Microbial regeneration and respiration of Fe(III) outcompetes sulphate respiration in ferruginous, high-sulphate oligotrophic ecosystems

 

In anoxic lacustrine systems, at low-sulphate concentrations, sulphidisation acts as a crucial pathway driving the reductive dissolution of amorphous and nanocrystalline Fe-(oxyhydr)oxides in the presence of dissolved organic matter. The cycling of intermediate sulphur through a disproportionation reaction with the available Fe(III) stocks supports a continued intermediate sulphur-based respiration mechanism often referred to as cryptic. The prevalence of the so-called cryptic mechanism in meromictic, low-sulphate lakes could be attributed to the abundance of crystalline as opposed to more reactive amorphous iron (oxyhyd)roxides, which by immobilizing ferric iron also favour microbial sulphate reduction (MSR) promoting the accumulation of solid phase intermediate sulphur and sulphides^[1]. In a ferruginous, sulphate-rich and oligotrophic post-mining lake (Lake Medard, Czech Republic) we observed a departure from this condition as dissolved sulphide does not accumulate in the bottom water column nor precipitate in the anoxic sediments.^[2] Analyses of the bacterioplankton abundance in the hypolimnion indicate a marked niche compartmentalization, with Fe(II)-oxidising microbes, such as Gallionella sp., Rhodopseudomonas sp. and Sideroxydans sp., being important at the dysoxic to anoxic (ferruginous) interface where they drive the regeneration of ferric iron. On the other hand, Fe(III)-reducers, such as Geobacter sp. and Rhodoferax sp. are present at the O₂-depleted monimolimnion and in the uppermost anoxic sediments. Toward the redox interface, the chemolithotrophic community described above allows for Fe-(re)cycling and drives the oxidation and turnover of the scarcely available volatile fatty acids. Sulphate reducers (e.g. Desulfobulbaceae, Chrostridia, Desulfarculus) and microorganisms capable of anammox, such as Nitrosomonas  and Nitrosospira where found below the redoxcline. However, together these obligate anaerobes account for < 4% of the total bacterial OTUs identified in the monimolimnion. Our observations in this purported modern analogue to ferruginous, relatively sulphate-enriched Precambrian coastal zones raise the possibility that limited dissimilatory sulphate reduction in the Earth’s primitive ferruginous oceans was rather linked to the scarcity of suitable organic substrates and high rates of Fe-(re)cycling than to low levels of dissolved sulphate. The co-precipitation of minor amounts of gypsum/anhydrite and siderite, with Fe(II,III)-(oxyhydr)oxides further support a potential link between the deep Lake Medard precipitation environment and certain mid- to Late-Archean marginal settings, where these phases have been described to be primary and/or early diagenetic in origin. 

^[1] Hansel, C.M., Lentini, C.J., Tang, Y., et al. ISME J. 9, 2400–2412 (2015). 

^[2] Petrash, D.A., Jan, J., Sirová, et al. Environ. Sci. Process. Impacts 20, 1414–1426 (2018).