Organohalide-respiringDesulfolunaspecies isolated from marine environments

Abstract

The genus Desulfoluna comprises two anaerobic sulfate-reducing strains, D. spongiiphila AA1⊤ and D. butyratoxydans MSL71⊤ of which only the former was shown to perform organohalide respiration (OHR). Here we isolated a third member of this genus from marine intertidal sediment, designed D. spongiiphila strain DBB. All three Desulfoluna strains harbour three reductive dehalogenase gene clusters (rdhABC) and corrinoid biosynthesis genes in their genomes. Brominated but not chlorinated aromatic compounds were dehalogenated by all three strains. The Desulfoluna strains maintained OHR in the presence of 20 mM sulfate or 20 mM sulfide, which often negatively affect OHR. Strain DBB sustained OHR with 2% oxygen in the gas phase, in line with its genetic potential for reactive oxygen species detoxification. Reverse transcription-quantitative PCR (RT-qPCR) revealed differential induction of rdhA genes in strain DBB in response to 1,4-dibromobenzene or 2,6-dibromophenol. Proteomic analysis confirmed differential expression of rdhA1 with 1,4-dibromobenzene, and revealed a possible electron transport chain from lactate dehydrogenases and pyruvate oxidoreductase to RdhA1 via menaquinones and either RdhC, or Fix complex (electron transfer flavoproteins), or Qrc complex (Type-1 cytochrome c3:menaquinone oxidoreductase).

Organohalide respiration by aDesulforhopalus-dominated community

“…B12 is the required cofactor for corrinoid-dependent RDases linked with OHR (25). Based on the analysis of bins, the de novo biosynthesis observed for the colony-derived consortium could be achieved by bin.3 and bin.5 separately, without the non-essential cbiJ gene, in line with what we observed earlier in marine Desulfoluna strains capable of OHR (37), or coordinatively achieved with bin.4 by providing the cbiJ gene missing in other bins. Hence, in summary, the genomic inferences in terms of predicted metabolic capacity of the colony-derived consortium sufficiently explain the observed OHR capacity of the consortium in the absence of added B12 (Figure S4).…”

“…The complete inhibition of reductive debromination by acetylene furthermore suggests that acetylene inhibited activity of both types of RDases. Finally, the Desulforhopalus population (bin.5) is proposed to act as the B12 provider for OHRB (bin.3 and bin.4) due to its nearly-complete gene-set for de novo B12 biosynthesis except for cbiJ (Figure 6C), which was not required for OHR as previous described (37). Moreover, bin.4 contains a cbiJ gene indicating that this might play a role in the complete B12 biosynthesis of the isolated consortium.…”

“…Based on the five MAGs identified in this study, we propose ETCs and related activities in the 2, 6-DBP debrominating consortium studied here (Figure 6). bin.3 harbors two RDases, RDase1 and RDase2 (Figure 4), and we assumed that both RDases are part of ETCs that allow usage of hydrogen or lactate as electron donor as observed for Dehalobacter restrictus and Desulfoluna spongiiphila, respectively (37,79,80).…”

“…Marine medium was prepared for cultivation as previously described (36,37). The final growth medium was composed of 50 mL anoxic marine medium, Na2S•9H2O (0.48 g/L, 2 mM) serving as the reducing agent, and Resazurin (0.005 g/L) as the redox indicator.…”

Genome-resolved transcriptomics reveals novel organohalide-respiring bacteria from Aarhus Bay sediments

“…Desulfobacterota is a reclassified phylum from Deltaproteobacteria and well known for catalyzing sulfate reduction (69). Eighty-nine of the 939 representative genomes in the Desulfobacterota were found to carry RDase genes, similar to previously described strains of Desulfoluna, Desulfuromusa, and Desulfovibrio (21,74). Bin.21, classified into Desulfuromusa, had no annotated genes involved in OHR or sulfate reduction and had a high abundance when sulfate was absent as was found in the preceding study (20).…”