Sustained anthropogenic impact in Carter Saltpeter Cave, Carter County, Tennessee and the potential effects on manganese cycling

Journal of Cave and Karst Studies

Volumn 75, Issue 3, 2013, Pages 189-204

  Carmichael, Sarah K ^a   Carmichael, Mary J ^a,b   Strom, Amanda ^a   Johnson, Krissy W ^a   Roble, Leigh Anne ^a,c   Gao, Yongli ^d,e   Bräuer, Suzanna L ^a  

^a APPALACHIAN STATE UNIVERSITY   (United States)

^b WAKE FOREST UNIVERSITY   (United States)

^c University of Maryland   (United States)

^d EAST TENNESSEE STATE UNIVERSITY   (United States)

^e UNIVERSITY OF TEXAS AT SAN ANTONIO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTHROPOGENIC EFFECT; BIOFILM; CAVE SYSTEM; FECAL COLIFORM; FUNGUS; HETEROTROPHY; MANGANESE OXIDE; NUTRIENT DYNAMICS; PHYLOGENETICS;

CARTER COUNTY [TENNESSEE]; TENNESSEE; UNITED STATES;

BACTEROIDES; FUNGI; PREVOTELLA;

EID: 84880953758     PISSN: 10906924     EISSN: None     Source Type: Journal    
DOI: 10.4311/2012MB0267     Document Type: Article

References (78)

