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An oxygen reduction chain in the hyperthermophilic anaerobe Thermotoga maritima highlights horizontal gene transfer between Thermococcales and Thermotogales

Authors

  • Céline Le Fourn,

    1. Laboratoire Interactions et Modulateurs de Réponses – CNRS UPR3243 – IFR88, 31 chemin Joseph Aiguier, 13402 Marseille cedex 20, France.
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  • Gaël Brasseur,

    1. Laboratoire Interactions et Modulateurs de Réponses – CNRS UPR3243 – IFR88, 31 chemin Joseph Aiguier, 13402 Marseille cedex 20, France.
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  • Céline Brochier-Armanet,

    1. Université de Provence (Aix-Marseille I), Laboratoire de Chimie Bactérienne – CNRS UPR9043 – IFR88, 31 chemin Joseph Aiguier, 13402 Marseille cedex 20, France.
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  • Laetitia Pieulle,

    1. Laboratoire Interactions et Modulateurs de Réponses – CNRS UPR3243 – IFR88, 31 chemin Joseph Aiguier, 13402 Marseille cedex 20, France.
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  • Andrei Brioukhanov,

    1. Department of Microbiology, Biological Faculty, Lomonosov Moscow State University (MSU), 119991 Moscow, Russia.
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  • Bernard Ollivier,

    1. Laboratoire de Microbiologie, IFR BAIM – IRD, UMR D180, Universités de Provence et de la Méditerranée, 13288 Marseille cedex 09, France.
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  • Alain Dolla

    Corresponding author
    1. Laboratoire Interactions et Modulateurs de Réponses – CNRS UPR3243 – IFR88, 31 chemin Joseph Aiguier, 13402 Marseille cedex 20, France.
      E-mail dolla@ibsm.cnrs-mrs.fr; Tel. (+33) 491164149; Fax (+33) 491164540.
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E-mail dolla@ibsm.cnrs-mrs.fr; Tel. (+33) 491164149; Fax (+33) 491164540.

Summary

The hyperthermophile Thermotoga maritima, although strictly anaerobic, is able to grow in the presence of low amounts of O2. Here, we show that this bacterium consumes O2 via a three-partner chain involving an NADH oxidoreductase (NRO), a rubredoxin (Rd) and a flavo-diiron protein (FprA) (locus tags: TM_0754, TM_0659 and TM_0755, respectively). In vitro experiments showed that the NADH-dependent O2 consumption rate was 881.9 (± 106.7) mol O2 consumed min−1 per mol of FprA at 37°C and that water was the main end-product of the reaction. We propose that this O2 reduction chain plays a central role in the O2 tolerance of T. maritima. Phylogenetic analyses suggest that the genes coding for these three components were acquired by an ancestor of Thermotogales from an ancestor of Thermococcales via a single gene transfer. This event likely also involved two ROS scavenging enzymes (neelaredoxin and rubrerythrin) that are encoded by genes clustered with those coding for FprA, NRO and Rd in the ancestor of Thermococcales. Such genomic organization would have provided the ancestor of Thermotogales with a complete set of enzymes dedicated to O2-toxicity defence. Beside Thermotogales and Thermococcales, horizontal gene transfers have played a major role in disseminating these enzymes within the hyperthermophilic anaerobic prokaryotic communities, allowing them to cope with fluctuating oxidative conditions that exist in situ.

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