Sustained Anthropogenic Impact in Carter Saltpeter Cave, Carter County, Tennessee and the Potential Effects on Manganese Cycling

Carmichael, Sarah K.; Carmichael, Mary Jane; Strom, Amanda; Johnson, K. W.; Roble, Leigh Anne; Gao, Yongli; Bräuer, Suzanna L.

doi:10.4311/2012mb0267

Cited by 9 publications

(19 citation statements)

References 69 publications

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“…Ferromanganese precipitates from Daniel Boone Caverns, a relatively pristine epigene karst cave in the Tennessee River Basin (Carmichael, Carmichael, Santelli, Strom, & Bräuer, ; Carmichael, Carmichael, Storm, et al., ), were collected in June 2014. Mn oxides form within biofilms, as coatings on rocks in pools or under seeps, as crusts along cave walls and speleothems, and as particles within mud formed by mineral weathering processes.…”

Section: Methodssupporting

confidence: 81%

Biogenic manganese oxides as reservoirs of organic carbon and proteins in terrestrial and marine environments

et al. 2016

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Manganese (Mn) oxides participate in a range of interactions with organic carbon (OC) that can lead to either carbon degradation or preservation. Here, we examine the abundance and composition of OC associated with biogenic and environmental Mn oxides to elucidate the role of Mn oxides as a reservoir for carbon and their potential for selective partitioning of particular carbon species. Mn oxides precipitated in natural brackish waters and by Mn(II)-oxidizing marine bacteria and terrestrial fungi harbor considerable levels of organic carbon (4.1-17.0 mol OC per kg mineral) compared to ferromanganese cave deposits which contain 1-2 orders of magnitude lower OC. Spectroscopic analyses indicate that the chemical composition of Mn oxide-associated OC from microbial cultures is homogeneous with bacterial Mn oxides hosting primarily proteinaceous carbon and fungal Mn oxides containing both protein- and lipopolysaccharide-like carbon. The bacterial Mn oxide-hosted proteins are involved in both Mn(II) oxidation and metal binding by these bacterial species and could be involved in the mineral nucleation process as well. By comparison, the composition of OC associated with Mn oxides formed in natural settings (brackish waters and particularly in cave ferromanganese rock coatings) is more spatially and chemically heterogeneous. Cave Mn oxide-associated organic material is enriched in aliphatic C, which together with the lower carbon concentrations, points to more extensive microbial or mineral processing of carbon in this system relative to the other systems examined in this study, and as would be expected in oligotrophic cave environments. This study highlights Mn oxides as a reservoir for carbon in varied environments. The presence and in some cases dominance of proteinaceous carbon within the biogenic and natural Mn oxides may contribute to preferential preservation of proteins in sediments and dominance of protein-dependent metabolisms in the subsurface biosphere.

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Section: Methodssupporting

confidence: 81%

Biogenic manganese oxides as reservoirs of organic carbon and proteins in terrestrial and marine environments

et al. 2016

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“…In contrast, a net reduction in fungal gene copy number from 3 × 10 7 to 2 × 10 7 copies per gram of soil, wet weight was observed at the Mn Falls site between non‐manipulated and manipulated samples, corresponding with a reduction in the ratio of fungi : bacteria from 0.009 to 0.004 for Mn Falls. This finding was not unexpected, as Mn Falls was previously found to contain blooms of bacteria that produced biogenic Mn oxides as a result of exogenous carbon input in the form of untreated sewage (Carmichael et al ., ).…”

Section: Resultsmentioning

confidence: 97%

“…However, microbial manganese (II) [Mn(II)] oxidation, which produces dark brown or black cryptocrystalline material, is visible in the field and has been shown to develop in response to nutrient input in shallow epigene caves, forming a massive Mn‐oxidizing biofilm (Carmichael et al ., 2013a,b). Although input of organic acids common in sewage such as acetate, butyrate and propionate (Cummings, ) encouraged growth of a bacterially driven Mn‐oxidizing community, the input of solid litter appeared to stimulate Mn(II) oxidation primarily by fungi (Carmichael et al ., ). This suggests that simple and complex sugars (particularly in solid form) support fungally driven Mn(II) oxidation, whereas organic acids (particularly in aquatic seepage) support bacterially driven Mn(II) oxidation (Fig.…”

Section: Introductionmentioning

confidence: 99%

Nutrient input influences fungal community composition and size and can stimulate manganese (II) oxidation in caves

