Oxygen reduction in the strict anaerobe Desulfovibrio vulgaris Hildenborough: characterization of two membrane-bound oxygen reductases

Abstract

Although Desulfovibrio vulgaris Hildenborough (DvH) is a strictly anaerobic bacterium, it is able to consume oxygen in different cellular compartments, including extensive periplasmic O 2 reduction with hydrogen as electron donor. The genome of DvH revealed the presence of cydAB and cox genes, encoding a quinol oxidase bd and a cytochrome c oxidase, respectively. In the membranes of DvH, we detected both quinol oxygen reductase [inhibited by heptyl-hydroxyquinoline-N-oxide (HQNO)] and cytochrome c oxidase activities. Spectral and HPLC data for the membrane fraction revealed the presence of o-, b-and d-type haems, in addition to a majority of c-type haems, but no a-type haem, in agreement with carbon monoxide-binding analysis. The cytochrome c oxidase is thus of the cc(o/b)o 3 type, a type not previously described. The monohaem cytochrome c 553 is an electron donor to the cytochrome c oxidase; its encoding gene is located upstream of the cox operon and is 50-fold more transcribed than coxI encoding the cytochrome c oxidase subunit I. Even when DvH is grown under anaerobic conditions in lactate/sulfate medium, the two terminal oxidase-encoding genes are expressed. Furthermore, the quinol oxidase bd-encoding genes are more highly expressed than the cox genes. The cox operon exhibits an atypical genomic organization, with the gene coxII located downstream of coxIV. The occurrence of these membrane-bound oxygen reductases in other strictly anaerobic Deltaproteobacteria is discussed.

Membrane-bound oxygen reductases of the anaerobic sulfate-reducing Desulfovibrio vulgaris Hildenborough: roles in oxygen defence and electron link with periplasmic hydrogen oxidation

“…Relative transcription levels of the genes encoding the cyt. c oxidase or the bd quinol oxidase showed that the latter genes were more highly expressed than the former (about 35-fold) in lactate-sulfate medium under anaerobic conditions in mid-exponential phase, which was in agreement with the higher abundance of the bd oxidase in membrane fractions, as deduced from optical spectroscopy (Lamrabet et al, 2011).…”

“…Cells and membranes were prepared as described previously (Lamrabet et al, 2011). In the case of O 2 reduction with hydrogen as an electron donor, cells were prepared in anaerobic buffer degassed with argon for all steps to prevent any inactivation of hydrogenases with O 2 .…”

“…c oxidase in the membrane fraction of Desulfovibrio vulgaris Hildenborough (DvH) and reported their spectroscopic and biochemical properties (Lamrabet et al, 2011). We pointed out that the cyt.…”

“…In the course of the evolutionary challenge to adapt to the presence of increasing O 2 levels, aerobic micro-organisms succeeded in using oxygen in complex high energy-yielding respiratory chains that include a terminal oxidase of the haem-copper superfamily (Pereira et al, 2001). Surprisingly, genome analysis indicates that some strictly anaerobic micro-organisms such as Geobacter, Pelobacter and Desulfovibrio species contain genes encoding such enzymes (Lamrabet et al, 2011). While their function is easily understandable in aerobic micro-organisms, the role of this enzyme in anaerobic forms of life is intriguing.…”

“…We pointed out that the cyt. c oxidase does not contain a but instead o/b-type haems in subunit I as well as two c-type haems in subunit II (Lobo et al, 2008) and is therefore the first described cc(b/o)o3-type haemcopper oxidase (Lamrabet et al, 2011). Relative transcription levels of the genes encoding the cyt.…”