Research Article: An integrated microbiological and electrochemical approach to determine distributions of Fe metabolism in acid mine drainage-induced “iron mound” sediments

Date Published: March 26, 2019

Publisher: Public Library of Science

Author(s): Andrew M. Leitholf, Chrystal E. Fretz, Raymond Mahanke, Zachary Santangelo, John M. Senko, Andrew R. Zimmerman.


Fe(III)-rich deposits referred to as “iron mounds” develop when Fe(II)-rich acid mine drainage (AMD) emerges at the terrestrial surface, and aeration of the fluids induces oxidation of Fe(II), with subsequent precipitation of Fe(III) phases. As Fe(III) phases accumulate in these systems, O2 gradients may develop in the sediments and influence the distributions and extents of aerobic and anaerobic microbiological Fe metabolism, and in turn the solubility of Fe. To determine how intrusion of O2 into iron mound sediments influences microbial community composition and Fe metabolism, we incubated samples of these sediments in a column format. O2 was only supplied through the top of the columns, and microbiological, geochemical, and electrochemical changes at discrete depths were determined with time. Despite the development of dramatic gradients in dissolved Fe(II) concentrations, indicating Fe(II) oxidation in shallower portions and Fe(III) reduction in the deeper portions, microbial communities varied little with depth, suggesting the metabolic versatility of organisms in the sediments with respect to Fe metabolism. Additionally, the availability of O2 in shallow portions of the sediments influenced Fe metabolism in deeper, O2-free sediments. Total potential (EH + self-potential) measurements at discrete depths in the columns indicated that Fe transformations and electron transfer processes were occurring through the sediments and could explain the impact of O2 on Fe metabolism past where it penetrates into the sediments. This work shows that O2 availability (or lack of it) minimally influences microbial communities, but influences microbial activities beyond its penetration depth in AMD-derived Fe(III) rich sediments. Our results indicate that O2 can modulate Fe redox state and solubility in larger volumes of iron mound sediments than only those directly exposed to O2.

Partial Text

Centuries of coal extraction in the Appalachian region of the United States has left a legacy of acid mine drainage (AMD), which remains the region’s greatest threat to surface water quality [1]. The major environmental damage caused by AMD occurs when the anoxic, acidic, and Fe(II)-rich fluid enters oxic, circumneutral streams, whereupon the higher pH enhances the oxidation of Fe(II) and precipitation of Fe(III) phases, which smother stream substrates and limit the development of robust stream ecosystems (e.g. algae, macroinvertebrates, fish; [2–4]). As such, removal of dissolved Fe(II) is the most pressing objective in AMD treatment and stream restoration activities [5]. In some cases, AMD flows as a 0.5–1 cm sheet over the terrestrial surface, resulting in aeration of the fluid and enhanced activities of Fe(II) oxidizing bacteria (FeOB; [6–11]). Continuous flow of AMD and sustained Fe(II) oxidation gives rise to massive Fe(III) (hydr)oxide deposits that are referred to as “iron mounds” or “iron terraces,” and can grow to thicknesses of meters [6, 7, 12]. While these iron mounds damage the soil and surficial systems that they cover, they may also be exploited for the treatment of AMD [6–11]. Under this scenario, the iron mounds represent iron removal systems, whereby the activities of FeOB induce oxidative removal of Fe from the AMD before the water enters nearby streams [6–11]. Notably, the iron mounds that we have encountered arise with little or no human intervention, suggesting that constructed iron mounds could serve as inexpensive and sustainable approaches to AMD treatment.

O2 availability, controlled by depth in the columns, minimally influenced the composition of microbial communities in iron mound sediments, but profoundly influenced their activities. The only phylotypes that exhibited a substantial change with depth at the conclusion of the column incubations were unassigned sequences that were similar to planktonic phylotypes observed in acidic (pH approximately 2) and high redox potential (approximately 470 mV) Rio Tinto, indicating that these organisms metabolize optimally under mostly oxic conditions [35, 38]. Otherwise, microbial communities throughout the remainder of the sediments were nearly identical (Fig 2E and S2 Fig). 16S rRNA gene-based surveys can still detect inactive organisms, which could explain the compositional similarities we have observed. In previous experiments at the Mushroom Farm, we have observed discernable shifts in microbial communities over shorter incubation times [9]. Additionally, a similar pattern of microbial community composition was observed in intact iron mound microbial communities [12]. In that case, relative abundances of phylotypes attributable to photosynthetic microeukaryotes and obligately aerobic, Fe(II) oxidizing Gallionella sp. diminished in deeper portions of the sediments, but other components of the microbial communities retained similar relative abundances [12]. The most notable constants in situ were Gammaproteobacteria assignable to Fe-metabolizing Xanthomonadaceae [12], which also remained abundant at the conclusion of our column incubations (Fig 2E). These observations illustrate the metabolic versatility of microorganisms with respect to Fe metabolism in AMD and AMD-impacted systems. They are often capable of Fe(II) oxidation and Fe(III) reduction, depending to some extent (but not completely) on the availability of O2 [14, 37, 39–41]. In the current work, we started with a homogenized microbial community from the upper 6 cm of an iron mound and challenged that community to adjust to limitations on O2 delivery. The communities did not vary dramatically from a compositional perspective, but exhibited dramatic differences in their activities.




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