Metatranscriptomic Analysis of Diminutive Thiomargarita-Like Bacteria (“Candidatus Thiopilula” spp.) from Abyssal Cold Seeps of the Barbados Accretionary Prism

Abstract

Large sulfur-oxidizing bacteria in the family Beggiatoaceae are important players in the global sulfur cycle. This group contains members of the well-known genera Beggiatoa, Thioploca, and Thiomargarita but also recently identified and relatively unknown candidate taxa, including "Candidatus Thiopilula" spp. and "Ca. Thiophysa" spp. We discovered a population of "Ca. Thiopilula" spp. colonizing cold seeps near Barbados at a ϳ4.7-km water depth. The Barbados population consists of spherical cells that are morphologically similar to Thiomargarita spp., with elemental sulfur inclusions and a central vacuole, but have much smaller cell diameters (5 to 40 m). Metatranscriptomic analysis revealed that when exposed to anoxic sulfidic conditions, Barbados "Ca. Thiopilula" organisms expressed genes for the oxidation of elemental sulfur and the reduction of nitrogenous compounds, consistent with their vacuolated morphology and intracellular sulfur storage capability. Metatranscriptomic analysis further revealed that anaerobic methane-oxidizing and sulfate-reducing organisms were active in the sediment, which likely provided reduced sulfur substrates for "Ca. Thiopilula" and other sulfur-oxidizing microorganisms in the community. The novel observations of "Ca. Thiopilula" and associated organisms reported here expand our knowledge of the globally distributed and ecologically successful Beggiatoaceae group and thus offer insight into the composition and ecology of deep cold seep microbial communities.T he family Beggiatoaceae contains the sulfur-oxidizing genera Beggiatoa, Thioploca, and Thiomargarita, including the largest known bacterium, Thiomargarita namibiensis, which can have cell diameters of Ͼ750 m (1, 2). Certain members of the Beggiatoaceae store nitrate in a large central vacuole, which supplies an electron acceptor to fuel anaerobic sulfur oxidation when oxygen is unavailable (2-4). As sulfide-oxidizing lithotrophs, members of the Beggiatoaceae thrive in diverse sulfidic environments (5, 6). Biomats constructed by these microorganisms are a conspicuous feature at oxygen minimum zones, hydrocarbon seeps, hydrothermal vents, and whale falls (see reference 7 and references therein), where they fill important roles in the global carbon and sulfur cycles. For example, the Beggiatoaceae are often primary producers in sulfidic marine sediments, where they act to conserve some of the potential energy present in sulfide that is produced during the anaerobic remineralization of organic carbon. As much as 80 to 95% of the sulfide produced during sulfate reduction escapes burial and is reoxidized, and much of this reoxidation occurs in the shallow sediment zone (8, 9). In addition to catalyzing important sulfur and nitrogen transformations, marine representatives of the Beggiatoaceae may even contribute to phosphate mineral formation (10-12). Furthermore, because of their large size and morphological complexity, Beggiatoa-and Thiomargarita-like cells have been identified in the fossil record and offer clues to microbial sul...

Barite encrustation of benthic sulfur‐oxidizing bacteria at a marine cold seep

“…While it is possible that living cells were present in void spaces within the crust, the lack of amplifiable DNA in rinsate fluids tested prior to DNA extraction from the crust, as well as the presence of partially mineralized Beggiatoa filaments in portions of the crust, suggest that at least some of the Beggiatoa DNA is coeval with barite precipitation. It is not surprising that Maribeggiatoa 16S rRNA gene sequences represent a relatively minor portion of the libraries here, given that numerous other studies have reported difficulties with amplifying 16S rRNA gene sequences from samples visibly dominated by Beggiatoa and related organisms in the family Beggiatoaceae (e.g., Sekar et al ., ; Salman et al ., ; Jones et al ., ).…”

Metabolic and spatio-taxonomic response of uncultivated seafloor bacteria following the Deepwater Horizon oil spill

“…Thiopilula spp. (MacGregor et al, 2013;Jones et al, 2015) based on reverse operation in Nautilia profundicola (Hanson Figure 4 Schematics of 14 gammaproteobacterial genome bins with the metabolic potential to degrade hydrocarbons (Groups 1-4), and a schematic showing the genes GSC1 likely uses to encode for denitrification and sulfide oxidation (representative bin of Group 5: GSC1-3). Genes present are represented by black symbols; those missing are red.…”

Profiling bacterial communities associated with sediment-based aquaculture bioremediation systems under contrasting redox regimes

“…Additional chemolithotrophic biomarkers involved in biogeochemical cycles included an enrichment of ferrous iron oxidisers (Acidomicrobiales) and the sulphur oxidising genus Thiopilula (Thiotrichales) in the oxic treatment30. Sulphur cycling in aquaculture systems is important as un-ionised dissolved hydrogen sulphide (H 2 S) is extremely toxic to many aquatic organisms, even at natural levels31.…”