Biofilm formation and cellulose expression by Bordetella avium 197N, the causative agent of bordetellosis in birds and an opportunistic respiratory pathogen in humans

Kimberley McLaughlin, Ayorinde O. Folorunso, Yusuf Y. Deeni, Dona Foster, Oksana Gorbatiuk, Simona M. Hapca, Corinna Immoor, Anna Koza, Ibrahim Mohammed, Olena Moshynets, Sergii Rogalsky, Kamil Zawadzki, Andrew J. Spiers

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    Abstract

    Although bacterial cellulose synthase (bcs) operons are widespread within the Proteobacteria phylum, subunits required for the partial-acetylation of the polymer appear to be restricted to a few γ-group soil, plant-associated and phytopathogenic pseudomonads, including Pseudomonas fluorescens SBW25 and several Pseudomonas syringae pathovars. However, a bcs operon with acetylation subunits has also been annotated in the unrelated β-group respiratory pathogen, Bordetella avium 197N. Our comparison of subunit protein sequences and GC content analyses confirms the close similarity between the B. avium 197N and pseudomonad operons and suggests that, in both cases, the cellulose synthase and acetylation subunits were acquired as a single unit. Using static liquid microcosms, we can confirm that B. avium 197N expresses low levels of cellulose in air–liquid interface biofilms and that biofilm strength and attachment levels could be increased by elevating c-di-GMP levels like the pseudomonads, but cellulose was not required for biofilm formation itself. The finding that B. avium 197N is capable of producing cellulose from a highly-conserved, but relatively uncommon bcs operon raises the question of what functional role this modified polymer plays during the infection of the upper respiratory tract or survival between hosts, and what environmental signals control its production.
    Original languageEnglish
    Pages (from-to)419–430
    Number of pages12
    JournalResearch in Microbiology
    Volume168
    Issue number5
    Early online date26 Jan 2017
    DOIs
    Publication statusPublished - Jun 2017

    Fingerprint

    Bordetella avium
    Operon
    Biofilms
    Cellulose
    Birds
    Acetylation
    Polymers
    Pseudomonas syringae
    Proteobacteria
    Pseudomonas fluorescens
    Protein Subunits
    Base Composition
    Respiratory Tract Infections
    Soil
    Survival
    cellulose synthase

    Cite this

    McLaughlin, Kimberley ; Folorunso, Ayorinde O. ; Deeni, Yusuf Y. ; Foster, Dona ; Gorbatiuk, Oksana ; Hapca, Simona M. ; Immoor, Corinna ; Koza, Anna ; Mohammed, Ibrahim ; Moshynets, Olena ; Rogalsky, Sergii ; Zawadzki, Kamil ; Spiers, Andrew J. / Biofilm formation and cellulose expression by Bordetella avium 197N, the causative agent of bordetellosis in birds and an opportunistic respiratory pathogen in humans. In: Research in Microbiology. 2017 ; Vol. 168, No. 5. pp. 419–430.
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    abstract = "Although bacterial cellulose synthase (bcs) operons are widespread within the Proteobacteria phylum, subunits required for the partial-acetylation of the polymer appear to be restricted to a few γ-group soil, plant-associated and phytopathogenic pseudomonads, including Pseudomonas fluorescens SBW25 and several Pseudomonas syringae pathovars. However, a bcs operon with acetylation subunits has also been annotated in the unrelated β-group respiratory pathogen, Bordetella avium 197N. Our comparison of subunit protein sequences and GC content analyses confirms the close similarity between the B. avium 197N and pseudomonad operons and suggests that, in both cases, the cellulose synthase and acetylation subunits were acquired as a single unit. Using static liquid microcosms, we can confirm that B. avium 197N expresses low levels of cellulose in air–liquid interface biofilms and that biofilm strength and attachment levels could be increased by elevating c-di-GMP levels like the pseudomonads, but cellulose was not required for biofilm formation itself. The finding that B. avium 197N is capable of producing cellulose from a highly-conserved, but relatively uncommon bcs operon raises the question of what functional role this modified polymer plays during the infection of the upper respiratory tract or survival between hosts, and what environmental signals control its production.",
    author = "Kimberley McLaughlin and Folorunso, {Ayorinde O.} and Deeni, {Yusuf Y.} and Dona Foster and Oksana Gorbatiuk and Hapca, {Simona M.} and Corinna Immoor and Anna Koza and Ibrahim Mohammed and Olena Moshynets and Sergii Rogalsky and Kamil Zawadzki and Spiers, {Andrew J.}",
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    McLaughlin, K, Folorunso, AO, Deeni, YY, Foster, D, Gorbatiuk, O, Hapca, SM, Immoor, C, Koza, A, Mohammed, I, Moshynets, O, Rogalsky, S, Zawadzki, K & Spiers, AJ 2017, 'Biofilm formation and cellulose expression by Bordetella avium 197N, the causative agent of bordetellosis in birds and an opportunistic respiratory pathogen in humans', Research in Microbiology, vol. 168, no. 5, pp. 419–430. https://doi.org/10.1016/j.resmic.2017.01.002

