Inactivation of phoPQ genes attenuates Salmonella Gallinarum biovar Gallinarum to susceptible chickens

Alves, Lucas Bocchini Rodrigues; Neto, Oliveiro Caetano de Freitas; Batista, Diego Felipe Alves; Barbosa, Fernanda de Oliveira; Rubio, Marcela da Silva; Souza, Andrei Itajahy Secundo de; Almeida, A. Bugalho de; Barrow, Paul; Berchieri, Ângelo

doi:10.1016/j.bjm.2017.09.006

Cited by 8 publications

(3 citation statements)

References 38 publications

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“…Choleraesuis, and S . Typhi attenuates virulence in chickens, pigs, and humans, respectively ( 59–61 ). Thus, we wondered whether the SsrB activation of ugtL is retained in S. enterica serovars with different host ranges.…”

Section: Resultsmentioning

confidence: 99%

Horizontally acquired regulatory gene activates ancestral regulatory system to promote Salmonella virulence

Choi

Groisman

2020

Nucleic Acids Research

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Horizontally acquired genes are typically regulated by ancestral regulators. This regulation enables expression of horizontally acquired genes to be coordinated with that of preexisting genes. Here, we report a singular example of the opposite regulation: a horizontally acquired gene that controls an ancestral regulator, thereby promoting bacterial virulence. We establish that the horizontally acquired regulatory gene ssrB is necessary to activate the ancestral regulatory system PhoP/PhoQ of Salmonella enterica serovar Typhimurium (S. Typhimurium) in mildly acidic pH, which S. Typhimurium experiences inside macrophages. SsrB promotes phoP transcription by binding upstream of the phoP promoter. SsrB also increases ugtL transcription by binding to the ugtL promoter region, where it overcomes gene silencing by the heat-stable nucleoid structuring protein H-NS, enhancing virulence. The largely non-pathogenic species S. bongori failed to activate PhoP/PhoQ in mildly acidic pH because it lacks both the ssrB gene and the SsrB binding site in the target promoter. Low Mg2+ activated PhoP/PhoQ in both S. bongori and ssrB-lacking S. Typhimurium, indicating that the SsrB requirement for PhoP/PhoQ activation is signal-dependent. By controlling the ancestral genome, horizontally acquired genes are responsible for more crucial abilities, including virulence, than currently thought.

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Section: Resultsmentioning

confidence: 99%

Horizontally acquired regulatory gene activates ancestral regulatory system to promote Salmonella virulence

Choi

Groisman

2020

Nucleic Acids Research

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“…In Salmonella serovars Typhimurium and Gallinarum, SPI-3 is located in the sel C tRNA locus with 17 kb size and approximately ten genes, such as sug R, rhu M, rmb A, mis L, fid L, mar T, sls A, cig R, mgt B and mgt C, that might play a role in virulence ( Blanc-Potard et al., 1999 ; Rodrigues Alves et al., 2018 ). The genes from this region, as mis L, are involved in the intestinal colonization, including both adhesion and invasion of epithelial cells ( Wang et al., 2018 ).…”

Section: Discussionmentioning

confidence: 99%

Genomic and Evolutionary Analysis of Salmonella enterica Serovar Kentucky Sequence Type 198 Isolated From Livestock In East Africa

Saraiva

Benevides

Silva

et al. 2022

Front. Cell. Infect. Microbiol.

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Since its emergence in the beginning of the 90’s, multidrug-resistant (MDR) Salmonella enterica subsp. enterica serovar Kentucky has become a significant public health problem, especially in East Africa. This study aimed to investigate the antimicrobial resistance profile and the genotypic relatedness of Salmonella Kentucky isolated from animal sources in Ethiopia and Kenya (n=19). We also investigated population evolutionary dynamics through phylogenetic and pangenome analyses with additional publicly available Salmonella Kentucky ST198 genomes (n=229). All the 19 sequenced Salmonella Kentucky isolates were identified as ST198. Among these isolates, the predominant genotypic antimicrobial resistance profile observed in ten (59.7%) isolates included the aac(3)-Id, aadA7, strA-strB, blaTEM-1B, sul1, and tet(A) genes, which mediated resistance to gentamicin, streptomycin/spectinomycin, streptomycin, ampicillin, sulfamethoxazole and tetracycline, respectively; and gyrA and parC mutations associated to ciprofloxacin resistance. Four isolates harbored plasmid types Incl1 and/or Col8282; two of them carried both plasmids. Salmonella Pathogenicity islands (SPI-1 to SPI-5) were highly conserved in the 19 sequenced Salmonella Kentucky isolates. Moreover, at least one Pathogenicity Island (SPI 1–4, SPI 9 or C63PI) was identified among the 229 public Salmonella Kentucky genomes. The phylogenetic analysis revealed that almost all Salmonella Kentucky ST198 isolates (17/19) stemmed from a single strain that has accumulated ciprofloxacin resistance-mediating mutations. A total of 8,104 different genes were identified in a heterogenic and still open Salmonella Kentucky ST198 pangenome. Considering the virulence factors and antimicrobial resistance genes detected in Salmonella Kentucky, the implications of this pathogen to public health and the epidemiological drivers for its dissemination must be investigated.

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“…The UgtL protein is highly conserved (�98% deduced shared amino acid sequence identity) in S. enterica serovars that, like serovar Typhimurium, infect a variety of warm-blooded animals and in which PhoP is required for virulence (Fig 7A). For instance, phoP inactivation in S. Gallinarum, S. Choleraesuis, and S. Typhi attenuates virulence in chickens, pigs, and humans, respectively [32][33][34].…”

Section: The Ugts Gene Is Narrowly Distributed In Non-typhoidal S Ent...mentioning

confidence: 99%

Differential synthesis of novel small protein times Salmonella virulence program

2022

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Gene organization in operons enables concerted transcription of functionally related genes and efficient control of cellular processes. Typically, an operon is transcribed as a polycistronic mRNA that is translated into corresponding proteins. Here, we identify a bicistronic operon transcribed as two mRNAs, yet only one allows translation of both genes. We establish that the novel gene ugtS forms an operon with virulence gene ugtL, an activator of the master virulence regulatory system PhoP/PhoQ in Salmonella enterica serovar Typhimurium. Only the longer ugtSugtL mRNA carries the ugtS ribosome binding site and therefore allows ugtS translation. Inside macrophages, the ugtSugtL mRNA species allowing translation of both genes is produced hours before that allowing translation solely of ugtL. The small protein UgtS controls the kinetics of PhoP phosphorylation by antagonizing UgtL activity, preventing premature activation of a critical virulence program. Moreover, S. enterica serovars that infect cold-blooded animals lack ugtS. Our results establish how foreign gene control of ancestral regulators enables pathogens to time their virulence programs.

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Inactivation of phoPQ genes attenuates Salmonella Gallinarum biovar Gallinarum to susceptible chickens

Cited by 8 publications

References 38 publications

Horizontally acquired regulatory gene activates ancestral regulatory system to promote Salmonella virulence

Horizontally acquired regulatory gene activates ancestral regulatory system to promote Salmonella virulence

Genomic and Evolutionary Analysis of Salmonella enterica Serovar Kentucky Sequence Type 198 Isolated From Livestock In East Africa

Differential synthesis of novel small protein times Salmonella virulence program

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