Lose to win: marT pseudogenization in Salmonella enterica serovar Typhi contributed to the surV-dependent survival to H2O2, and inside human macrophage-like cells

A. P. Ortega, N. A. Villagra, I. M. Urrutia, L. M. Valenzuela, A. Talamilla-Espinoza, A. A. Hidalgo, P. I. Rodas, F. Gil, I. L. Calderón, D. Paredes-Sabja, G. C. Mora, J. A. Fuentes

Resultado de la investigación: Research - revisión exhaustivaArticle

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Resumen

The difference in host range between Salmonella enterica serovar Typhimurium (S. Typhimurium) and Salmonella enterica serovar Typhi (S. Typhi) can be partially attributed to the gain of functions, to the loss of functions (i.e. pseudogenization), or to a combination of both processes. As previously reported, the loss of functions by pseudogenization may play a role in bacterial evolution, especially in host-restricted pathogens such as S. Typhi. The marT-fidL operon, located at the SPI-3, encodes the MarT transcriptional regulator and a hypothetical protein (i.e. FidL) with no significant similarities to known proteins, respectively. Even though predicted S. Typhimurium FidL exhibit 99.4% identity with S. Typhi FidL, marT has been annotated as a pseudogene in S. Typhi. In this work, we found that S. Typhi expressing S. Typhimurium marT-fidL exhibited an increased accumulation of reactive oxygen species (ROS), leading to a decreased survival in presence of H2O2. Moreover, we found that that the presence of a functional copy of S. Typhimurium marT-fidL in S. Typhi resulted in a repression of surV (STY4039), an ORF found in the S. Typhi SPI-3 but absent from S. Typhimurium SPI-3, that contribute to the resistance to H2O2 by decreasing the accumulation of ROS. Finally, we observed that the presence of S. Typhimurium marT-fidL in S. Typhi negatively affected the survival inside macrophage-like cells, but not in epithelial cells, after 24 h post infection. Therefore, this work provides evidence arguing that marT pseudogenization in Salmonella Typhi contributed to the surV-dependent survival against H2O2, and inside human macrophage-like cells. This is a good example of how the loss of functions (marT pseudogenization) and the gain of functions (presence of surV) might contribute to phenotypic changes improving virulence.

IdiomaEnglish
Páginas111-121
Número de páginas11
PublicaciónInfection, Genetics and Evolution
Volumen45
DOI
EstadoPublished - 1 nov 2016

Huella dactilar

Salmonella Typhi
serotypes
macrophages
cells
Salmonella typhi
Macrophages
Survival
Serogroup
loss
salmonella
protein
reactive oxygen species
proteins
Reactive Oxygen Species
Proteins
host range
virulence
pathogen
infection
repression

Keywords

    ASJC Scopus subject areas

    • Microbiology
    • Ecology, Evolution, Behavior and Systematics
    • Molecular Biology
    • Genetics
    • Microbiology (medical)
    • Infectious Diseases

    Citar esto

    @article{86df4e605d0c4ad0815e6dc21ad47c88,
    title = "Lose to win: marT pseudogenization in Salmonella enterica serovar Typhi contributed to the surV-dependent survival to H2O2, and inside human macrophage-like cells",
    abstract = "The difference in host range between Salmonella enterica serovar Typhimurium (S. Typhimurium) and Salmonella enterica serovar Typhi (S. Typhi) can be partially attributed to the gain of functions, to the loss of functions (i.e. pseudogenization), or to a combination of both processes. As previously reported, the loss of functions by pseudogenization may play a role in bacterial evolution, especially in host-restricted pathogens such as S. Typhi. The marT-fidL operon, located at the SPI-3, encodes the MarT transcriptional regulator and a hypothetical protein (i.e. FidL) with no significant similarities to known proteins, respectively. Even though predicted S. Typhimurium FidL exhibit 99.4% identity with S. Typhi FidL, marT has been annotated as a pseudogene in S. Typhi. In this work, we found that S. Typhi expressing S. Typhimurium marT-fidL exhibited an increased accumulation of reactive oxygen species (ROS), leading to a decreased survival in presence of H2O2. Moreover, we found that that the presence of a functional copy of S. Typhimurium marT-fidL in S. Typhi resulted in a repression of surV (STY4039), an ORF found in the S. Typhi SPI-3 but absent from S. Typhimurium SPI-3, that contribute to the resistance to H2O2 by decreasing the accumulation of ROS. Finally, we observed that the presence of S. Typhimurium marT-fidL in S. Typhi negatively affected the survival inside macrophage-like cells, but not in epithelial cells, after 24 h post infection. Therefore, this work provides evidence arguing that marT pseudogenization in Salmonella Typhi contributed to the surV-dependent survival against H2O2, and inside human macrophage-like cells. This is a good example of how the loss of functions (marT pseudogenization) and the gain of functions (presence of surV) might contribute to phenotypic changes improving virulence.",
    keywords = "HO resistance, Macrophage survival, marT, Pseudogene, Salmonella, surV",
    author = "Ortega, {A. P.} and Villagra, {N. A.} and Urrutia, {I. M.} and Valenzuela, {L. M.} and A. Talamilla-Espinoza and Hidalgo, {A. A.} and Rodas, {P. I.} and F. Gil and Calderón, {I. L.} and D. Paredes-Sabja and Mora, {G. C.} and Fuentes, {J. A.}",
    year = "2016",
    month = "11",
    doi = "10.1016/j.meegid.2016.08.029",
    volume = "45",
    pages = "111--121",
    journal = "Infection, Genetics and Evolution",
    issn = "1567-1348",
    publisher = "Elsevier",

    }

    Lose to win : marT pseudogenization in Salmonella enterica serovar Typhi contributed to the surV-dependent survival to H2O2, and inside human macrophage-like cells. / Ortega, A. P.; Villagra, N. A.; Urrutia, I. M.; Valenzuela, L. M.; Talamilla-Espinoza, A.; Hidalgo, A. A.; Rodas, P. I.; Gil, F.; Calderón, I. L.; Paredes-Sabja, D.; Mora, G. C.; Fuentes, J. A.

