The life sulfuric: microbial ecology of sulfur cycling in marine sediments

Abstract

Almost the entire seafloor is covered with sediments that can be more than 10 000 m thick and represent a vast microbial ecosystem that is a major component of Earth's element and energy cycles. Notably, a significant proportion of microbial life in marine sediments can exploit energy conserved during transformations of sulfur compounds among different redox states. Sulfur cycling, which is primarily driven by sulfate reduction, is tightly interwoven with other important element cycles (carbon, nitrogen, iron, manganese) and therefore has profound implications for both cellular- and ecosystem-level processes. Sulfur-transforming microorganisms have evolved diverse genetic, metabolic, and in some cases, peculiar phenotypic features to fill an array of ecological niches in marine sediments. Here, we review recent and selected findings on the microbial guilds that are involved in the transformation of different sulfur compounds in marine sediments and emphasise how these are interlinked and have a major influence on ecology and biogeochemistry in the seafloor. Extraordinary discoveries have increased our knowledge on microbial sulfur cycling, mainly in sulfate-rich surface sediments, yet many questions remain regarding how sulfur redox processes may sustain the deep-subsurface biosphere and the impact of organic sulfur compounds on the marine sulfur cycle.

Figure 1

Conceptual depiction of the sulfur cycle in marine sediments, including main reactions of inorganic and organic sulfur compounds, selected taxa, sulfur oxidation via long‐range electron transport by cable bacteria, sulfate‐dependent anaerobic methane oxidation, and transformations of sulfur compounds of intermediate oxidation states (sulfur cycle intermediates, SCI). Blue lines depict biologically‐mediated sulfur transformations that can also be components of disproportionation reactions. Orange lines depict abiotic reactions. Inorganic sulfur compounds are depicted within yellow eclipses. Other electron acceptors are depicted within orange ellipses, and electron donors are depicted within blue ellipses. OSM = organo‐sulfur molecules, C_org = organic matter. DIET = direct‐interspecies electron transport. ANME = anaerobic methane‐oxidising.

Figure 2

Phylogenetic tree showing the diversity of major DsrAB lineages, including sequences from the environment and isolated strains. The tree was based on a previously described DsrAB sequence set (Müller et al., 2015), including new sequences from the phyla Chloroflexi (Wasmund et al., 2016) and Gemmatimonadetes (Baker et al., 2015), and the candidate phylum Rokubacteria (Hug et al., 2016), and constructed with Fasttree (LG model of amino‐acid evolution) and an indel filter covering 530 alignment positions. Branches are unscaled. Clades with representatives from known phyla are labelled in different background colours. Desulfatiglans anilini lineage (not shown) is collapsed into the LA‐dsrAB Firmicutes group. Clades without cultured representatives are shown in grey. The three major DsrAB protein families, namely the reductive bacterial type, the oxidative bacterial type and the reductive archaeal type, are shown. The designation ‘uncultured DsrAB lineage’ depicts a stable, monophyletic lineage that consists only of environmental dsrAB sequences and has family‐level or higher taxon diversity. LA‐dsrAB, laterally acquired dsrAB. Moorella dsrAB copy 1 clustered with the LA‐dsrAB Firmicutes group. Selected accession numbers (for screen‐view only due to small font size) are given for some branches to aid in identification. See publication by Müller et al. (2015) for further information.