Sulfate Reduction and Possible Aerobic Metabolism of the Sulfate-Reducing Bacterium Desulfovibrio oxyclinae in a Chemostat Coculture with Marinobacter sp. Strain MB under Exposure to Increasing Oxygen Concentrations

Abstract

A chemostat coculture of the sulfate-reducing bacterium Desulfovibrio oxyclinae together with a facultative aerobe heterotroph tentatively identified as Marinobacter sp. strain MB was grown under anaerobic conditions and then exposed to a stepwise-increasing oxygen influx (0 to 20% O 2 in the incoming gas phase). The coculture consumed oxygen efficiently, and no residual oxygen was detected with an oxygen supply of up to 5%. Sulfate reduction persisted at all levels of oxygen input, even at the maximal level, when residual oxygen in the growth vessel was 87 M. The portion of D. oxyclinae cells in the coculture decreased gradually from 92% under anaerobic conditions to 27% under aeration. Both absolute cell numbers and viable cell counts of the organism were the same as or even higher than those observed in the absence of oxygen input. The patterns of consumption of electron donors and acceptors suggest that aerobic incomplete oxidation of lactate to acetate is performed by D. oxyclinae under high oxygen input. Both organisms were isolated from the same oxic zone of a cyanobacterial mat where they have to adapt to daily shifts from oxic to anoxic conditions. This type of syntrophic association may occur in natural habitats, enabling sulfate-reducing bacteria to cope with periodic exposure to oxygen.The photic zone of cyanobacterial mats is characterized by extreme shifts in oxygen and sulfide concentrations from oxygen supersaturation during the light period to anoxic, sulfideenriched conditions in the dark (24). These changes are a challenge for the organisms living in such a habitat. Daily exposure to high oxygen concentrations may be deleterious to obligately anaerobic organisms, such as sulfate-reducing bacteria (SRB) (13,18,24). High numbers of SRB were found in the oxic zone of a cyanobacterial mat from the Solar Lake (Sinai) throughout the diurnal cycle (10,21,22,25,27), indicating that these organisms can deal with exposure to elevated oxygen concentrations of even up to 1.5 mM. Moreover, high rates of sulfate reduction were found in the oxic layers of these microbial mats (4, 5, 9), as well as in microbial mats from Baja California, Mexico (2).None of the SRB isolated so far can either grow aerobically or reduce sulfate under high concentrations of oxygen. Desulfovibrio vulgaris Hildenborough was found to be capable of slow linear aerobic growth under very low concentrations of oxygen. Oxygen concentrations of only 0.07% were toxic to this organism (14). The oxygen-tolerant SRB Desulfovibrio oxyclinae isolated in our laboratory (16) was demonstrated to persist in continuous culture gassed with 1% O 2 , although flocculation occurred after exposure to oxygen (25).It was previously demonstrated that SRB in the upper layer of cyanobacterial mats can form close associations with oxygen-scavenging bacteria (12, 26). Such consortia may be responsible, at least in part, for the observed in situ sulfatereducing activity under aerobic conditions.In this report, we present the effects of exposure to oxygen on the ...

Micron-scale mapping of sulfur cycling across the oxycline of a cyanobacterial mat: a paired nanoSIMS and CARD-FISH approach

“…SRB are also found in aggregates with similar scale and spatial distribution as that apparent in the nano-SIMS data (Figures 1 and 3). This observed clumping of SRB, particularly in the oxic zone (Figure 5a), has been reported from other oxic habitats, and is thought to generate microenvironments that favor continued sulfate reduction (Cypionka, 2000;Sigalevich et al, 2000;Wieland et al, 2005). The occurrence of SRB in oxic zones may be a trade-off between oxygen stress and the proximity to photosynthate that can be used during sulfate reduction (Frund and Cohen, 1992;Wieland et al, 2005).…”

“…The occurrence of SRB in oxic zones may be a trade-off between oxygen stress and the proximity to photosynthate that can be used during sulfate reduction (Frund and Cohen, 1992;Wieland et al, 2005). Both SRB populations and organic substrate consumption are known to vary with depth, supporting spatially variable sulfate reduction based upon the flow of energy and organic carbon substrates (Frund and Cohen, 1992;Risatti et al, 1994;Sigalevich et al, 2000;Wieland et al, 2005;Musselwhite et al, 2007). Such heterogeneous sulfate reduction naturally explains the patchiness in sulfide abundance and isotopic composition observed in this study.…”

“…Mat-associated sulfate-reducing bacteria (SRB) were initially considered to be strict anaerobes residing below the oxic/anoxic chemocline, which was inhabited by sulfide oxidizers and presumably sulfur disproportionators that catabolize intermediate valence compounds (S 0 , S 2 O 3 2À , SO 3 2À ) . The discovery of abundant SRB and elevated sulfate-reduction rates in the oxic surface layers of mats indicates a more complicated spatial organization of the different sulfur-cycling metabolisms (Frund and Cohen, 1992;Canfield and Des Marais, 1993;Krekeler et al, 1997;Minz et al, 1999a;Sigalevich et al, 2000;Wieringa et al, 2000;Baumgartner et al, 2006). Indeed, among SRB, there is evidence for vertical segregation between different phylogenetic clades in microbial mats (Risatti et al, 1994;Minz et al, 1999b;Decho et al, 2005;Wieland et al, 2005).…”

Microbial Diversity of a Heavily Polluted Microbial Mat and Its Community Changes following Degradation of Petroleum Compounds

“…It is likely that anaerobic processes are more important in the natural environment of Wadi Gaza, in which the fine-grained sediment is oxygen depleted at depths below a few millimeters. The presence and metabolic activity of anaerobic organisms in mainly oxic zones of microbial mats have been demonstrated previously (46,55,56). The presence of band L2, phylogenetically shown to represent green nonsulfur bacteria, only in the presence of organo-clay complexes in the light opens the unexplored possibility that anoxygenic phototrophs, particularly those with known photoheterotrophic modes of growth, such as Chloroflexus, could be used in bioremediation studies.…”

Kinetic of biogenic sulfide production for microbial consortia isolated from soils with different bioaccessible concentrations of lead

“…Agar (10 g L -1 ) was added to create a solid medium. After 1 month of incubation, the tubes took on a dark color, which is indicative of the presence of iron sulfides (Sigalevich et al 2000). Onemilliliter aliquots were spread onto Petri dishes containing Postgate solid medium (PSM) and incubated for 1 month inside an anaerobic chamber.…”