1. Ahmed, W., Goonetilleke, A., and Gardner, T., 2008a, Alternative indicators for detection and quantification of faecal pollution: Water, v. 39, p. 39-45.
2. Ahmed, W., Goonetilleke, A., Powell, D., Chauhan, K., and Gardner, T., 2009a, Comparison of molecular markers to detect fresh sewage in environmental waters: Water Research, v. 43, p. 4908-4917.
3. Ahmed, W., Goonetilleke, A., Powell, D., and Gardner, T., 2009b, Evaluation of multiple sewage-associated Bacteroides PCR markers for sewage pollution tracking: Water Research, v. 43, p. 4872-4877.
4. Ahmed, W., Powell, D., Goonetilleke, A., and Gardner, T., 2008b, Detection and source identification of faecal pollution in non-sewered catchment by means of host-specific molecular markers: Water Science and Technology, v. 58, no. 3, p. 579-586.
5. Anderson, C.R., Johnson, H.A., Caputo, N., Davis, R.E., Torpey, J.W., and Tebo, B.M., 2009, Mn(II) oxidation is catalyzed by Heme Peroxidases in "Aurantimonas manganoxydans" Strain SI85-9A1 and Erythrobacter sp. Strain SD-21: Applied and Environmental Microbiology, v. 75, p. 4130-4138.
6. Barton, H.A., and Jurado, V., 2007, What's up down there? Microbial diversity in caves: Microbe, v. 2, no. 3, p. 132-138.
7. Bernhard, A.E., and Field, K.G., 2000a, Identification of nonpoint sources of fecal polluton in coastal waters by using host-specific 16S ribosomal DNA genetic markers from fecal anaerobes: Applied and Environmental Microbiology, v. 66, p. 1587-1594.
8. Bernhard, A.E., and Field, K.G., 2000b, A PCR assay to discriminate human and ruminant feces on the basis of host differences in Bactreoides-Prevotella genes encoding 16S rRNA: Applied and Environmental Microbiology, v. 66, p. 4571-4574.
9. Blehert, D.S., Lorch, J.M., Ballmann, A.E., Cryan, P.M., and Meteyer, C.U., 2011, Bat white-nose syndrome in North America: Microbe, v. 6, p. 267-273.
10. Bräuer, S.L., Adams, C., Kranzler, K., Murphy, D., Xu, M., Zuber, P., Simon, H.M., Baptista, A.M., and Tebo, B.M., 2011, Culturable Rhodobacter and Shewanella species are abundant in estuarine turbidity maxima of the Columbia River: Environmental Microbiology, v. 13, no. 3, p. 589-603.
11. Carmichael, M.J., Carmichael, S.K., Santelli, C.M., Strom, A.C., and Bräuer, S.L., 2013, Mn(II)-oxidizing bacteria are abundant and environmentally relevant members of ferromanganese deposits in caves of the upper Tennessee River Basin: Geomicrobiology Journal. DOI: 10.1080/01490451.2013.769651
12. Chelius, M.K., Beresford, G., Horton, H., Quirk, M., Selby, G., Simpson, R.T., Horrocks, R., and Moore, J.C., 2009, Impacts of alterations of organic inputs on the bacterial community within the sediments of Wind Cave, South Dakota, USA: International Journal of Speleology, v. 38, no. 1, p. 1-10.
13. Corstjens, P., de Vrind, J.P.M., Goosen, T., and de Vrind-de Jong, E.W., 1997, Identification and molecular analysis of the Leptothrix discophora SS-1 mofA gene, a gene putatively encoding a manganese-oxidizing protein with copper domains: Geomicrobiology Journal, v. 14, p. 91-108.
14. Denver, J.M., 1989, Effects of agricultural practices and septic-system effluent on the quality of water in the unconfined aquifer in parts of eastern Sussex County, Delaware, Newark, DE, Delaware Geological Survey, University of Delaware.
15. Dorai-Raj, S., Grady, J.O., and Colleran, E., 2009, Specificity and sensitivity evaluation of novel and existing Bacteroidales and Bifidobacteria-specific PCR assays on feces and sewage samples and their application for microbial source tracking in Ireland: Water Research, v. 43, no. 19, p. 4980-4988.
16. Duckworth, O.W., and Sposito, G., 2007, Siderophore-promoted dissolution of synthetic and biogenic layer-type Mn oxides: Chemical Geology, v. 242, no. 3-4, p. 497-508.
17. Engel, A.S., Meisinger, D.B., Porter, M.L., Payn, R.A., Schmid, M., Stern, L.A., Schleifer, K.H., and Lee, N.M., 2010, Linking phylogenetic and functional diversity to nutrient spiraling in microbial mats from Lower Kane Cave (USA): The ISME Journal, v. 4, p. 98-110.
18. Felsenstein, J., 2008, PHYLIP (Phylogeny Inference Package) version 3.68, Seattle, WA, University of Washington.
19. Fischer, T.B., Heaney, P.J., Jang, J.H., Ross, D.E., Brantley, S.L., Post, J.E., and Tien, M., 2008, Continuous time-resolved X-ray diffraction of the biocatalyzed reduction of Mn oxide: American Mineralogist, v. 93, no. 11-12, p. 1929-1932.
20. Francis, C.A., and Tebo, B.M., 2002, Enzymatic manganese(II) oxidation by metabolically-dormant spores of diverse Bacillus species: Applied and Environmental Microbiology, v. 68, p. 874-880.
21. Gao, Y., Gibson, N., Burnham, T., and Evanshen, B., 2006, Water chemistry and quality changes in the Rockhouse cave system, Carter County, TN, The Sixteenth Tennessee Water Resources Symposium, 1B-3-IB-6 p.
