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Brucella ovis  is a non-zoonotic bacterium causing contagious epididymitis and other genital lesions in rams and responsible for significant economic losses in sheep-breeding areas. It is a naturally rough (without O-chains in the lipopolysaccharide)  Brucella  species whose virulence mechanisms have been less explored than those of zoonotic smooth brucellae (bearing O-chains that mask other outer membrane molecules). Considering the rough nature of  Brucella ovis , the influence of surface components other than O-chains on its biological properties may be greater than in smooth  Brucella  species. Here we describe the construction and characterization of the  mucR  deletion mutant of virulent  B. ovis  PA, which is defective in a transcriptional regulator, affecting surface properties and virulence in smooth brucellae. This mutant showed increased amounts of three proteins identified as HdeA (acid-activated chaperone), Omp25d (outer membrane protein undetectable in the parental strain), and BOV_A0299 (hypothetical protein of unknown function). This observation correlated with the enhanced transcription of the corresponding genes and constitutes the first report on this type of proteome alteration in  Brucella  Δ mucR  mutants. The upstream regions of the three genes contained AT rich domains with T-A steps described as binding sites for MucR in the  Brucella abortus  2308  babR  promoter (gene also upregulated in  B. ovis  Δ mucR ), which suggests that  hdeA, omp25d , and  BOV_A0299  expression could be repressed by MucR through a direct binding to their promoter regions. Relative quantification of transcripts of several other genes selected according to the transcriptome of smooth brucellae Δ mucR  mutants revealed not only similarities but also relevant differences among strains, such as those detected in flagellar and  virB  genes. Periplasmic HdeA has been related to the resistance of  B. abortus  to acidic pH, conditions encountered by  Brucella  inside phagocytes, but the deletion of  hdeA  in  B. ovis  PA and the Δ mucR  mutant did not modify any of the evaluated properties of these strains. The  B. ovis  PA Δ mucR  and Δ mucR Δ hdeA  mutants had defective  in vitro  growth and altered surface properties and architecture, exemplified by detectable amounts of Omp25d. Moreover, they showed virulence attenuation but established persistent splenic infection in mice, which encourages their evaluation as specifical attenuated vaccines against  B. ovis .

frontiers in veterinary science

The Transcriptional Regulator MucR, but Not Its Controlled Acid-Activated Chaperone HdeA, Is Essential for Virulence and Modulates Surface Architecture and Properties in Brucella ovis PA