Genomic evidence for sulfur intermediates as new biogeochemical hubs in a model aquatic microbial ecosystem

Abstract

Background The sulfur cycle encompasses a series of complex aerobic and anaerobic transformations of S-containing molecules and plays a fundamental role in cellular and ecosystem-level processes, influencing biological carbon transfers and other biogeochemical cycles. Despite their importance, the microbial communities and metabolic pathways involved in these transformations remain poorly understood, especially for inorganic sulfur compounds of intermediate oxidation states (thiosulfate, tetrathionate, sulfite, polysulfides). Isolated and highly stratified, the extreme geochemical and environmental features of meromictic ice-capped Lake A, in the Canadian High Arctic, provided an ideal model ecosystem to resolve the distribution and metabolism of aquatic sulfur cycling microorganisms along redox and salinity gradients. Results Applying complementary molecular approaches, we identified sharply contrasting microbial communities and metabolic potentials among the markedly distinct water layers of Lake A, with similarities to diverse fresh, brackish and saline water microbiomes. Sulfur cycling genes were abundant at all depths and covaried with bacterial abundance. Genes for oxidative processes occurred in samples from the oxic freshwater layers, reductive reactions in the anoxic and sulfidic bottom waters and genes for both transformations at the chemocline. Up to 154 different genomic bins with potential for sulfur transformation were recovered, revealing a panoply of taxonomically diverse microorganisms with complex metabolic pathways for biogeochemical sulfur reactions. Genes for the utilization of sulfur cycle intermediates were widespread throughout the water column, co-occurring with sulfate reduction or sulfide oxidation pathways. The genomic bin composition suggested that in addition to chemical oxidation, these intermediate sulfur compounds were likely produced by the predominant sulfur chemo- and photo-oxidisers at the chemocline and by diverse microbial degraders of organic sulfur molecules. Conclusions The Lake A microbial ecosystem provided an ideal opportunity to identify new features of the biogeochemical sulfur cycle. Our detailed metagenomic analyses across the broad physico-chemical gradients of this permanently stratified lake extend the known diversity of microorganisms involved in sulfur transformations over a wide range of environmental conditions. The results indicate that sulfur cycle intermediates and organic sulfur molecules are major sources of electron donors and acceptors for aquatic and sedimentary microbial communities in association with the classical sulfur cycle.

Metagenomic Views of Microbial Communities in Sand Sediments Associated with Coral Reefs

“…dimethyl sulfoxide (DMSO) are particularly abundant in coral reef and permeable coral reef carbonate sediments (Deschaseaux, et al 2019). Accordingly, genes for anaerobic dimethylsulfoxide reductase (dmsA) that converts DMSO to dimethyl sul de DMS were also identi ed in Proteobacteria, Desulfobacterota, Planctomycetota, and Bacteroidota genomes, accounting for 1.9% of total microbial cells and providing an alternative energy source under anoxic conditions (Vigneron, et al 2021).…”

Large and interacting effects of temperature and nutrient addition on stratified microbial ecosystems in a small, replicated, and liquid‐dominated Winogradsky column approach

“…The mentioned studies show that important insights come from analyses of observations of naturally occurring aquatic ecosystems (Vigneron et al, 2021), and theoretical models of the plausible and relevant ecological and biochemical processes. In addition, in the field of global change biology, targeted experiments that employ a limited number of standardized synthetic model ecosystems have been described as an “entirely different approach” (Hutchins et al, 2019) and are considered vital alongside studies of naturally occurring ecosystems (Lahti et al, 2014) and hybrids of both approaches (De Vos et al, 2017).…”

“…Stratification of lakes is a common seasonal phenomenon of the temperate zone, which is dependent on the depth and the surface area of the lake (Gorham & Boyce, 1989). Stratified lakes show warm and oxygen-rich upper water layers, dominated by cyanobacteria and algae, and colder (anoxic) deeper layers, that harbor heterotrophic biomass-degraders and sulfate-reducing bacteria (Diao et al, 2017(Diao et al, , 2018Guggenheim et al, 2020;Vigneron et al, 2021). In between these layers, the metalimnion can be found, which is formed by decreasing light-intensities and oxygen concentrations (microaerophilic), and an increasing pool of reduced sulfur compounds, creating ideal niches for phototrophic sulfur bacteria and chemolithoautotrophic micro-organisms (Bush et al, 2017;Diao et al, 2017Diao et al, , 2018Jorgensen et al, 1979;Morrison et al, 2017;Nyirabuhoro et al, 2020;Savvichev et al, 2018;Vavourakis et al, 2019;Vigneron et al, 2021;Wörner & Pester, 2019;Wu et al, 2019).…”

Vertical structure of the bacterial diversity in meromictic Fayetteville Green Lake

“…The distribution of these and other microbes may give insight into the microbial sulfur and carbon biogeochemical cycles of the lake (Øvreås et al, 1997; Scholten et al, 2005). In other meromictic lakes, characterization of the microbial communities throughout the water column has been useful in identifying important microbial groups in major biogeochemical cycles (Diao et al, 2018; Kojima et al, 2014; Vigneron et al, 2021). Here, we report the physicochemical characteristics and the results of 16S rRNA gene sequencing through the chemocline of FGL and compare our results to similar meromictic lakes.…”