Geochemical Niches of Iron-Oxidizing Acidophiles in Acidic Coal Mine Drainage

Jones, Daniel S.; Kohl, Courtney; Grettenberger, Christen L.; Larson, Lance N.; Burgos, William D.; Macalady, Jennifer L.

doi:10.1128/aem.02919-14

Cited by 69 publications

(49 citation statements)

References 51 publications

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“…The FISH counts for three AMD taxa (an acidophilic Gallionella sp., Acidithiobacillus ferrooxidans, and Ferrovum myxofaciens) were retrieved from Jones et al (13) and Brown et al (14) and combined with the counts from Scalp Level Run. A local polynomial regression (Loess) curve was fitted to the relationship of pH and relative abundance for each taxon using a span value of 1 in the "loess" command in R (51).…”

Section: Methodsmentioning

confidence: 99%

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Efficient Low-pH Iron Removal by a Microbial Iron Oxide Mound Ecosystem at Scalp Level Run

Grettenberger

Pearce

Bibby

et al. 2017

Appl Environ Microbiol

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Acid mine drainage (AMD) is a major environmental problem affecting tens of thousands of kilometers of waterways worldwide. Passive bioremediation of AMD relies on microbial communities to oxidize and remove iron from the system; however, iron oxidation rates in AMD environments are highly variable among sites. At Scalp Level Run (Cambria County, PA), first-order iron oxidation rates are 10 times greater than at other coal-associated iron mounds in the Appalachians. We examined the bacterial community at Scalp Level Run to determine whether a unique community is responsible for the rapid iron oxidation rate. Despite strong geochemical gradients, including a Ͼ10-fold change in the concentration of ferrous iron from 57.3 mg/liter at the emergence to 2.5 mg/liter at the base of the coal tailings pile, the bacterial community composition was nearly constant with distance from the spring outflow. Scalp Level Run contains many of the same taxa present in other AMD sites, but the community is dominated by two strains of Ferrovum myxofaciens, a species that is associated with high rates of Fe(II) oxidation in laboratory studies.IMPORTANCE Acid mine drainage pollutes more than 19,300 km of rivers and streams and 72,000 ha of lakes worldwide. Remediation is frequently ineffective and costly, upwards of $100 billion globally and nearly $5 billion in Pennsylvania alone. Microbial Fe(II) oxidation is more efficient than abiotic Fe(II) oxidation at low pH (P. C. Singer and W. Stumm, Science 167:1121-1123, 1970, https://doi.org/10.1126/ science.167.3921.1121). Therefore, AMD bioremediation could harness microbial Fe(II) oxidation to fuel more-cost-effective treatments. Advances will require a deeper understanding of the ecology of Fe(II)-oxidizing microbial communities and the factors that control their distribution and rates of Fe(II) oxidation. We investigated bacterial communities that inhabit an AMD site with rapid Fe(II) oxidation and found that they were dominated by two operational taxonomic units (OTUs) of Ferrovum myxofaciens, a taxon associated with high laboratory rates of iron oxidation. This research represents a step forward in identifying taxa that can be used to enhance costeffective AMD bioremediation.KEYWORDS Ferrovum myxofaciens, acid mine drainage, environmental microbiology, extremophiles, iron oxidation A cid mine drainage (AMD) is a devastating and widespread industrial pollution problem (1-6). The effects of AMD are felt especially hard in the Appalachian Plateau in the eastern United States, where over 8,000 km of streams are polluted by

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Section: Methodsmentioning

confidence: 99%

“…1) are 10 times greater than those at other sites in Pennsylvania and the Iberian Pyrite Belt (13). We hypothesized that a unique bacterial community is responsible for the rapid oxidation of Fe(II) at Scalp Level Run.…”

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Efficient Low-pH Iron Removal by a Microbial Iron Oxide Mound Ecosystem at Scalp Level Run

Grettenberger

Pearce

Bibby

et al. 2017

Appl Environ Microbiol

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“…Hydrodynamic variables, such as velocity, retention time, turbulence, and precipitation patterns, can also affect microbial community dynamics (32,33). Across so-called terraced iron formations (TIFs), geochemical gradients establish such that Fe(II) and pH covary across each site (19,(34)(35)(36). At TIF sites in the Appalachian bituminous coal basin, microbial assemblages have been well explained by the combination of pH and Fe(II) concentration (19,36).…”

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confidence: 99%

“…Natural or engineered TIFs can be used to oxidize Fe(II) and remove total iron [Fe(T)] in passive treatment systems (34)(35)(36)(37)(38). Active bioreactors can also effectively oxidize Fe(II) and remove Fe(T) from solution and are considerably more effective than passive systems on a space basis.…”

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confidence: 99%

Geochemical and Temporal Influences on the Enrichment of Acidophilic Iron-Oxidizing Bacterial Communities

