Disguised as a Sulfate Reducer: Growth of the Deltaproteobacterium Desulfurivibrio alkaliphilus by Sulfide Oxidation with Nitrate

Abstract

This study demonstrates that the deltaproteobacterium Desulfurivibrio alkaliphilus can grow chemolithotrophically by coupling sulfide oxidation to the dissimilatory reduction of nitrate and nitrite to ammonium. Key genes of known sulfide oxidation pathways are absent from the genome of D. alkaliphilus. Instead, the genome contains all of the genes necessary for sulfate reduction, including a gene for a reductive-type dissimilatory bisulfite reductase (DSR). Despite this, growth by sulfate reduction was not observed. Transcriptomic analysis revealed a very high expression level of sulfate-reduction genes during growth by sulfide oxidation, while inhibition experiments with molybdate pointed to elemental sulfur/polysulfides as intermediates. Consequently, we propose that D. alkaliphilus initially oxidizes sulfide to elemental sulfur, which is then either disproportionated, or oxidized by a reversal of the sulfate reduction pathway. This is the first study providing evidence that a reductive-type DSR is involved in a sulfide oxidation pathway. Transcriptome sequencing further suggests that nitrate reduction to ammonium is performed by a novel type of periplasmic nitrate reductase and an unusual membrane-anchored nitrite reductase.

Mimicking microbial interactions under nitrate‐reducing conditions in an anoxic bioreactor: enrichment of novel Nitrospirae bacteria distantly related to Thermodesulfovibrio

“…Sulfide might be used by the reverse reaction of the sulfate reduction pathway; however, when we analyzed the phylogenetic relationship of the relevant DsrA protein encoded by these organisms, we noted that it falls into the sulfate-reducing and not the sulfideoxidizing cluster, making it unlikely that these bacteria are able to oxidize sulfide with DsrAB. It has however recently been reported that a reductive-type DsrAB might be able to work in the oxidative direction (Thorup et al, 2017), but this result has not yet been biochemically validated. We did not find a sulfide quinone oxidoreductase that could complement this activity, making it unlikely that sulfide is used as an electron donor.…”

Phototrophic marine benthic microbiomes: the ecophysiology of these biological entities

“…Nitrate is reduced to ammonia rather than denitrified to N 2 and, therefore, this nutrient remains available for the sediment microbial community. Remarkably, even some sulfate-reducing bacteria contribute to the oxidation of sulfide with nitrate by inversing the pathway of dissimilatory sulfate reduction (Thorup et al, 2017). Similar as Beggiatoa, Desulfurivibrio alkaliphilus oxidizes sulfide initially to elemental sulfur, which is subsequently oxidized to sulfate.…”

Geologic legacy spanning >90 years explains unique Yellowstone hot spring geochemistry and biodiversity

“…, Thorup et al . ). Importantly, catalytic directionality is generally consistent with phylogenetic placement of DsrAB (Müller et al .…”

“…5). DsrAB functions in both the forward (SO 4 2− reduction) and reverse (S oxidation) directions and may also be potentially involved in S /polysulfide disproportionation (Müller et al 2014, Thorup et al 2017. Importantly, catalytic directionality is generally consistent with phylogenetic placement of DsrAB (Müller et al 2015).…”