    En: Infection, Genetics and Evolution, Vol. 45, 01.11.2016, p. 111-121.

    Resultado de la investigación: Research - revisión exhaustivaArticle

    TY - JOUR

    T1 - Lose to win

    T2 - Infection, Genetics and Evolution

    AU - Ortega,A. P.

    AU - Villagra,N. A.

    AU - Urrutia,I. M.

    AU - Valenzuela,L. M.

    AU - Talamilla-Espinoza,A.

    AU - Hidalgo,A. A.

    AU - Rodas,P. I.

    AU - Gil,F.

    AU - Calderón,I. L.

    AU - Paredes-Sabja,D.

    AU - Mora,G. C.

    AU - Fuentes,J. A.

    PY - 2016/11/1

    Y1 - 2016/11/1

    N2 - The difference in host range between Salmonella enterica serovar Typhimurium (S. Typhimurium) and Salmonella enterica serovar Typhi (S. Typhi) can be partially attributed to the gain of functions, to the loss of functions (i.e. pseudogenization), or to a combination of both processes. As previously reported, the loss of functions by pseudogenization may play a role in bacterial evolution, especially in host-restricted pathogens such as S. Typhi. The marT-fidL operon, located at the SPI-3, encodes the MarT transcriptional regulator and a hypothetical protein (i.e. FidL) with no significant similarities to known proteins, respectively. Even though predicted S. Typhimurium FidL exhibit 99.4% identity with S. Typhi FidL, marT has been annotated as a pseudogene in S. Typhi. In this work, we found that S. Typhi expressing S. Typhimurium marT-fidL exhibited an increased accumulation of reactive oxygen species (ROS), leading to a decreased survival in presence of H2O2. Moreover, we found that that the presence of a functional copy of S. Typhimurium marT-fidL in S. Typhi resulted in a repression of surV (STY4039), an ORF found in the S. Typhi SPI-3 but absent from S. Typhimurium SPI-3, that contribute to the resistance to H2O2 by decreasing the accumulation of ROS. Finally, we observed that the presence of S. Typhimurium marT-fidL in S. Typhi negatively affected the survival inside macrophage-like cells, but not in epithelial cells, after 24 h post infection. Therefore, this work provides evidence arguing that marT pseudogenization in Salmonella Typhi contributed to the surV-dependent survival against H2O2, and inside human macrophage-like cells. This is a good example of how the loss of functions (marT pseudogenization) and the gain of functions (presence of surV) might contribute to phenotypic changes improving virulence.

    AB - The difference in host range between Salmonella enterica serovar Typhimurium (S. Typhimurium) and Salmonella enterica serovar Typhi (S. Typhi) can be partially attributed to the gain of functions, to the loss of functions (i.e. pseudogenization), or to a combination of both processes. As previously reported, the loss of functions by pseudogenization may play a role in bacterial evolution, especially in host-restricted pathogens such as S. Typhi. The marT-fidL operon, located at the SPI-3, encodes the MarT transcriptional regulator and a hypothetical protein (i.e. FidL) with no significant similarities to known proteins, respectively. Even though predicted S. Typhimurium FidL exhibit 99.4% identity with S. Typhi FidL, marT has been annotated as a pseudogene in S. Typhi. In this work, we found that S. Typhi expressing S. Typhimurium marT-fidL exhibited an increased accumulation of reactive oxygen species (ROS), leading to a decreased survival in presence of H2O2. Moreover, we found that that the presence of a functional copy of S. Typhimurium marT-fidL in S. Typhi resulted in a repression of surV (STY4039), an ORF found in the S. Typhi SPI-3 but absent from S. Typhimurium SPI-3, that contribute to the resistance to H2O2 by decreasing the accumulation of ROS. Finally, we observed that the presence of S. Typhimurium marT-fidL in S. Typhi negatively affected the survival inside macrophage-like cells, but not in epithelial cells, after 24 h post infection. Therefore, this work provides evidence arguing that marT pseudogenization in Salmonella Typhi contributed to the surV-dependent survival against H2O2, and inside human macrophage-like cells. This is a good example of how the loss of functions (marT pseudogenization) and the gain of functions (presence of surV) might contribute to phenotypic changes improving virulence.

    KW - HO resistance

    KW - Macrophage survival

    KW - marT

    KW - Pseudogene

    KW - Salmonella

    KW - surV

    UR - http://www.scopus.com/inward/record.url?scp=84984662466&partnerID=8YFLogxK

    U2 - 10.1016/j.meegid.2016.08.029

    DO - 10.1016/j.meegid.2016.08.029

    M3 - Article

    VL - 45

    SP - 111

    EP - 121

    JO - Infection, Genetics and Evolution

    JF - Infection, Genetics and Evolution

    SN - 1567-1348

    ER -