title: Growth of the obligate anaerobe Desulfovibrio vulgaris Hildenborough under continuous low oxygen concentration sparging: impact of the membrane-bound oxygen reductases.
abstract: Although obligate anaerobe, the sulfate-reducing bacterium Desulfovibrio vulgaris Hildenborough (DvH) exhibits high aerotolerance that involves several enzymatic systems, including two membrane-bound oxygen reductases, a bd-quinol oxidase and a cc(b/o)o3 cytochrome oxidase. Effect of constant low oxygen concentration on growth and morphology of the wild-type, single (Δbd, Δcox) and double deletion (Δcoxbd) 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% O2 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 Δbd 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 Δbd and, to a lesser extent, Δcox 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.
authors.affiliation: Aix-Marseille Université, CNRS, LCB-UMR7283, Marseille, France.
authors.forename: Fanny
authors.initials: F
authors.lastname: Ramel
authors.affiliation: Aix-Marseille Université, CNRS, LCB-UMR7283, Marseille, France.
authors.forename: Gael
authors.initials: G
authors.lastname: Brasseur
authors.affiliation: Aix-Marseille Université, CNRS, LCB-UMR7283, Marseille, France.
authors.forename: Laetitia
authors.initials: L
authors.lastname: Pieulle
authors.affiliation: Aix-Marseille Université, CNRS, LCB-UMR7283, Marseille, France.
authors.forename: Odile
authors.initials: O
authors.lastname: Valette
authors.affiliation: Aix-Marseille Université, Université de Toulon, CNRS, IRD, MIO, UM110, 13288 Marseille, Cedex 09, France.
authors.forename: Agnès
authors.initials: A
authors.lastname: Hirschler-Réa
authors.affiliation: Aix-Marseille Université, Université de Toulon, CNRS, IRD, MIO, UM110, 13288 Marseille, Cedex 09, France.
authors.forename: Marie Laure
authors.initials: ML
authors.lastname: Fardeau
authors.affiliation: Aix-Marseille Université, CNRS, LCB-UMR7283, Marseille, France.
authors.forename: Alain
authors.initials: A
authors.lastname: Dolla
mesh_terms: D000693:Anaerobiosis; D018533:Biomass; D049109:Cell Proliferation / Q000502:physiology; D016969:Desulfovibrio vulgaris / Q000235:genetics / Q000254:growth & development* / Q000378:metabolism*; D003576:Electron Transport Complex IV / Q000378:metabolism*; D019344:Lactic Acid / Q000378:metabolism; D010084:Oxidation-Reduction; D010088:Oxidoreductases / Q000378:metabolism*; D010100:Oxygen / Q000378:metabolism*; D050743:Pyruvate Synthase / Q000378:metabolism
chemical_list: D019344:Lactic Acid; D010088:Oxidoreductases; C020094:duroquinol oxidase; D050743:Pyruvate Synthase; C038862:cytochrome o oxidase; D003576:Electron Transport Complex IV; D010100:Oxygen
references.citation: Anaerobe. 2008 Jun;14(3):145-56
references.pmid: 18457966
references.citation: Anaerobe. 2012 Aug;18(4):454-8
references.pmid: 22706208
references.citation: Biochem Biophys Res Commun. 1993 May 28;193(1):100-5
references.pmid: 8503894
references.citation: Environ Microbiol. 1999 Dec;1(6):489-94
references.pmid: 11207770
references.citation: Microbiology. 2013 Dec;159(Pt 12):2663-73
references.pmid: 24085836
references.citation: Appl Environ Microbiol. 1996 Apr;62(4):1405-15
references.pmid: 8919802
references.citation: Appl Environ Microbiol. 2000 Nov;66(11):5013-8
references.pmid: 11055957
references.citation: Anaerobe. 1996 Feb;2(1):1-9
references.pmid: 16887549
references.citation: Biochemistry. 2007 Oct 2;46(39):11177-84
references.pmid: 17784736
references.citation: J Biol Chem. 2011 Mar 11;286(10):7812-21
references.pmid: 21199874
references.citation: Antonie Van Leeuwenhoek. 2006 Feb;89(2):221-37
references.pmid: 16710634
references.citation: Appl Environ Microbiol. 1999 Oct;65(10):4659-65
references.pmid: 10508103
references.citation: Curr Microbiol. 2006 Apr;52(4):274-81
references.pmid: 16550467
references.citation: Proc Natl Acad Sci U S A. 1994 Oct 11;91(21):10173-7
references.pmid: 7937858
references.citation: Biochemistry. 2005 May 3;44(17):6492-501
references.pmid: 15850383
references.citation: Appl Environ Microbiol. 1999 Nov;65(11):5117-23
references.pmid: 10543830
references.citation: Environ Microbiol. 2012 Oct;14(10):2711-25
references.pmid: 22947039
references.citation: Biochim Biophys Acta. 2011 Nov;1807(11):1398-413
references.pmid: 21756872
references.citation: Annu Rev Microbiol. 2000;54:827-48
references.pmid: 11018146
references.citation: Environ Microbiol. 2001 Jan;3(1):63-71
references.pmid: 11225724
references.citation: J Bacteriol. 2007 Aug;189(16):5996-6010
references.pmid: 17545284
references.citation: Biochim Biophys Acta. 1997 Aug 22;1321(2):107-27
references.pmid: 9332500
references.citation: Nat Struct Biol. 2000 Nov;7(11):1041-5
references.pmid: 11062560
references.citation: J Bacteriol. 1997 Sep;179(17):5598-601
references.pmid: 9287020
references.citation: Nat Methods. 2012 Jul;9(7):676-82
references.pmid: 22743772
references.citation: Antonie Van Leeuwenhoek. 2008 May;93(4):347-62
references.pmid: 18060515
references.citation: Appl Environ Microbiol. 2000 Nov;66(11):5019-23
references.pmid: 11055958
references.citation: FEBS Lett. 2001 May 4;496(1):40-3
references.pmid: 11343703
references.citation: Biosci Rep. 1997 Jun;17(3):303-17
references.pmid: 9337485
references.citation: J Bioenerg Biomembr. 2008 Oct;40(5):521-31
references.pmid: 18975062
references.citation: Science. 1991 Mar 22;251:1471-3
references.pmid: 11538266
references.citation: Biochimie. 2006 Jan;88(1):85-94
references.pmid: 16040186
references.citation: Appl Environ Microbiol. 1999 Nov;65(11):5107-16
references.pmid: 10543829
references.citation: Appl Environ Microbiol. 1992 Jan;58(1):70-7
references.pmid: 16348641
references.citation: ISME J. 2013 Sep;7(9):1752-63
references.pmid: 23575370
references.citation: Biochim Biophys Acta. 1995 Jul 3;1250(1):49-59
references.pmid: 7612653
references.citation: J Bacteriol. 2006 Sep;188(17):6253-60
references.pmid: 16923892
references.citation: Appl Environ Microbiol. 1998 Oct;64(10):3731-9
references.pmid: 9758792
references.citation: Appl Environ Microbiol. 1991 Mar;57(3):847-56
references.pmid: 16348450
references.citation: Biochemistry. 2008 Jan 22;47(3):957-64
references.pmid: 18161989
references.citation: Syst Appl Microbiol. 1998 Jun;21(2):212-9
references.pmid: 9704109
references.citation: J Biol Chem. 2004 Jan 16;279(3):1787-93
references.pmid: 14594815
references.citation: Arch Microbiol. 2001 Oct;176(4):306-9
references.pmid: 11685376
references.citation: Microbiology. 2011 Sep;157(Pt 9):2720-32
references.pmid: 21737501