Microbial consumption of zero‐valence sulfur in marine benthic habitats

Abstract

Zero-valence sulfur (S°) is a central intermediate in the marine sulfur cycle and forms conspicuous accumulations at sediment surfaces, hydrothermal vents and in oxygen minimum zones. Diverse microorganisms can utilize S°, but those consuming S° in the environment are largely unknown. We identified possible key players in S° turnover on native or introduced S° in benthic coastal and deep-sea habitats using the 16S ribosomal RNA approach, (in situ) growth experiments and activity measurements. In all habitats, the epsilonproteobacterial Sulfurimonas/Sulfurovum group accounted for a substantial fraction of the microbial community. Deltaproteobacterial Desulfobulbaceae and Desulfuromonadales were also frequently detected, indicating S° disproportionation and S° respiration under anoxic conditions. Sulfate production from S° particles colonized in situ with Sulfurimonas/Sulfurovum suggested that this group oxidized S°. We also show that the type strain Sulfurimonas denitrificans is able to access cyclooctasulfur (S₈), a metabolic feature not yet demonstrated for sulfur oxidizers. The ability to oxidize S°, in particular S8 , likely facilitates niche partitioning among sulfur oxidizers in habitats with intense microbial sulfur cycling such as sulfidic sediment surfaces. Our results underscore the previously overlooked but central role of Sulfurimonas/Sulfurovum group for conversion of free S° at the seafloor surface.

Sulphur-cycling bacteria and ciliated protozoans in a Beggiatoaceae mat covering organically enriched sediments beneath a salmon farm in a southern Chilean fjord

“…can grow chemolithoautotrophically using S 0 , H 2 or reduced sulphur compounds as electron donors. Their co-occurrence with Sulfurovum highlights their central role as key group for conversion of free S 0 on the sea floor surface (Pjevac et al, 2014).…”

“…The dominance pattern could be considered as indicative of relatively strong SRB activity with high organic loads, with Desulfobacteraceae followed by Desulfobulbaceae as the dominant taxa (Kondo et al, 2012), instead of Desulfobacteraceae, Desulfovibrionaceae and Desulfuromonadaceae which are associated with regular organic loads (Saravanakumar et al, 2012). Additionally, detection of Desulfobulbaceae could be indicative of S 0 disproportionation under anoxic conditions (Pjevac et al, 2014) or could indicate filaments described as 'cable bacteria', which would able to electrically couple sulphide oxidation and oxygen reduction across the mat (Larsen et al, 2015), both are hypotheses that should be addressed by further exploration of organic-enriched sediments beneath aquaculture.…”

“…The clone with the larger sequence (*505, 1374 bp) has as nearest references an endosymbiont of a hydrothermal vent gastropod (AB235231, 98%) (Suzuki et al, 2006) and different reported microbes colonizing basaltic rocks (unpublished) (AB235231, KC682116, FJ497267, 98%). Another clone with long sequence (*458, 1350 bp) has as nearest references the uncultured Sulfurimonas assigned in an anoxic fjord in western Sweden (KC545729, 99%) (unpublished), another involved in S 0 -consumption in marine benthic habitats (KF624542, 98%) (Pjevac et al, 2014) and one uncultured bacterium in a near-shore anoxic basin (EU265985, 98%) (Schmidtova et al, 2009).…”

Impact of Seasonal Hypoxia on Activity and Community Structure of Chemolithoautotrophic Bacteria in a Coastal Sediment

“…In sulfidic marine sediments found in tidal and deep-sea habitats, complex S 0 niche partitioning has been proposed where uncultured sulfur-oxidizing Gammaproteobacteria mainly thrive on free sulfide, the epsilonproteobacterial Sulfurimonas/Sulfurovum group oxidizes elemental sulfur, and members of the deltaproteobacterial Desulfobulbaceae family may perform S 0 disproportionation (46).…”

High potential for temperate viruses to drive carbon cycling in chemoautotrophy‐dominated shallow‐water hydrothermal vents

“…To our knowledge, this represents the first experimental evidence of the potentially high functional impact of temperate viruses on natural microbial assemblages in chemoautotrophs‐dominated marine ecosystems (Howard‐Varona et al ., ). As epsilonproteobacteria, including the Sulfurovum gen ., can be abundant also in non‐vent environments (Pjevac et al ., ; ; Hamilton et al ., ), our results trigger future research on the possibly relevant role of similar provirus‐host dynamics also in other ecosystems.…”