Tags

Type your tag names separated by a space and hit enter

Regulatory Evolution of the phoH Ancestral Gene in Salmonella enterica Serovar Typhimurium.
J Bacteriol. 2022 May 17; 204(5):e0058521.JB

Abstract

One important event for the divergence of Salmonella from Escherichia coli was the acquisition by horizontal transfer of the Salmonella pathogenicity island 1 (SPI-1), containing genes required for the invasion of host cells by Salmonella. HilD is an AraC-like transcriptional regulator in SPI-1 that induces the expression of the SPI-1 and many other acquired virulence genes located in other genomic regions of Salmonella. Additionally, HilD has been shown to positively control the expression of some ancestral genes (also present in E. coli and other bacteria), including phoH. In this study, we determined that both the gain of HilD and cis-regulatory evolution led to the integration of the phoH gene into the HilD regulon. Our results indicate that a HilD-binding sequence was generated in the regulatory region of the S. enterica serovar Typhimurium phoH gene, which mediates the activation of promoter 1 of this gene under SPI-1-inducing conditions. Furthermore, we found that repression by H-NS, a histone-like protein, was also adapted on the S. Typhimurium phoH gene and that HilD activates the expression of this gene in part by antagonizing H-NS. Additionally, our results revealed that the expression of the S. Typhmurium phoH gene is also activated in response to low phosphate but independently of the PhoB/R two-component system, known to regulate the E. coli phoH gene in response to low phosphate. Thus, our results indicate that cis-regulatory evolution has played a role in the expansion of the HilD regulon and illustrate the phenomenon of differential regulation of ortholog genes. IMPORTANCE Two mechanisms mediating differentiation of bacteria are well known: acquisition of genes by horizontal transfer events and mutations in coding DNA sequences. In this study, we found that the phoH ancestral gene is differentially regulated between Salmonella Typhimurium and Escherichia coli, two closely related bacterial species. Our results indicate that this differential regulation was generated by mutations in the regulatory sequence of the S. Typhimurium phoH gene and by the acquisition by S. Typhimurium of foreign DNA encoding the transcriptional regulator HilD. Thus, our results, together with those from an increasing number of studies, indicate that cis-regulatory evolution can lead to the rewiring and reprogramming of transcriptional regulation, which also plays an important role in the divergence of bacteria through time.

Authors+Show Affiliations

Departamento de Microbiología Molecular, Instituto de Biotecnología, Universidad Nacional Autónoma de México, Cuernavaca, Morelos, Mexico.Unidad de Investigación en Medicina Experimental, Facultad de Medicina, Universidad Nacional Autónoma de México, Mexico City, Mexico.Unidad de Investigación Médica en Enfermedades Infecciosas y Parasitarias, Hospital de Pediatría, Centro Médico Nacional Siglo XXI, Instituto Mexicano del Seguro Social, Mexico City, Mexico.Departamento de Microbiología Molecular, Instituto de Biotecnología, Universidad Nacional Autónoma de México, Cuernavaca, Morelos, Mexico.

Pub Type(s)

Journal Article
Research Support, Non-U.S. Gov't

Language

eng

PubMed ID

35404111

Citation

Valdespino-Díaz, Marcos A., et al. "Regulatory Evolution of the phoH Ancestral Gene in Salmonella Enterica Serovar Typhimurium." Journal of Bacteriology, vol. 204, no. 5, 2022, pp. e0058521.
Valdespino-Díaz MA, Rosales-Reyes R, De la Cruz MA, et al. Regulatory Evolution of the phoH Ancestral Gene in Salmonella enterica Serovar Typhimurium. J Bacteriol. 2022;204(5):e0058521.
Valdespino-Díaz, M. A., Rosales-Reyes, R., De la Cruz, M. A., & Bustamante, V. H. (2022). Regulatory Evolution of the phoH Ancestral Gene in Salmonella enterica Serovar Typhimurium. Journal of Bacteriology, 204(5), e0058521. https://doi.org/10.1128/jb.00585-21
Valdespino-Díaz MA, et al. Regulatory Evolution of the phoH Ancestral Gene in Salmonella Enterica Serovar Typhimurium. J Bacteriol. 2022 May 17;204(5):e0058521. PubMed PMID: 35404111.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - Regulatory Evolution of the phoH Ancestral Gene in Salmonella enterica Serovar Typhimurium. AU - Valdespino-Díaz,Marcos A, AU - Rosales-Reyes,Roberto, AU - De la Cruz,Miguel A, AU - Bustamante,Víctor H, Y1 - 2022/04/11/ PY - 2022/10/11/pmc-release PY - 2022/4/12/pubmed PY - 2022/5/20/medline PY - 2022/4/11/entrez KW - AraC-like KW - Escherichia coli KW - H-NS KW - HilD KW - PhoB/R KW - SPI-1 KW - Salmonella KW - cis-regulatory KW - phoH KW - regulatory evolution SP - e0058521 EP - e0058521 JF - Journal of bacteriology JO - J Bacteriol VL - 204 IS - 5 N2 - One important event for the divergence of Salmonella from Escherichia coli was the acquisition by horizontal transfer of the Salmonella pathogenicity island 1 (SPI-1), containing genes required for the invasion of host cells by Salmonella. HilD is an AraC-like transcriptional regulator in SPI-1 that induces the expression of the SPI-1 and many other acquired virulence genes located in other genomic regions of Salmonella. Additionally, HilD has been shown to positively control the expression of some ancestral genes (also present in E. coli and other bacteria), including phoH. In this study, we determined that both the gain of HilD and cis-regulatory evolution led to the integration of the phoH gene into the HilD regulon. Our results indicate that a HilD-binding sequence was generated in the regulatory region of the S. enterica serovar Typhimurium phoH gene, which mediates the activation of promoter 1 of this gene under SPI-1-inducing conditions. Furthermore, we found that repression by H-NS, a histone-like protein, was also adapted on the S. Typhimurium phoH gene and that HilD activates the expression of this gene in part by antagonizing H-NS. Additionally, our results revealed that the expression of the S. Typhmurium phoH gene is also activated in response to low phosphate but independently of the PhoB/R two-component system, known to regulate the E. coli phoH gene in response to low phosphate. Thus, our results indicate that cis-regulatory evolution has played a role in the expansion of the HilD regulon and illustrate the phenomenon of differential regulation of ortholog genes. IMPORTANCE Two mechanisms mediating differentiation of bacteria are well known: acquisition of genes by horizontal transfer events and mutations in coding DNA sequences. In this study, we found that the phoH ancestral gene is differentially regulated between Salmonella Typhimurium and Escherichia coli, two closely related bacterial species. Our results indicate that this differential regulation was generated by mutations in the regulatory sequence of the S. Typhimurium phoH gene and by the acquisition by S. Typhimurium of foreign DNA encoding the transcriptional regulator HilD. Thus, our results, together with those from an increasing number of studies, indicate that cis-regulatory evolution can lead to the rewiring and reprogramming of transcriptional regulation, which also plays an important role in the divergence of bacteria through time. SN - 1098-5530 UR - https://www.unboundmedicine.com/medline/citation/35404111/Regulatory_Evolution_of_the_phoH_Ancestral_Gene_in_Salmonella_enterica_Serovar_Typhimurium_ DB - PRIME DP - Unbound Medicine ER -