Carmichael

Zorn

Santelli

et al. 2015

Environ Microbiol Rep

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Little is known about the fungal role in biogeochemical cycling in oligotrophic ecosystems. This study compared fungal communities and assessed the role of exogenous carbon on microbial community structure and function in two southern Appalachian caves: an anthropogenically impacted cave and a near-pristine cave. Due to carbon input from shallow soils, the anthropogenically impacted cave had an order of magnitude greater fungal and bacterial quantitative-polymerase chain reaction (qPCR) gene copy numbers, had significantly greater community diversity, and was dominated by ascomycotal phylotypes common in early phase, labile organic matter decomposition. Fungal assemblages in the near-pristine cave samples were dominated by Basidiomycota typically found in deeper soils (and/or in late phase, recalcitrant organic matter decomposition), suggesting more oligotrophic conditions. In situ carbon and manganese (II) [Mn(II)] addition over 10 weeks resulted in growth of fungal mycelia followed by increased Mn(II) oxidation. A before/after comparison of the fungal communities indicated that this enrichment increased the quantity of fungal and bacterial cells, yet decreased overall fungal diversity. Anthropogenic carbon sources can therefore dramatically influence the diversity and quantity of fungi, impact microbial community function, and stimulate Mn(II) oxidation, resulting in a cascade of changes that can strongly influence nutrient and trace element biogeochemical cycles in karst aquifers.

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“…At the time of sampling, the CSPC Mn Falls site was thought to be heavily impacted by organic input from sewage effluent (Carmichael et al 2013). Bacterial biomass in cave pools has been shown to increase proportionally with organic carbon input (Simon and Buikema Jr. 1997), and cell concentrations in the range of 1 × 10 9 cells/mL have been reported in sewage (Fierer and Lennon 2011).…”

Section: Ferromanganese Biofilm Community Compositionmentioning

confidence: 99%

“…Lechuguilla Cave has been described as deep and oligotrophic (Northup et al 2003), whereas a parallel study of CSPC indicates that it has been severely impacted by nutrient loading from the surface (Carmichael et al 2013). Future research should attempt to elucidate the cause of these observed differences, with an initial focus on the increased role of surface impact in shallow vs. deep cave systems.…”

Section: Ferromanganese Biofilm Community Compositionmentioning

confidence: 99%

Mn(II)-oxidizing Bacteria are Abundant and Environmentally Relevant Members of Ferromanganese Deposits in Caves of the Upper Tennessee River Basin

Carmichael

Santelli

et al. 2013

Geomicrobiology Journal

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The upper Tennessee River Basin contains the highest density of our nation's caves; yet, little is known regarding speleogenesis or Fe and Mn biomineralization in these predominantly epigenic systems. Mn:Fe ratios of Mn and Fe oxide-rich biofilms, coatings, and mineral crusts that were abundant in several different caves ranged from ca. 0.1 to 1.0 as measured using ICP-OES. At sites where the Mn:Fe ratio approached 1.0 this represented an order of magnitude increase above the bulk bedrock ratio, suggesting that biomineralization processes play an important role in the formation of these cave ferromanganese deposits. Estimates of total bacterial SSU rRNA genes in ferromanganese biofilms, coatings, and crusts measured approximately 7×10 7 -9×10 9 cells/g wet weight sample. A SSU-rRNA based molecular survey of biofilm material revealed that 21% of the 34 recovered dominant (non-singleton) OTUs were closely related to known metal-oxidizing bacteria or clones isolated from oxidized metal deposits. Several different isolates that promote the oxidation of Mn(II) compounds were obtained in this study, some from high dilutions (10 ) of deposit material. In contrast to studies of caves in other regions, SSU rRNA sequences of Mn-oxidizing bacterial isolates in this study most closely matched those of Pseudomonas, Leptothrix, Flavobacterium, and Janthinobacterium. Combined data from geochemical analyses, molecular surveys, and culture-based experiments suggest that a unique consortia of Mn(II)-oxidizing bacteria are abundant and promoting biomineralization processes within the caves of the upper Tennessee River Basin.

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Sustained Anthropogenic Impact in Carter Saltpeter Cave, Carter County, Tennessee and the Potential Effects on Manganese Cycling

Abstract: Anthropogenic impact is a pervasive problem in heavily trafficked cave systems and fecal contamination is equally problematic in many cave and karst waters worldwide.

Cited by 9 publications

References 69 publications

Biogenic manganese oxides as reservoirs of organic carbon and proteins in terrestrial and marine environments

Biogenic manganese oxides as reservoirs of organic carbon and proteins in terrestrial and marine environments

Nutrient input influences fungal community composition and size and can stimulate manganese (II) oxidation in caves

Mn(II)-oxidizing Bacteria are Abundant and Environmentally Relevant Members of Ferromanganese Deposits in Caves of the Upper Tennessee River Basin

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