Niche partitioning of diverse sulfur-oxidizing bacteria at hydrothermal vents

Abstract

At deep-sea hydrothermal vents, primary production is carried out by chemolithoautotrophic microorganisms, with the oxidation of reduced sulfur compounds being a major driver for microbial carbon fixation. Dense and highly diverse assemblies of sulfur-oxidizing bacteria (SOB) are observed, yet the principles of niche differentiation between the different SOB across geochemical gradients remain poorly understood. In this study niche differentiation of the key SOB was addressed by extensive sampling of active sulfidic vents at six different hydrothermal venting sites in the Manus Basin, off Papua New Guinea. We subjected 33 diffuse fluid and water column samples and 23 samples from surfaces of chimneys, rocks and fauna to a combined analysis of 16S rRNA gene sequences, metagenomes and real-time in situ measured geochemical parameters. We found Sulfurovum Epsilonproteobacteria mainly attached to surfaces exposed to diffuse venting, while the SUP05-clade dominated the bacterioplankton in highly diluted mixtures of vent fluids and seawater. We propose that the high diversity within Sulfurimonas- and Sulfurovum-related Epsilonproteobacteria observed in this study derives from the high variation of environmental parameters such as oxygen and sulfide concentrations across small spatial and temporal scales.

Spatially distinct, temporally stable microbial populations mediate biogeochemical cycling at and below the seafloor in hydrothermal vent fluids

“…In addition, a study within a single vent field at Axial Seamount showed differences in gene expression patterns between both diffuse vents as well as within the intra‐field waters between vent sites (Olins et al ., ). Finally, through the reconstruction of genomes from metagenomes (Tyson et al ., ; Dick et al ., ; Hug et al ., ), recent genomic binning studies at hydrothermal systems have revealed the presence of novel microbial and viral groups as well as their metabolic potential, including the discovery of auxiliary metabolic genes for sulfur oxidation within deep ocean viruses and the potential importance of hydrocarbon degradation distal to venting fluids, including within hydrothermal plumes (Anantharaman et al ., ; Li et al ., ; Sheik et al ., ; Meier et al ., ).…”

“…Recently, a number of metagenomic and metatranscriptomic studies of microbial communities within and around hydrothermal vents have led to new insights about the diversity of microbial metabolisms present and expressed under different geological and chemical conditions (e.g., Dick et al ., ; Urich et al ., ; Li et al ., ; Anantharaman et al ., ; Fortunato and Huber, ; Meier et al ., ; Reveillaud et al ., ; Olins et al ., ). For example, hydrothermal vent plumes sampled above the seafloor were shown to vary chemically and be taxonomically and metabolically distinct from seafloor vent fluid and subseafloor communities (Dick et al ., ).…”

Transcriptomic and proteomic insight into the mechanism of cyclooctasulfur‐ versus thiosulfate‐oxidation by the chemolithoautotroph Sulfurimonas denitrificans

“…In addition to the described function in S. denitrificans , the soxY 2 Z 2 genes of the soxCD Y 2 Z 2 operon show a much higher level of diversification between different Sulfurimonas and Sulfurovum species (up to 79% nucleotide sequence dissimilarity) than soxY 1 Z 1 of the soxABXY 1 Z 1 operon (Meier et al ., ). Moreover, the sequence similarity between the two SoxYZ copies in S. denitrificans and other Campylobacteria is very low.…”

“…In fact, no significant identity, except for the export signal sequence, is detectable on the nucleotide level for either gene. This highly divergent intragenomic duplication, and the intergenomic diversification of the SoxY 2 Z 2 proteins, is present in all currently available Sulfurimonas and Sulfurovum genomes (Meier et al ., ). Furthermore, a significantly higher expression level of SoxY 2 Z 2 proteins when compared with SoxY 1 Z 1 proteins has been found in the metaproteomes of Campylobacteria ‐dominated biofilms forming on black‐smoker chimneys (Pjevac et al ., ).…”

“…With the exception of the potential involvement of the hypothetical protein in the activation and transport of S 8 into the cell, we were not able to identify a possible mechanism for the activation of cyclooctasulfur, as has for example been proposed for acidophilic sulfur‐oxidizing bacteria (Rohwerder and Sand, ; Mangold et al ., ; Chen et al ., ). However, our data confirm the previously hypothesized differential regulation of the two SOX gene clusters present in S. denitrificans in response to the available sulfur substrate (Sievert et al ., ; Meier et al ., ; Pjevac et al ., ), allowing us to propose a possible oxidation pathway. In thiosulfate‐grown cultures, the first gene cluster encoding soxABXY 1 Z 1 was highly transcribed and the corresponding proteins were found in significantly higher abundance compared with growth with S 8 , confirming their involvement in thiosulfate oxidation as previously proposed (Friedrich et al ., , ).…”