22. Geszvain, K., McCarthy, J.K., and Tebo, B.M., 2013, Elimination of manganese (II, III) oxidation in Pseudomonas putida GB-1 by a double knockout of two putative multicopper oxidase genes: Applied and Environmental Microbiology, v. 79, no. 1, p. 357-366.
23. Gillieson, D.S., 2011, Management of Caves, in van Beynen, P., ed., Karst Management, New York, Springer, p. 141-158.
24. Goeppert, N., and Goldscheider, N., 2011, Transport and variability of fecal bacteria in carbonate conglomerate aquifers: Ground Water, v. 49, p. 77-84.
25. Goldscheider, N., Hunkeler, D., and Rossi, P., 2006, Review: Microbial biocenoses in pristine aquifers and an assessment of investigative methods: Hydrogeology Journal, v. 14, p. 926-941.
26. Green, R.T., Painter, S.L., Sun, A., and Worthington, S.R.H., 2006, Groundwater contamination in karst terranes: Water, Air, & Soil Pollution: Focus, v. 6, no. 1-2, p. 157-170.
27. Hansel, C.M., Zeiner, C.A., Santelli, C.M., and Webb, S.M., 2012, Mn (II) oxidation by an ascomycete fungus is linked to superoxide production during asexual reproduction: Proceedings of the National Academy of Sciences, v. 109, no. 31, p. 12621-12625.
28. Hayashi, H., Sakamoto, M., and Benno, Y., 2002, Phylogenetic analysis of the human gut microbiota using 16S rDNA clone libraries and strictly anaerobic culture-based methods: Microbiology and Immunology, v. 46, no. 8, p. 535-548.
29. Hayashi, H., Shibata, K., Sakamoto, M., Tomita, S., and Benno, Y., 2007, Prevotella copri sp. nov. and Prevotella stercorea sp. nov., isolated from human faeces: International Journal of Systematic and Evolutionary Microbiology, v. 57, no. 5, p. 941-946.
30. Hoagland, A.D., Hill, W.T., and Fulweiler, R.E., 1965, Genesis of the Ordovician zinc deposits in east Tennessee: Economic Geology, v. 60, no. 4, p. 693-714.
31. Horner-Devine, M.C., Leibold, M.A., Smith, V.H., and Bohannan, B.J.M., 2003, Bacterial diversity patterns along a gradient of primary productivity: Ecology Letters, v. 6, p. 613-622.
32. Ikner, L.A., Toomey, R.S., Nolan, G., Neilson, J.W., Pryor, B.M., and Maier, R.M., 2007, Culturable microbial diversity and the impact of tourism in Kartchner Caverns, Arizona: Microbial Ecology, v. 53, p. 30-42.
33. Johnson, G.C., 2002, Water Quality of Springs in the Valley and Ridge Physiographic Province in the Upper Tennessee River Basin, 1997, U.S. Geological Survey Water-Resources Investigations Report 02-4180.
34. Johnson, K., Carmichael, M., McDonald, W., Rose, N., Pitchford, J., Windelspecht, M., Karatan, E., and Bräuer, S., 2012, Increased abundance of Gallionella spp., Leptothrix spp. and total bacteria in response to enhanced Mn and Fe concentrations in a disturbed southern Appalachian high elevation wetland: Geomicrobiology Journal, v. 29, no. 2, p. 124-138.
35. Johnson, M., Zaretskaya, I., Raytselis, Y., Merezhuk, Y., McGinnis, S., and Madden, T.L., 2008, NCBI BLAST: a better web interface: Nucleic Acids Research, v. 36, p. W5-W9.
36. Johnson, T.B., McKay, L.D., Layton, A.C., Jones, S.W., Johnson, G.C., Cashdollar, J.L., Dahling, D.R., Villegas, L.F., Fout, G.S., and Williams, D.E., 2011, Viruses and bacteria in karst and fractured rock aquifers in east Tennessee, USA: Ground Water, v. 49, no. 1, p. 98-110.
37. Johnston, M.D., Muench, B.A., Banks, E.D., and Barton, H.A., 2012, Human urine in Lechuguilla Cave: the microbiological impact and potential for bioremediation: Journal of Cave and Karst Studies, v. 74, no. 3, p. 278-291.
38. Ju-Yong, J., Park, H.-D., Lee, K.-H., Hwang, J.-H., and Ka, J.-O., 2010, Quantitative analysis of human-and cow-specific 16S rRNA gene markers for assessment of fecal pollution in river waters by Real-Time PCR: Journal of Microbiology and Biotechnology, v. 20, p. 245-253.
39. Krumbein, W.E., and Altmann, H.J., 1973, A new method for the detection and enumeration of manganese oxidizing and reducing microorganisms: Helgolander Wissenschaftlichen Untersuchungen, v. 25, p. 347-356.
40. Lamendella, R., Santo Domingo, J.W., Oerther, D.B., Vogel, J.R., and Stoeckel, D.M., 2007, Assessment of fecal pollution sources in a small northern-plains watershed using PCR and phylogenetic analyses of Bacteroidetes 16S rRNA gene: FEMS Microbiology Ecology, v. 59, no. 3, p. 651-660.
41. Lamendella, R., Santo Domingo, J.W., Yannarell, A.C., Ghosh, S., Di Giovanni, G., Mackie, R.I., and Oerther, D.B., 2009, Evaluation of swine-specific PCR assays used for fecal source tracking and analysis of molecular diversity of swine-specific "Bacteroidales" populations: Applied and Environmental Microbiology, v. 75, no. 18, p. 5787-5796.
