Oscillations between reducing and oxidizing conditions are observed at the interface of anaerobic/oxic and anaerobic/anoxic environments, and are often stimulated by an alternating flux of electron donors (e.g., organic carbon) and electron acceptors (e.g., O2 and NO3−). In iron (Fe) rich soils and sediments, these oscillations may stimulate the growth of both Fe-reducing bacteria (FeRB) and Fe-oxidizing bacteria (FeOB), and their metabolism may induce cycling between Fe(II) and Fe(III), promoting the transformation of Fe (hydr)oxide minerals. Here, we examine the mineralogical evolution of lepidocrocite and ferrihydrite, and the adaptation of a natural microbial community to alternating Fe-reducing (anaerobic with addition of glucose) and Fe-oxidizing (with addition of nitrate or air) conditions. The growth of FeRB (e.g., Geobacter) is stimulated under anaerobic conditions in the presence of glucose. However, the abundance of these organisms depends on the availability of Fe(III) (hydr)oxides. Redox cycling with nitrate results in decreased Fe(II) oxidation thereby decreasing the availability of Fe(III) for FeRB. Additionally, magnetite is detected as the main product of both lepidocrocite and ferrihydrite reduction. In contrast, introduction of air results in increased Fe(II) oxidation, increasing the availability of Fe(III) and the abundance of Geobacter. In the lepidocrocite reactors, Fe(II) oxidation by dissolved O2 promotes the formation of ferrihydrite and lepidocrocite, whereas in the ferrihydrite reactors we observe a decrease in magnetite stoichiometry (e.g., oxidation). Understanding Fe (hydr)oxide transformation under environmentally relevant redox cycling conditions provides insight into nutrient availability and transport, contaminant mobility, and microbial metabolism in soils and sediments.
Dissimilatory iron-reducing bacteria (DIRB) are known to use humic substances (HS) as electron shuttles for dissimilatory iron reduction (DIR) by transferring electrons to HS-quinone moieties, which in turn rapidly reduce Fe(III) oxides. However, the potential for HS to serve as a source of organic carbon (OC) that can donate electrons for DIR is unknown. We studied whether humic acids (HA) and humins (HM) recovered from peat soil by sodium pyrophosphate extraction could serve as both electron shuttles and electron donors for DIR by freshwater sediment microorganisms. Both HA and HM served as electron shuttles in cultures amended with glucose. However, only HA served as an electron donor for DIR. Metagenomes from HA-containing cultures had an overrepresentation of genes involved in polysaccharide and to a lesser extent aromatic compound degradation, suggesting complex OC metabolism. Genomic searches for the porin-cytochrome complex involved in DIR resulted in matches to Ignavibacterium/Melioribacter, DIRB capable of polymeric OC metabolism. These results indicate that such taxa may have played a role in both DIR and decomposition of complex OC. Our results suggest that decomposition of HS coupled to DIR and other anaerobic pathways could play an important role in soil and sediment OC metabolism.
Recent studies have suggested the potential for release of iron (hydr)oxide-bound organic carbon (OC) during dissimilatory iron oxide reduction (DIR). However, the stability of iron (hydr)oxide-bound OC in the presence of a natural microbial consortium capable of driving both OC metabolism and DIR has not been resolved. Pure ferrihydrite (Fhy) and Fhy−humic acid coprecipitates (Fhy-HA) were inoculated with a small quantity of freshwater sediment and incubated under anoxic conditions in the presence and absence of H 2 or glucose as electron donors for DIR. H 2 promoted DIR led to release of ca. 1 mM dissolved organic carbon (DOC). However, comparable amounts of DOC were released from both pure Fhy and Fhy-HA, similar to DOC levels in mineral-free, inoculum-only controls. These results suggest that the observed DOC release during H 2 -promoted DIR originated from OC contained in the inoculum as opposed to the much larger pool (ca. 38 mM) of OC in the Fhy-HA. Thus, DIR preferentially released sorbed OC with low aromaticity (inoculum OC) versus highly aromatic OC (HA) coprecipitated with iron oxide. Our findings provide new insight into the extent and mechanisms by which DIR is likely to influence aqueous/solidphase OC partitioning in anoxic soils and sediments.
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