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Understanding the physiological roles of polyhydroxybutyrate (PHB) in Rhodospirillum rubrum S1 under aerobic chemoheterotrophic conditions

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Abstract

Polyhydroxybutyrate (PHB) is an important biopolymer accumulated by bacteria and associated with cell survival and stress response. Here, we make two surprising findings in the PHB-accumulating species Rhodospirillum rubrum S1. We first show that the presence of PHB promotes the increased assimilation of acetate preferentially into biomass rather than PHB. When R. rubrum is supplied with 13C-acetate as a PHB precursor, 83.5 % of the carbon in PHB comes from acetate. However, only 15 % of the acetate ends up in PHB with the remainder assimilated as bacterial biomass. The PHB-negative mutant of R. rubrum assimilates 2-fold less acetate into biomass compared to the wild-type strain. Acetate assimilation proceeds via the ethylmalonyl-CoA pathway with (R)-3-hydroxybutyrate as a common intermediate with the PHB pathway. Secondly, we show that R. rubrum cells accumulating PHB have reduced ribulose 1,5-bisphosphate carboxylase (RuBisCO) activity. RuBisCO activity reduces 5-fold over a 36-h period after the onset of PHB. In contrast, a PHB-negative mutant maintains the same level of RuBisCO activity over the growth period. Since RuBisCO controls the redox potential in R. rubrum, PHB likely replaces RuBisCO in this role. R. rubrum is the first bacterium found to express RuBisCO under aerobic chemoheterotrophic conditions.

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Authors and Affiliations

  1. UCD Earth Institute, O’Brien Centre for Science, University College Dublin, Belfield, Dublin 4, Ireland

    Tanja Narancic, Elisa Scollica & Kevin E. O’Connor

  2. School of Biomolecular and Biomedical Science, University College Dublin, Belfield, Dublin 4, Ireland

    Tanja Narancic, Elisa Scollica, Cormac Murphy & Kevin E. O’Connor

  3. NovaUCD, Belfield Innovation Park, University College Dublin, Bioplastech Ltd., Belfield, Dublin 4, Ireland

    Shane T. Kenny

  4. Institute of Food and Health and Conway Institute, University College Dublin, Belfield, Dublin 4, Ireland

    Helena Gibbons, Eibhlin Carr & Lorraine Brennan

  5. School of Biomolecular and Biomedical Sciences, Conway, University College Dublin, Belfield, Dublin 4, Ireland

    Gerard Cagney & Kieran Wynne

  6. Institut für Molekulare Mikrobiologie und Biotechnologie, Westfälische Wilhelms-Universität, Münster, Germany

    Matthias Raberg, Daniel Heinrich & Alexander Steinbüchel

  7. Environmental Sciences Department, King Abdulaziz University, Jeddah, Saudi Arabia

    Alexander Steinbüchel

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  1. Tanja Narancic
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  2. Elisa Scollica
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  12. Alexander Steinbüchel
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Correspondence to Kevin E. O’Connor.

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This article does not contain any studies with human participants or animals performed by any of the authors.

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This work was funded by the European Commission’s The Seventh Framework Programme project SYNPOL (311815).

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The authors declare that they have no conflict of interest.

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Tanja Narancic and Elisa Scollica contributed equally to this work.

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Narancic, T., Scollica, E., Kenny, S.T. et al. Understanding the physiological roles of polyhydroxybutyrate (PHB) in Rhodospirillum rubrum S1 under aerobic chemoheterotrophic conditions. Appl Microbiol Biotechnol 100, 8901–8912 (2016). https://doi.org/10.1007/s00253-016-7711-5

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