Sheng

Bibby

Grettenberger

et al. 2016

Appl Environ Microbiol

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Two acid mine drainage (AMD) sites in the Appalachian bituminous coal basin were selected to enrich for Fe(II)-oxidizing microbes and measure rates of low-pH Fe(II) oxidation in chemostatic bioreactors. Microbial communities were enriched for 74 to 128 days in fed-batch mode, then switched to flowthrough mode (additional 52 to 138 d) to measure rates of Fe(II) oxidation as a function of pH (2.1 to 4.2) and influent Fe(II) concentration (80 to 2,400 mg/liter). Biofilm samples were collected throughout these operations, and the microbial community structure was analyzed to evaluate impacts of geochemistry and incubation time. Alpha diversity decreased as the pH decreased and as the Fe(II) concentration increased, coincident with conditions that attained the highest rates of Fe(II) oxidation. The distribution of the seven most abundant bacterial genera could be explained by a combination of pH and Fe(II) concentration. Acidithiobacillus, Ferrovum, Gallionella, Leptospirillum, Ferrimicrobium, Acidiphilium, and Acidocella were all found to be restricted within specific bounds of pH and Fe(II) concentration. Temporal distance, defined as the cumulative number of pore volumes from the start of flowthrough mode, appeared to be as important as geochemical conditions in controlling microbial community structure. Both alpha and beta diversities of microbial communities were significantly correlated to temporal distance in the flowthrough experiments. Even after long-term operation under nearly identical geochemical conditions, microbial communities enriched from the different sites remained distinct. While these microbial communities were enriched from sites that displayed markedly different field rates of Fe(II) oxidation, rates of Fe(II) oxidation measured in laboratory bioreactors were essentially the same. These results suggest that the performance of suspended-growth bioreactors for AMD treatment may not be strongly dependent on the inoculum used for reactor startup. IMPORTANCEThis study showed that different microbial communities enriched from two sites maintained distinct microbial community traits inherited from their respective seed materials. Long-term operation (up to 128 days of fed-batch enrichment followed by up to 138 days of flowthrough experiments) of these two systems did not lead to the same, or even more similar, microbial communities. However, these bioreactors did oxidize Fe(II) and remove total iron [Fe(T)] at very similar rates. These results suggest that the performance of suspended-growth bioreactors for AMD treatment may not be strongly dependent on the inoculum used for reactor startup. This would be advantageous, because system performance should be well constrained and predictable for many different sites. N iche models use environmental and geochemical information to explain and predict the composition and diversity of microbial communities. In these models, different geochemical conditions act as key niche parameters controlling microbial community composition. For example, pH (1-4),...

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“…is meanwhile a third candidate for playing a role in ferrous iron oxidation at acidic conditions (Hallberg, 2010). Brown et al (2011) andJones et al (2011) proposed recently that pH and ferrous iron concentration could dictate whether Ferrovum or Acidithiobacillus might dominate a microbial consortium. Their assumption is corroborated by the results from this and a previous study from Ziegler et al (2009).…”

Section: Microbial Niches In the Biofilmmentioning

confidence: 99%

Oxygen-dependent niche formation of a pyrite-dependent acidophilic consortium built by archaea and bacteria

et al. 2013

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Biofilms can provide a number of different ecological niches for microorganisms. Here, a multispecies biofilm was studied in which pyrite-oxidizing microbes are the primary producers. Its stability allowed not only detailed fluorescence in situ hybridization (FISH)-based characterization of the microbial population in different areas of the biofilm but also to integrate these results with oxygen and pH microsensor measurements conducted before. The O 2 concentration declined rapidly from the outside to the inside of the biofilm. Hence, part of the population lives under microoxic or anoxic conditions. Leptospirillum ferrooxidans strains dominate the microbial population but are only located in the oxic periphery of the snottite structure. Interestingly, archaea were identified only in the anoxic parts of the biofilm. The archaeal community consists mainly of so far uncultured Thermoplasmatales as well as novel ARMAN (Archaeal Richmond Mine Acidophilic Nanoorganism) species. Inductively coupled plasma analysis and X-ray absorption near edge structure spectra provide further insight in the biofilm characteristics but revealed no other major factors than oxygen affecting the distribution of bacteria and archaea. In addition to catalyzed reporter deposition FISH and oxygen microsensor measurements, microautoradiographic FISH was used to identify areas in which active CO 2 fixation takes place. Leptospirilla as well as acidithiobacilli were identified as primary producers. Fixation of gaseous CO 2 seems to proceed only in the outer rim of the snottite. Archaea inhabiting the snottite core do not seem to contribute to the primary production. This work gives insight in the ecological niches of acidophilic microorganisms and their role in a consortium. The data provided the basis for the enrichment of uncultured archaea.

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Geochemical Niches of Iron-Oxidizing Acidophiles in Acidic Coal Mine Drainage

Cited by 69 publications

References 51 publications

Efficient Low-pH Iron Removal by a Microbial Iron Oxide Mound Ecosystem at Scalp Level Run

Efficient Low-pH Iron Removal by a Microbial Iron Oxide Mound Ecosystem at Scalp Level Run

Geochemical and Temporal Influences on the Enrichment of Acidophilic Iron-Oxidizing Bacterial Communities

Oxygen-dependent niche formation of a pyrite-dependent acidophilic consortium built by archaea and bacteria

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