri; Renato L. Santos; Felix J. Sangari; Juan M. García Lobo; Maarten F. de Jong; Qinghu Ren; Garry Myers; Lauren M. Brinkac; William C. Nelson; Robert T. DeBoy; Samuel Angiuoli; Hoda Khouri; George Dimitrov; Jeffrey R. Robinson; Stephanie Mulligan; Richard L. Walker; Philip E. Elzer; Karl A. Hassan; Ian T. Paulsen

doi:10.1371/journal.pone.0005519

Genome degradation in Brucella ovis corresponds with narrowing of its host range and tissue tropism

Renee M. Tsolis^*, Rekha Seshadri, Renato L. Santos, Felix J. Sangari, Juan M. García Lobo, Maarten F. de Jong, Qinghu Ren, Garry Myers, Lauren M. Brinkac, William C. Nelson, Robert T. DeBoy, Samuel Angiuoli, Hoda Khouri, George Dimitrov, Jeffrey R. Robinson, Stephanie Mulligan, Richard L. Walker, Philip E. Elzer, Karl A. Hassan, Ian T. Paulsen

^*Corresponding author for this work

Research output: Contribution to journal › Article › peer-review

96 Citations (Scopus)

Abstract

Brucella ovis is a veterinary pathogen associated with epididymitis in sheep. Despite its genetic similarity to the zoonotic pathogens B. abortus, B. melitensis and B. suis, B. ovis does not cause zoonotic disease. Genomic analysis of the type strain ATCC25840 revealed a high percentage of pseudogenes and increased numbers of transposable elements compared to the zoonotic Brucella species, suggesting that genome degradation has occurred concomitant with narrowing of the host range of B. ovis. The absence of genomic island 2, encoding functions required for lipopolysaccharide biosynthesis, as well as inactivation of genes encoding urease, nutrient uptake and utilization, and outer membrane proteins may be factors contributing to the avirulence of B. ovis for humans. A 26.5 kb region of B. ovis ATCC25840 Chromosome II was absent from all the sequenced human pathogenic Brucella genomes, but was present in all of 17 B. ovis isolates tested and in three B. ceti isolates, suggesting that this DNA region may be of use for differentiating B. ovis from other Brucella spp. This is the first genomic analysis of a non-zoonotic Brucella species. The results suggest that inactivation of genes involved in nutrient acquisition and utilization, cell envelope structure and urease may have played a role in narrowing of the tissue tropism and host range of B. ovis.

Original language	English
Article number	e5519
Pages (from-to)	1-9
Number of pages	9
Journal	PLoS ONE
Volume	4
Issue number	5
DOIs	https://doi.org/10.1371/journal.pone.0005519
Publication status	Published - 13 May 2009

Access to Document

10.1371/journal.pone.0005519

Cite this

Tsolis, R. M., Seshadri, R., Santos, R. L., Sangari, F. J., García Lobo, J. M., de Jong, M. F., Ren, Q., Myers, G., Brinkac, L. M., Nelson, W. C., DeBoy, R. T., Angiuoli, S., Khouri, H., Dimitrov, G., Robinson, J. R., Mulligan, S., Walker, R. L., Elzer, P. E., Hassan, K. A., & Paulsen, I. T. (2009). Genome degradation in Brucella ovis corresponds with narrowing of its host range and tissue tropism. PLoS ONE, 4(5), 1-9. [e5519]. https://doi.org/10.1371/journal.pone.0005519

@article{4a978b9df2f04a408c53bc3e57cd25fc,

title = "Genome degradation in Brucella ovis corresponds with narrowing of its host range and tissue tropism",

abstract = "Brucella ovis is a veterinary pathogen associated with epididymitis in sheep. Despite its genetic similarity to the zoonotic pathogens B. abortus, B. melitensis and B. suis, B. ovis does not cause zoonotic disease. Genomic analysis of the type strain ATCC25840 revealed a high percentage of pseudogenes and increased numbers of transposable elements compared to the zoonotic Brucella species, suggesting that genome degradation has occurred concomitant with narrowing of the host range of B. ovis. The absence of genomic island 2, encoding functions required for lipopolysaccharide biosynthesis, as well as inactivation of genes encoding urease, nutrient uptake and utilization, and outer membrane proteins may be factors contributing to the avirulence of B. ovis for humans. A 26.5 kb region of B. ovis ATCC25840 Chromosome II was absent from all the sequenced human pathogenic Brucella genomes, but was present in all of 17 B. ovis isolates tested and in three B. ceti isolates, suggesting that this DNA region may be of use for differentiating B. ovis from other Brucella spp. This is the first genomic analysis of a non-zoonotic Brucella species. The results suggest that inactivation of genes involved in nutrient acquisition and utilization, cell envelope structure and urease may have played a role in narrowing of the tissue tropism and host range of B. ovis.",

author = "Tsolis, {Renee M.} and Rekha Seshadri and Santos, {Renato L.} and Sangari, {Felix J.} and {Garc{\'i}a Lobo}, {Juan M.} and {de Jong}, {Maarten F.} and Qinghu Ren and Garry Myers and Brinkac, {Lauren M.} and Nelson, {William C.} and DeBoy, {Robert T.} and Samuel Angiuoli and Hoda Khouri and George Dimitrov and Robinson, {Jeffrey R.} and Stephanie Mulligan and Walker, {Richard L.} and Elzer, {Philip E.} and Hassan, {Karl A.} and Paulsen, {Ian T.}",

