Signal peptide etiquette during assembly of a complex respiratory enzyme

Martyn J. James, Sarah J. Coulthurst, Tracy Palmer, Frank Sargent (Lead / Corresponding author)

    Research output: Contribution to journalArticle

    12 Citations (Scopus)

    Abstract

    Salmonella enterica serovar Typhimurum is a Gram-negative pathogen capable of respiration with a number of terminal electron acceptors. Tetrathionate reductase is important for the infection process and is encoded by the ttrBCA operon where TtrA and TtrB are metallocofactor-containing proteins targeted to the periplasmic side of the membrane by two different Tat targeting peptides. In this work, the inter-relationship between these two signal peptides has been explored. Molecular genetics and biochemical approaches reveal that the processing of the TtrB Tat signal peptide is dependent on the successful assembly of its partner protein, TtrA. Inactivation of either the TtrA or the TtrB Tat targeting peptides individually was observed to have limited overall effects on assembly of the enzyme or on cellular tetrathionate reductase activity. However, inactivation of both signal peptides simultaneously was found to completely abolish physiological tetrathionate reductase activity. These data suggest both signals are normally active during assembly of the enzyme, and imply a code of conduct exists between the signal peptides where one can compensate for inactivity in the other. Since it appears likely that tetrathionate reductase presents itself for export as a multi-signal complex, these observations also have implications for the mechanism of the bacterial Tat translocase.

    Original languageEnglish
    Pages (from-to)400-414
    Number of pages15
    JournalMolecular Microbiology
    Volume90
    Issue number2
    DOIs
    Publication statusPublished - Oct 2013

    Fingerprint

    Protein Sorting Signals
    Enzymes
    Peptides
    Salmonella enterica
    Operon
    Molecular Biology
    Respiration
    Proteins
    Electrons
    Membranes
    tetrathionate reductase
    Infection

    Cite this

    @article{490c0f7bff0b40c4bd01a3a2cab064ee,
    title = "Signal peptide etiquette during assembly of a complex respiratory enzyme",
    abstract = "Salmonella enterica serovar Typhimurum is a Gram-negative pathogen capable of respiration with a number of terminal electron acceptors. Tetrathionate reductase is important for the infection process and is encoded by the ttrBCA operon where TtrA and TtrB are metallocofactor-containing proteins targeted to the periplasmic side of the membrane by two different Tat targeting peptides. In this work, the inter-relationship between these two signal peptides has been explored. Molecular genetics and biochemical approaches reveal that the processing of the TtrB Tat signal peptide is dependent on the successful assembly of its partner protein, TtrA. Inactivation of either the TtrA or the TtrB Tat targeting peptides individually was observed to have limited overall effects on assembly of the enzyme or on cellular tetrathionate reductase activity. However, inactivation of both signal peptides simultaneously was found to completely abolish physiological tetrathionate reductase activity. These data suggest both signals are normally active during assembly of the enzyme, and imply a code of conduct exists between the signal peptides where one can compensate for inactivity in the other. Since it appears likely that tetrathionate reductase presents itself for export as a multi-signal complex, these observations also have implications for the mechanism of the bacterial Tat translocase.",
    author = "James, {Martyn J.} and Coulthurst, {Sarah J.} and Tracy Palmer and Frank Sargent",
    note = "This article is protected by copyright. All rights reserved.",
    year = "2013",
    month = "10",
    doi = "10.1111/mmi.12373",
    language = "English",
    volume = "90",
    pages = "400--414",
    journal = "Molecular Microbiology",
    issn = "0950-382X",
    publisher = "Wiley",
    number = "2",

    }

    Signal peptide etiquette during assembly of a complex respiratory enzyme. / James, Martyn J.; Coulthurst, Sarah J.; Palmer, Tracy; Sargent, Frank (Lead / Corresponding author).

    In: Molecular Microbiology, Vol. 90, No. 2, 10.2013, p. 400-414.

    Research output: Contribution to journalArticle

    TY - JOUR

    T1 - Signal peptide etiquette during assembly of a complex respiratory enzyme

    AU - James, Martyn J.

    AU - Coulthurst, Sarah J.

    AU - Palmer, Tracy

    AU - Sargent, Frank

    N1 - This article is protected by copyright. All rights reserved.

    PY - 2013/10

    Y1 - 2013/10

    N2 - Salmonella enterica serovar Typhimurum is a Gram-negative pathogen capable of respiration with a number of terminal electron acceptors. Tetrathionate reductase is important for the infection process and is encoded by the ttrBCA operon where TtrA and TtrB are metallocofactor-containing proteins targeted to the periplasmic side of the membrane by two different Tat targeting peptides. In this work, the inter-relationship between these two signal peptides has been explored. Molecular genetics and biochemical approaches reveal that the processing of the TtrB Tat signal peptide is dependent on the successful assembly of its partner protein, TtrA. Inactivation of either the TtrA or the TtrB Tat targeting peptides individually was observed to have limited overall effects on assembly of the enzyme or on cellular tetrathionate reductase activity. However, inactivation of both signal peptides simultaneously was found to completely abolish physiological tetrathionate reductase activity. These data suggest both signals are normally active during assembly of the enzyme, and imply a code of conduct exists between the signal peptides where one can compensate for inactivity in the other. Since it appears likely that tetrathionate reductase presents itself for export as a multi-signal complex, these observations also have implications for the mechanism of the bacterial Tat translocase.

    AB - Salmonella enterica serovar Typhimurum is a Gram-negative pathogen capable of respiration with a number of terminal electron acceptors. Tetrathionate reductase is important for the infection process and is encoded by the ttrBCA operon where TtrA and TtrB are metallocofactor-containing proteins targeted to the periplasmic side of the membrane by two different Tat targeting peptides. In this work, the inter-relationship between these two signal peptides has been explored. Molecular genetics and biochemical approaches reveal that the processing of the TtrB Tat signal peptide is dependent on the successful assembly of its partner protein, TtrA. Inactivation of either the TtrA or the TtrB Tat targeting peptides individually was observed to have limited overall effects on assembly of the enzyme or on cellular tetrathionate reductase activity. However, inactivation of both signal peptides simultaneously was found to completely abolish physiological tetrathionate reductase activity. These data suggest both signals are normally active during assembly of the enzyme, and imply a code of conduct exists between the signal peptides where one can compensate for inactivity in the other. Since it appears likely that tetrathionate reductase presents itself for export as a multi-signal complex, these observations also have implications for the mechanism of the bacterial Tat translocase.

    U2 - 10.1111/mmi.12373

    DO - 10.1111/mmi.12373

    M3 - Article

    VL - 90

    SP - 400

    EP - 414

    JO - Molecular Microbiology

    JF - Molecular Microbiology

    SN - 0950-382X

    IS - 2

    ER -