Growth of the Obligate Anaerobe Desulfovibrio vulgaris Hildenborough under Continuous Low Oxygen Concentration Sparging: Impact of the Membrane-Bound Oxygen Reductases

Fanny Ramel (1) , Gael Brasseur (1) , Laetitia Pieulle (1) , Odile Valette (1) , Agnès Hirschler-Réa (2) , Marie Laure Fardeau (2) , Alain Dolla (1)

1 LCB - Laboratoire de chimie bactérienne
2 MIO - Institut méditerranéen d'océanologie

Although obligate anaerobe, the sulfate-reducing bacterium Desulfovibrio vulgaris Hilden-borough (DvH) exhibits high aerotolerance that involves several enzymatic systems, including two membrane-bound oxygen reductases, a bd-quinol oxidase and a cc(b/o)o(3) cytochrome oxidase. Effect of constant low oxygen concentration on growth and morphology of the wild-type, single (Delta bd,Delta cox) and double deletion (Delta coxbd) mutant strains of the genes encoding these oxygen reductases was studied. When both wild-type and deletion mutant strains were cultured in lactate/sulfate medium under constant 0.02% O-2 sparging, they were able to grow but the final biomasses and the growth yield were lower than that obtained under anaerobic conditions. At the end of the growth, lactate was not completely consumed and when conditions were then switched to anaerobic, growth resumed. Time-lapse microscopy revealed that a large majority of the cells were then able to divide (over 97%) but the time to recover a complete division event was longer for single deletion mutant Delta bd than for the three other strains. Determination of the molar growth yields on lactate suggested that a part of the energy gained from lactate oxidation was derived toward cells protection/repairing against oxidative conditions rather than biosynthesis, and that this part was higher in the single deletion mutant Delta bd and, to a lesser extent, Delta cox strains. Our data show that when DvH encounters oxidative conditions, it is able to stop growing and to rapidly resume growing when conditions are switched to anaerobic, suggesting that it enters active dormancy sate under oxidative conditions. We propose that the pyruvate-ferredoxin oxidoreductase (PFOR) plays a central role in this phenomenon by reversibly switching from an oxidative-sensitive fully active state to an oxidative-insensitive inactive state. The oxygen reductases, and especially the bd-quinol oxidase, would have a crucial function by maintaining reducing conditions that permit PFOR to stay in its active state.

Mots clés: SULFATE-REDUCING BACTERIA; PYRUVATE-FERREDOXIN OXIDOREDUCTASE; SP STRAIN MB; CYTOCHROME BD; MICROBIAL MAT; VULGATIS HILDENBOROUGH; AZOTOBACTER-VINELANDII; OXIDATIVE STRESS; DEPENDENT GROWTH; SP. NOV

Domaines: Bactériologie; Biochimie [q-bio.BM]; Chimie organique

Fanny Ramel, Gael Brasseur, Laetitia Pieulle, Odile Valette, Agnès Hirschler-Réa, et al.. Growth of the Obligate Anaerobe Desulfovibrio vulgaris Hildenborough under Continuous Low Oxygen Concentration Sparging: Impact of the Membrane-Bound Oxygen Reductases. PLoS ONE, 2015, 10, pp.e0123455. ⟨10.1371/journal.pone.0123455⟩. ⟨hal-01216176⟩