    Biofilm formation and cellulose expression by Bordetella avium 197N, the causative agent of bordetellosis in birds and an opportunistic respiratory pathogen in humans. / McLaughlin, Kimberley; Folorunso, Ayorinde O.; Deeni, Yusuf Y.; Foster, Dona; Gorbatiuk, Oksana; Hapca, Simona M.; Immoor, Corinna; Koza, Anna; Mohammed, Ibrahim; Moshynets, Olena; Rogalsky, Sergii; Zawadzki, Kamil; Spiers, Andrew J.

    In: Research in Microbiology, Vol. 168, No. 5, 06.2017, p. 419–430.

    Research output: Contribution to journalArticle

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    T1 - Biofilm formation and cellulose expression by Bordetella avium 197N, the causative agent of bordetellosis in birds and an opportunistic respiratory pathogen in humans

    AU - McLaughlin, Kimberley

    AU - Folorunso, Ayorinde O.

    AU - Deeni, Yusuf Y.

    AU - Foster, Dona

    AU - Gorbatiuk, Oksana

    AU - Hapca, Simona M.

    AU - Immoor, Corinna

    AU - Koza, Anna

    AU - Mohammed, Ibrahim

    AU - Moshynets, Olena

    AU - Rogalsky, Sergii

    AU - Zawadzki, Kamil

    AU - Spiers, Andrew J.

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    N2 - Although bacterial cellulose synthase (bcs) operons are widespread within the Proteobacteria phylum, subunits required for the partial-acetylation of the polymer appear to be restricted to a few γ-group soil, plant-associated and phytopathogenic pseudomonads, including Pseudomonas fluorescens SBW25 and several Pseudomonas syringae pathovars. However, a bcs operon with acetylation subunits has also been annotated in the unrelated β-group respiratory pathogen, Bordetella avium 197N. Our comparison of subunit protein sequences and GC content analyses confirms the close similarity between the B. avium 197N and pseudomonad operons and suggests that, in both cases, the cellulose synthase and acetylation subunits were acquired as a single unit. Using static liquid microcosms, we can confirm that B. avium 197N expresses low levels of cellulose in air–liquid interface biofilms and that biofilm strength and attachment levels could be increased by elevating c-di-GMP levels like the pseudomonads, but cellulose was not required for biofilm formation itself. The finding that B. avium 197N is capable of producing cellulose from a highly-conserved, but relatively uncommon bcs operon raises the question of what functional role this modified polymer plays during the infection of the upper respiratory tract or survival between hosts, and what environmental signals control its production.

    AB - Although bacterial cellulose synthase (bcs) operons are widespread within the Proteobacteria phylum, subunits required for the partial-acetylation of the polymer appear to be restricted to a few γ-group soil, plant-associated and phytopathogenic pseudomonads, including Pseudomonas fluorescens SBW25 and several Pseudomonas syringae pathovars. However, a bcs operon with acetylation subunits has also been annotated in the unrelated β-group respiratory pathogen, Bordetella avium 197N. Our comparison of subunit protein sequences and GC content analyses confirms the close similarity between the B. avium 197N and pseudomonad operons and suggests that, in both cases, the cellulose synthase and acetylation subunits were acquired as a single unit. Using static liquid microcosms, we can confirm that B. avium 197N expresses low levels of cellulose in air–liquid interface biofilms and that biofilm strength and attachment levels could be increased by elevating c-di-GMP levels like the pseudomonads, but cellulose was not required for biofilm formation itself. The finding that B. avium 197N is capable of producing cellulose from a highly-conserved, but relatively uncommon bcs operon raises the question of what functional role this modified polymer plays during the infection of the upper respiratory tract or survival between hosts, and what environmental signals control its production.

    U2 - 10.1016/j.resmic.2017.01.002

    DO - 10.1016/j.resmic.2017.01.002

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