Active sulfur cycling in the terrestrial deep subsurface

Abstract

The deep terrestrial subsurface remains an environment where there is limited understanding of the extant microbial metabolisms. At Olkiluoto, Finland, a deep geological repository is under construction for the final storage of spent nuclear fuel. It is therefore critical to evaluate the potential impact microbial metabolism, including sulfide generation, could have upon the safety of the repository. We investigated a deep groundwater where sulfate is present, but groundwater geochemistry suggests limited microbial sulfate-reducing activity. Examination of the microbial community at the genome-level revealed microorganisms with the metabolic capacity for both oxidative and reductive sulfur transformations. Deltaproteobacteria are shown to have the genetic capacity for sulfate reduction and possibly sulfur disproportionation, while Rhizobiaceae, Rhodocyclaceae, Sideroxydans, and Sulfurimonas oxidize reduced sulfur compounds. Further examination of the proteome confirmed an active sulfur cycle, serving for microbial energy generation and growth. Our results reveal that this sulfide-poor groundwater harbors an active microbial community of sulfate-reducing and sulfide-oxidizing bacteria, together mediating a sulfur cycle that remained undetected by geochemical monitoring alone. The ability of sulfide-oxidizing bacteria to limit the accumulation of sulfide was further demonstrated in groundwater incubations and highlights a potential sink for sulfide that could be beneficial for geological repository safety.

Bacterial and Archaeal Diversity and Abundance in Shallow Subsurface Clay Sediments at Jianghan Plain, China

“…In addition, Woesearchaeota were mainly found in upper sediment samples from the borehole (Supplementary Figure 3), which coincide with its wide ecological niches ranging from oxic to anoxic biotopes and might provide a series of intermediates for other aerobes and anaerobes due to reported heterotrophic and syntrophic lifestyle (Castelle et al, 2015;Liu et al, 2018). The sediments of A3 and A4 were characterized by the significant portion of microbial populations associated with reductions of nitrate (Anaeromyxobacter and nitratedependent methanotrophic Methanoperedens-like archaea), Fe (Anaeromyxobacter and Chloroflexi bacterium RBG_16_58_14), and sulfate (Deltaproteobacteria) ( Supplementary Figure 3; He and Sanford, 2003;Muyzer and Stams, 2008;Anantharaman et al, 2016;Welte et al, 2016;Bell et al, 2020). This is consistent with observations of low levels of nitrate and sulfate, but high level of HCl-extractable Fe 2+ in the samples A3 and A4, which further support the idea of an oxic to anoxic transition between the sediments of A2 and A3 (Figure 2).…”

Multiple role of diazotrophs in coupling nitrogen and iron biogeochemical processes through vertical soil profiles of different paddy soil types

“…Combined with previous reports that showed the S-driven Fe reduction coupled to anaerobic ammonium oxidation [21] , these data highlighted that the biogeochemical cycling of S, Fe and N could be coupled in Hapli-type anthrosol. To gain comprehensive and deeper understanding of mechanism coupling multielement biogeochemical processes in paddy soils, metagenomic approaches and hydrogeochemical evidences for element transformation should be further considered [58] .…”

A biochemical view on the biological sulfur cycle

“…For example, cryptic sulfur cycling is inferred to occur in sediments from Aarhus Bay (Baltic Sea) (Holmkvist et al, 2011) and Black Sea sediments (Mikucki et al, 2009) that were considered to be devoid of active sulfate reduction. Cryptic sulfur cycling has furthermore been described for subglacial lakes where sulfate-sulfur is apparently reduced and re-oxidized back via coupling to reductive iron cycling (Mikucki et al, 2009), for sulfide-poor groundwater of the deep terrestrial subsurface (Bell et al, 2020) as well as for marine oxygen minimum zones (Canfield et al, 2010;Johnston et al, 2014) where extensive sulfur cycles are presumably tied to reductive nitrogen cycling.…”

“…Rather, sulfur-oxidizing capabilities were assigned to organisms grouped into families known for metabolic versatility, e.g. the alphaproteobacterial Rhodobacteraceae, Rhodocyclaceae or Rhizobicaceae (Bell et al, 2020;Lenk et al, 2012).…”