Oxygen uptake rates in the hyperthermophilic anaerobe Thermotoga maritima grown in a bioreactor under controlled oxygen

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ORIGINAL PAPER

Oxygen uptake rates in the hyperthermophilic anaerobe Thermotoga maritima grown in a bioreactor under controlled oxygen exposure: clues to its defence strategy against oxidative stress Raja Lakhal • Richard Auria • Sylvain Davidson • Bernard Ollivier • Marie-Claire Durand • Alain Dolla • Moktar Hamdi • Yannick Combet-Blanc Received: 28 September 2010 / Revised: 12 January 2011 / Accepted: 17 February 2011 / Published online: 12 March 2011 Ó Springer-Verlag 2011

Abstract A 2.3-L bioreactor was specially adapted to grow hyperthermophilic microorganisms under controlled conditions of temperature, pH, redox potential and dissolved O2. Using this bioreactor regulated at 80°C and pH 7.0, we demonstrated that Thermotoga maritima recovered its growth despite being exposed to oxygen for a short time (30 min with a maximum concentration of 23 lM of dissolved oxygen). Under these conditions, we demonstrated that O2 uptake rate, estimated at 73.6 lmoles O2 min-1 g proteins-1 for dissolved oxygen, was optimal and constant, when dissolved oxygen was present in a range of 22–5 lM. Transcription analyses revealed that during short oxygen exposure, T. maritima expressed genes coding for enzymes to deal with O2 and reactive oxygen species (ROS) such as peroxides. Thus, genes encoding ROS-scavenging systems, alkyl hydroperoxide reductase (ahp), thioredoxin-dependent thiol peroxidase (bcp 2) and to a lesser extent neelaredoxin (nlr) and rubrerythrin (rbr), were found to be upregulated during oxygen exposure. The oxygen reductase Communicated by Harald Huber. R. Lakhal  R. Auria  S. Davidson  B. Ollivier  Y. Combet-Blanc (&) UMR_D180 IRD, ESIL, Universite´s de Provence et de la Me´diterrane´e, 163 avenue de Luminy, Case 925, 13288 Marseille Cedex 09, France e-mail: [email protected] M.-C. Durand  A. Dolla Unite´ Interactions et Modulateurs de Re´ponses, IFR88-CNRS, 31 chemin Joseph-Aiguier, 13402 Marseille Cedex 20, France M. Hamdi Laboratoire d’Ecologie et de Technologie Microbienne, Institut National des Sciences Applique´es et de Technologies (INSAT), Universite´ de Carthage, 2 boulevard de la Terre, B.P. 676, 1080 Tunis, Tunisia

FprA, homologous to the rubredoxin-oxygen oxidoreductase (ROO) found in Desulfovibrio species, is proposed as a primary consumer of O2 in T. maritima. Moreover, the expression of frpA was shown to depend on the redox (Eh) level of the culture medium. Keywords Oxygen

Thermotoga maritima  Oxidative stress 

Introduction Thermotoga spp. are hyperthermophilic or thermophilic fermentative anaerobic bacteria that belong to a deepbranching lineage within the domain Bacteria (Huber et al. 1986; Woese 1987; Darimont and Sterner 1994; Nelson et al. 1999). They inhabit various hot ecosystems, including hot springs, hydrothermal vents and oil reservoirs (Huber and Stetter 1992; Jeanthon et al. 1995; Fardeau et al. 1997), characterized by hostile physicochemical gradients e.g. of oxygen (von Damm 1990; Jorgensen et al. 1992; Wenzho¨fer et al. 2000) as in hydrothermal vent ecosystems