Microbial diversity involved in iron and cryptic sulfur cycling in the ferruginous, low-sulfate waters of Lake Pavin.

Jasmine S Berg,Christel Laberty-Robert,Dominique Lamy,Jennyfer Miot,Arnaud Duverger,Didier Jézéquel,John M Senko

doi:10.1371/journal.pone.0212787

Abstract

Both iron- and sulfur- reducing bacteria strongly impact the mineralogy of iron, but their activity has long been thought to be spatially and temporally segregated based on the higher thermodynamic yields of iron over sulfate reduction. However, recent evidence suggests that sulfur cycling can predominate even under ferruginous conditions. In this study, we investigated the potential for bacterial iron and sulfur metabolisms in the iron-rich (1.2 mM dissolved Fe2+), sulfate-poor (< 20 μM) Lake Pavin which is expected to host large populations of iron-reducing and iron-oxidizing microorganisms influencing the mineralogy of iron precipitates in its permanently anoxic bottom waters and sediments. 16S rRNA gene amplicon libraries from at and below the oxycline revealed that highly diverse populations of sulfur/sulfate-reducing (SRB) and sulfur/sulfide-oxidizing bacteria represented up to 10% and 5% of the total recovered sequences in situ, respectively, which together was roughly equivalent to the fraction of putative iron cycling bacteria. In enrichment cultures amended with key iron phases identified in situ (ferric iron phosphate, ferrihydrite) or with soluble iron (Fe2+), SRB were the most competitive microorganisms, both in the presence and absence of added sulfate. The large fraction of Sulfurospirillum, which are known to reduce thiosulfate and sulfur but not sulfate, present in all cultures was likely supported by Fe(III)-driven sulfide oxidation. These results support the hypothesis that an active cryptic sulfur cycle interacts with iron cycling in the lake. Analyses of mineral phases showed that ferric phosphate in cultures dominated by SRB was transformed to vivianite with concomitant precipitation of iron sulfides. As colloidal FeS and vivianite have been reported in the monimolimnion, we suggest that SRB along with iron-reducing bacteria strongly influence iron mineralogy in the water column and sediments of Lake Pavin.

Highlights

Ferric iron (Fe3+) and sulfate (SO42-) reduction together are quantitatively the most important terminal electron accepting processes in both freshwater and marine anoxic environments (e.g., [1,2,3])
While other studies have highlighted the importance of facultative in iron reduction in Lake Pavin [41,42], we found that populations of Geothrix and Geobacter together constituted a large proportion of iron-reducing bacteria (IRB) at all depths
We identified the potential for microbial iron and sulfur cycling likely influencing the iron mineralogy at the redox transition zone of Lake Pavin

Summary

Introduction

Ferric iron (Fe3+) and sulfate (SO42-) reduction together are quantitatively the most important terminal electron accepting processes in both freshwater and marine anoxic environments (e.g., [1,2,3]). Iron, being the 4th most abundant element in the Earth’s crust, is ubiquitous in freshwater and marine sediments and is greatly exploited by microbial respiration processes there Competition between microbial iron and sulfate reduction for organic carbon sources and electron donors is governed by thermodynamic yields which are in turn pH- and iron-mineral-dependent Even in freshwater systems, where sulfate concentrations are typically 100–1,000 times lower than in seawater, high rates of microbial sulfate reduction can be sustained through rapid re-oxidation of sulfide by sulfide-oxidizing prokaryotes or by abiotic reactions with ferric iron species, and possibly by redox-active organic substances, e.g. certain humic acids [12]

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Results

Conclusion