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

Date Published: February 22, 2019

Publisher: Public Library of Science

Author(s): Jasmine S. Berg, Didier Jézéquel, Arnaud Duverger, Dominique Lamy, Christel Laberty-Robert, Jennyfer Miot, John M. Senko.

http://doi.org/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.

Partial Text

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., [1–3]). Iron, being the 4th most abundant element in the Earth’s crust, is ubiquitous in freshwater and marine sediments and is therefore greatly exploited by microbial respiration processes there (e.g. [4,5]). Sulfate is the 2nd most abundant dissolved anion in seawater and is often utilized to such an extent that it becomes depleted in the upper centimeters of marine sediments [6]. 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 (e.g. [7]). Under acidic to neutral conditions predominating in most natural waters, Fe(III) reduction to Fe(II) is expected to be thermodynamically more favorable than sulfate reduction to sulfide (ΣH2S). Iron-reducing bacteria have therefore long been thought to outcompete sulfate-reducing bacteria for electron donors, leading to inhibition of sulfate reduction in iron-rich, sulfate-poor zones [8]. However, the dynamics governing the competition between iron- and sulfate-reducing bacteria have recently been re-examined as concomitant iron and sulfate reduction [9,10], as well as the dominance of sulfate reduction over iron reduction [11] have been observed. 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].

In this study, we identified the potential for microbial iron and sulfur cycling likely influencing the iron mineralogy at the redox transition zone of Lake Pavin. While it is difficult to distinguish between the relative contributions of abiotic (sulfide-driven) iron reduction versus dissimilatory iron reduction, our data show that there is a great potential for microbial iron-reducing activity in the lake water column. Compared to other stratified lakes where phototrophic iron and sulfide oxidation has been described (Lake Matano, Lake La Cruz, Lake Cadagno), Lake Pavin appears to be relatively poor in phototrophic IOB and SOB which constituted only a tiny fraction (< 0.3%) of our 16S rRNA gene libraries. Instead, the identification of microaerobic to anaerobic, chemotrophic IOB in situ, together with the formation of the iron oxide lepidocrocite in one enrichment culture, suggests that microbial iron oxidation with oxygen or nitrate may influence iron mineral transformations in the water column. Since nitrate reduction appears to occur just below the oxycline [77], Lake Pavin may be a promising environment for the targeted cultivation and isolation of nitrate-dependent Fe(II)-oxidizers which have not yet been identified in water column environments.   Source: http://doi.org/10.1371/journal.pone.0212787

 

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