Ferrihydrite-associated organic matter (OM) stimulates reduction by <i>Shewanella oneidensis</i> MR-1 and a complex microbial consortia

Abstract

Abstract. The formation of Fe(III) oxides in natural environments occurs in the presence of natural organic matter (OM), resulting in the formation of OM-mineral complexes that form through adsorption or coprecipitation processes. Thus, microbial Fe(III) reduction in natural environments most often occurs in the presence of OM-mineral complexes rather than pure Fe(III) minerals. This study investigated to what extent does the content of adsorbed or coprecipitated OM on ferrihydrite influence the rate of Fe(III) reduction by Shewanella oneidensis MR-1, a model Fe(III)-reducing microorganism, in comparison to a microbial consortium extracted from the acidic, Fe-rich Schlöppnerbrunnen fen. We found that increased OM content led to increased rates of microbial Fe(III) reduction by S. oneidensis MR-1 in contrast to earlier findings with the model organism Geobacter bremensis. Ferrihydrite-OM coprecipitates were reduced slightly faster than ferrihydrites with adsorbed OM. Surprisingly, the complex microbial consortia stimulated by a mixture of electrons donors (lactate, acetate, and glucose) mimics S. oneidensis under the same experimental Fe(III)-reducing conditions suggesting similar mechanisms of electron transfer whether or not the OM is adsorbed or coprecipitated to the mineral surfaces. We also followed potential shifts of the microbial community during the incubation via 16S rRNA gene sequence analyses to determine variations due to the presence of adsorbed or coprecipitated OM-ferrihydrite complexes in contrast to pure ferrihydrite. Community profile analyses showed no enrichment of typical model Fe(III)-reducing bacteria, such as Shewanella or Geobacter sp., but an enrichment of fermenters (e.g., Enterobacteria) during pure ferrihydrite incubations which are known to use Fe(III) as an electron sink. Instead, OM-mineral complexes favored the enrichment of microbes including Desulfobacteria and Pelosinus sp., both of which can utilize lactate and acetate as an electron donor under Fe(III)-reducing conditions. In summary, this study shows that increasing concentrations of OM in OM-mineral complexes determines microbial Fe(III) reduction rates and shapes the microbial community structure involved in the reductive dissolution of ferrihydrite. Similarities observed between the complex Fe(III)-reducing microbial consortia and the model Fe(III)-reducer S. oneidensis MR-1 suggest electron-shuttling mechanisms dominate in OM-rich environments, including soils, sediments, and fens, where natural OM interacts with Fe(III) oxides during mineral formation.

Is microbial reduction of Fe (III) in podzolic soils influencing C release?

“…Accordingly, faster Fe(III) reduction rates were measured with increasing C load in fresh Fe-OM associations in studies using Shewanella spp. (Pédrot et al, 2011;Shimizu et al, 2013;Cooper et al, 2017;Adhikari et al, 2017), while an inhibition of the reduction of SRO-Fe oxide was observed with increasing adsorption or coprecipitation involving OC when Geobacter spp. is used (Eusterhues et al, 2014;Poggenburg et al, 2016).…”

“…In the literature, no clear picture has yet emerged regarding the impact of adsorbed and co-precipitated OM on the microbial reactivity of Fe phases. Previous studies (Pédrot et al, 2011;Shimizu et al, 2013;Eusterhues et al, 2014;Poggenburg et al, 2016;Adhikari et al, 2017;Cooper et al, 2017;Poggenburg et al, 2018) focused on fresh and synthetic OMA, but not on those formed in soils. Actually, fresh synthetic OMA considerably differ from natural soil OMA as they did not form from complex soil solutions and/or evolve from long-term transformations (Cornell and Schwertmann, 2003).…”

“…can use various strategies to reduce Fe(III) from oxidesi.e. direct contact, electron shuttles, or by production of complexing ligands like siderophores (Cooper et al, 2017) while Geobacter sp. does not produce electron-shuttling molecules or chelators relying mostly on direct contact (Nevin and Lovley, 2000).…”

Reactive Iron and Iron‐Bound Organic Carbon in Surface Sediments of the River‐Dominated Bohai Sea (China) Versus the Southern Yellow Sea

“…Due to the close association of riverine "dissolved" Fe with dissolved OM (DOM), Fe removal by flocculation and aggregation also renders concomitant removal of associated DOM (Forsgren et al, 1996;Fox, 1984;Jilbert et al, 2018). The concomitant flocculation of Fe and the associated DOM and their burial as Fe-OM aggregates in sediments may have profound influences on Fe geochemistry and OC burial because the interactions of OC with Fe exert an important control on biotic/abiotic reactivity of Fe oxides and OC stabilization against microbial decomposition by sorption on reactive Fe oxides (Cooper et al, 2017;Lalonde et al, 2012;Q. Zhao, Adhikari, et al, 2016;Q.…”

Fe(II)-catalyzed transformation of ferrihydrite associated with natural organic matter

“…Coprecipitated OM was found to reduce ferrihydrite bio-reduction rates (101). Some studies, however, found that coprecipitated humic acid reduced ferrihydrite bioreduction rates at low C/Fe ratios (≤ 0.8) but enhanced the extent of bio-reduction at high C/Fe ratios (≥ 1.8) (104,105).…”