year = "2009",

month = may,

day = "13",

doi = "10.1371/journal.pone.0005519",

language = "English",

volume = "4",

pages = "1--9",

journal = "PLoS ONE",

issn = "1932-6203",

publisher = "Public Library of Science",

number = "5",

}

Tsolis, RM, Seshadri, R, Santos, RL, Sangari, FJ, García Lobo, JM, de Jong, MF, Ren, Q, Myers, G, Brinkac, LM, Nelson, WC, DeBoy, RT, Angiuoli, S, Khouri, H, Dimitrov, G, Robinson, JR, Mulligan, S, Walker, RL, Elzer, PE, Hassan, KA & Paulsen, IT 2009, 'Genome degradation in Brucella ovis corresponds with narrowing of its host range and tissue tropism', PLoS ONE, vol. 4, no. 5, e5519, pp. 1-9. https://doi.org/10.1371/journal.pone.0005519

TY - JOUR

T1 - Genome degradation in Brucella ovis corresponds with narrowing of its host range and tissue tropism

AU - Tsolis, Renee M.

AU - Seshadri, Rekha

AU - Santos, Renato L.

AU - Sangari, Felix J.

AU - García Lobo, Juan M.

AU - de Jong, Maarten F.

AU - Ren, Qinghu

AU - Myers, Garry

AU - Brinkac, Lauren M.

AU - Nelson, William C.

AU - DeBoy, Robert T.

AU - Angiuoli, Samuel

AU - Khouri, Hoda

AU - Dimitrov, George

AU - Robinson, Jeffrey R.

AU - Mulligan, Stephanie

AU - Walker, Richard L.

AU - Elzer, Philip E.

AU - Hassan, Karl A.

AU - Paulsen, Ian T.

PY - 2009/5/13

Y1 - 2009/5/13

N2 - Brucella ovis is a veterinary pathogen associated with epididymitis in sheep. Despite its genetic similarity to the zoonotic pathogens B. abortus, B. melitensis and B. suis, B. ovis does not cause zoonotic disease. Genomic analysis of the type strain ATCC25840 revealed a high percentage of pseudogenes and increased numbers of transposable elements compared to the zoonotic Brucella species, suggesting that genome degradation has occurred concomitant with narrowing of the host range of B. ovis. The absence of genomic island 2, encoding functions required for lipopolysaccharide biosynthesis, as well as inactivation of genes encoding urease, nutrient uptake and utilization, and outer membrane proteins may be factors contributing to the avirulence of B. ovis for humans. A 26.5 kb region of B. ovis ATCC25840 Chromosome II was absent from all the sequenced human pathogenic Brucella genomes, but was present in all of 17 B. ovis isolates tested and in three B. ceti isolates, suggesting that this DNA region may be of use for differentiating B. ovis from other Brucella spp. This is the first genomic analysis of a non-zoonotic Brucella species. The results suggest that inactivation of genes involved in nutrient acquisition and utilization, cell envelope structure and urease may have played a role in narrowing of the tissue tropism and host range of B. ovis.

AB - Brucella ovis is a veterinary pathogen associated with epididymitis in sheep. Despite its genetic similarity to the zoonotic pathogens B. abortus, B. melitensis and B. suis, B. ovis does not cause zoonotic disease. Genomic analysis of the type strain ATCC25840 revealed a high percentage of pseudogenes and increased numbers of transposable elements compared to the zoonotic Brucella species, suggesting that genome degradation has occurred concomitant with narrowing of the host range of B. ovis. The absence of genomic island 2, encoding functions required for lipopolysaccharide biosynthesis, as well as inactivation of genes encoding urease, nutrient uptake and utilization, and outer membrane proteins may be factors contributing to the avirulence of B. ovis for humans. A 26.5 kb region of B. ovis ATCC25840 Chromosome II was absent from all the sequenced human pathogenic Brucella genomes, but was present in all of 17 B. ovis isolates tested and in three B. ceti isolates, suggesting that this DNA region may be of use for differentiating B. ovis from other Brucella spp. This is the first genomic analysis of a non-zoonotic Brucella species. The results suggest that inactivation of genes involved in nutrient acquisition and utilization, cell envelope structure and urease may have played a role in narrowing of the tissue tropism and host range of B. ovis.

UR - http://www.scopus.com/inward/record.url?scp=65849486254&partnerID=8YFLogxK

U2 - 10.1371/journal.pone.0005519

DO - 10.1371/journal.pone.0005519

M3 - Article

C2 - 19436743

AN - SCOPUS:65849486254

SN - 1932-6203

VL - 4

SP - 1

EP - 9

JO - PLoS ONE

JF - PLoS ONE

IS - 5

M1 - e5519

ER -

Genome degradation in Brucella ovis corresponds with narrowing of its host range and tissue tropism

Abstract

Access to Document

Other files and links

Fingerprint

Cite this