When first isolated, D. thermomarina was placed in the Deltaproteobacteria but was not assigned at lower taxonomic ranks. Following genome-wide taxonomic analysis with GTDB-Tk, D. thermomarina is robustly placed in the Dissulfuribacterales order (phylum Desulfobacterota, class Dissulfuribacteria), but does not cluster with any characterized families within this order. D. thermomarina is sufficiently divergent from its closest characterized relative, Dissulfuribacter thermophilus, to suggest that these organisms represent separate families within the Dissulfibacterales. We therefore propose assignment of D. thermomarina as the type species of a novel family, Dissulfurirhabdaceae, within the Dissulfuribacterales order of Desulfobacterota.
Sulfur disproportionators are expected to encode the same marker genes as sulfate reducers (e.g. Anantharaman et. al., 2018); consistent with this expectation, D. thermomarina encodes sulfate adenylyltransferase, adenylylsulfate reductase, dissimilatory sulfite reductase, and the complex DsrMKJOP, which is associated with sulfite reduction. Known sulfur disproportionators in the Desulfobulbaceae family of Desulfobacterota encode AprB proteins with a truncated tail; this conserved truncation has been proposed as a molecular marker of the capacity for sulfur disproportionation (Bertran 2019). D. thermomarina encodes an AprB protein with a similar truncation despite encoding an AprB protein that is only distantly related to those of the Desulfobulbaceae (Fig. 2). This AprB truncation appears to have independently evolved in D. thermomarina, reinforcing interpretations of the association between this marker and the capacity for disproportionation; moreover, the apparently independent acquisition of the AprB truncation and the capacity for disproportionation in D. thermomarina and members of the Desulfobulbaceae suggests that this might be a more widespread trait that has evolved convergently multiple times in ancestrally sulfate reducing lineages.
D. thermomarina is capable of autotrophic growth (Slobodkina et. al., 2016) and encodes CO dehydrogenase/acetyl-CoA synthase, suggesting it makes use of the reductive acetyl-CoA (Wood-Ljungdahl) pathway like many sulfate reducing bacteria (Berg 2011). The genome encodes a hydrogenase annotated by HydDB as a Group 1c NiFe hydrogenase associated with anaerobic respiratory uptake of H2. D. thermomarina does not encode canonical proteins for aerobic respiration or denitrification, consistent with its inability to use O2 or nitrate as electron acceptors in culture (Slobodkina et. al., 2016). However, this organism encodes a bd O2 reductase; while these enzymes can in some cases be coupled to aerobic respiration (e.g. in Nitrospira, Palomo et al. 2018), they are often found in obligate anaerobes (e.g. Ward et. al., 2015) in which they are likely used for O2 detoxification and oxidative stress tolerance (Forte et. al., 2017).
D. thermomarina is capable of disproportionating not only soluble sulfur species such as sulfite but also insoluble elemental sulfur (Slobodkina et. al., 2016). The mechanism of elemental sulfur disproportionation in D. thermomarina and other strains capable of this metabolism is not known yet, but likely involves novel extracellular electron transfer pathways. Extracellular multiheme cytochrome proteins are commonly involved in respiratory electron transfer to insoluble mineral substrates (e.g. McGlynn et. al., 2015, Shi et. al.. 2016) and could therefore be expected to be involved in disproportionation of elemental sulfur. Analysis of the D. thermomarina genome with CXXCH_finder (McGlynn et. al., 2015) recovered 81 proteins with heme binding domains, including one hypothetical protein with 26 heme binding motifs—on par with proteins from bacteria such as Geobacter and Shewanella, well known for their capacity for extracellular electron transfer and ability to respire extracellular mineral substrates (McGlynn et. al., 2015). This hypothetical protein shows low similarity to other proteins accessible on the NCBI database (< 50% to any sequences), but of all proteins from well-characterized organisms it is most similar to a hypothetical protein from Thermosulfidibacter takii, a thermophilic bacterium capable of elemental sulfur reduction. The putative extracellular electron transfer protein from D. thermomarina also has notable similarity (~ 30%) to extracellular iron oxide respiratory system periplasmic decaheme cytochrome c protein components from Shewanella oneidensis MR-1 including the protein DsmE associated with respiration of extracellular substrates (e.g. Bewley et. al., 2012). We therefore propose that D. thermomarina utilizes extracellular multiheme cytochrome proteins related to those in dissimilatory iron reducing bacteria in order to transfer electrons to insoluble substrates such as elemental sulfur. In contrast, members of the Desulfobulbales that are characterized as being capable of elemental sulfur disproportionation (e.g. Desulfobulbus propionicus, Desulfocapsa thiozymogenes) encode proteins with no more than 11 or 12 CxxCH motifs, suggesting that different lineages may have evolved multiple different mechanisms to enable the metabolism of insoluble sulfur compounds.