42. Learman, D.R., Wankel, S.D., Webb, S.M., Martinez, N., Madden, A.S., and Hansel, C.M., 2011, Coupled biotic-abiotic Mn(II) oxidation pathway mediates the formation and structural evolution of biogenic Mn oxides, Geochimica et Cosmochimica Acta.
43. Ley, R.E., Backheld, R., Turnbaugh, P.J., Lozupone, C.A., Knight, R.A., and Gordon, J.I., 2005, Obesity alters gut microbial ecology: Proceedings of the National Academy of Sciences, v. 102, p. 11070-11075.
44. Ley, R.E., Peterson, D.A., and Gordon, J.I., 2006, Ecological and evolutionary forces shaping microbial diversity in the human intestine: Cell, v. 124, no. 4, p. 837-848.
45. Liers, C., Arnstadt, T., Ullrich, R., and Hofrichter, M., 2011, Patterns of lignin degradation and oxidative enzyme secretion by different wood-and litter-colonizing basidiomycetes and ascomycetes grown on beech-wood: FEMS Microbiology Ecology, v. 78, no. 1, p. 91-102.
46. Ludwig, W., Strunk, O., Westram, R., Richter, L., Meier, H., Yadhukumar, Buchner, A., Lai, T., Steppi, S., Jobb, G., Forster, W., Brettske, I., Gerber, S., Ginhart, A.W., Gross, O., Grumann, S., Hermann, S., Jost, R., Konig, A., Liss, T., Lussmann, R., May, M., Nonhoff, B., Reichel, B., Strehlow, R., Stamatakis, A., Stuckmann, N., Vilbig, A., Lenke, M., Ludwig, T., Bode, A., and Schleifer, K.H., 2004, ARB: a software environment for sequence data: Nucleic Acids Research, v. 32, no. 4, p. 1363-1371.
47. Luther, G.W., 2010, The role of one-and two-electron transfer reactions in forming thermodynamically unstable intermediates as barriers in multielectron redox reactions: Aquatic Geochemistry, v. 16, no. 3, p. 395-420.
48. Macalady, J.L., Dattagupta, S., Schaperdoth, I., Jones, D.S., Druschel, G.K., and Eastman, D., 2008, Niche differentiation among sulfuroxidizing bacterial populations in cave waters: The ISME Journal, v. 2, p. 590-601.
49. Mikell, A.T., Smith, C.L., and Richardson, J.C., 1996, Evaluation of media and techniques to enumerate heterotrophic microbes from karst and sand aquifer springs: Microbial Ecology, v. 31, no. 2, p. 115-124.
50. Miller, J., and Hiskey, J., 1972, Electrokinetic behavior of fluorite as influenced by surface carbonation: Journal of Colloid and Interface Science, v. 41, no. 3, p. 567-573.
51. Minnesota Pollution Control Agency, 1999, Effects of Septic Systems on Ground Water Quality-Baxter, Minnesota, St. Paul, Ground Water Monitoring and Assessment Program, Ground Water and Toxics Monitoring Unit, Environmental Monitoring and Analysis Section, Environmental Outcomes Division, 37 p.
52. Mulec, J., Kristufek, V., and Chronakova, A., 2012, Comparative microbial sampling from eutrophic caves in Slovenia and Slovakia using RIDA(R) COUNT test kits: International Journal of Speleology, v. 41, p. 1-8.
53. Northup, D.E., 2011, Managing microbial communities in caves, in van Beynen, P., ed., Karst Management, New York, Springer, p. 225-240.
54. Northup, D.E., Barns, S.M., Yu, L.E., Spilde, M.N., Schelble, R.T., Dano, K.E., Crossey, L.J., Connolly, C.A., Boston, P.J., Natvig, D.O., and Dahm, C.N., 2003, Diverse microbial communities inhabiting ferromanganese deposits in Lechuguilla and Spider Caves: Environmental Microbiology, v. 5, no. 11, p. 1071-1086.
55. Northup, D.E., and Lavoie, K.H., 2001, Geomicrobiology of caves: A review: Geomicrobiology Journal, v. 18, no. 3, p. 199-222.
56. Porter, M.L., 2007, Subterranean biogeography: what have we learned from molecular techniques?: Journal of Cave and Karst Studies, v. 69, p. 179-186.
57. Portillo, M.C., and Gonzalez, J.M., 2010, Differential effects of distinct bacterial biofilms in a cave environment: Current Topics in Microbiology, v. 60, p. 435-438.
58. Portillo, M.C., Porca, E., Cuezva, S., Canaveras, C., Sanchez-Moral, S., and Gonzalez, J.M., 2009, Is the availability of different nutrients a critical factor for the impact of bacteria on subterraneous carbon budgets?: Naturwissenschaften, v. 96, p. 1035-1042.
59. Post, J.E., 1999, Manganese oxide minerals: crystal structures and economic and environmental significance: Proceedings of the National Academy of Sciences USA, v. 96, p. 3447-3454.
60. Potter, R.M., and Rossman, G.R., 1979, The tetravalent manganese oxides: identification, hydration, and structural relationships by infrared spectroscopy: American Mineralogist, v. 64, p. 1199-1218.
61. Pruesse, E., Quast, C., Knittel, K., Fuchs, B.M., Ludwig, W., Peplies, J., and Glockner, F.O., 2007, SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB: Nucleic Acids Research, v. 35, no. 21, p. 7188-7196.
62. Reischer, G.H., Kasper, D.C., Steinborn, R., Farnleitner, A.H., and Mach, R.L., 2007, A quantitative real-time PCR assay for the highly sensitive and specific detection of human faecal influence in spring water from a large alpine catchment area: Letters in Applied Microbiology, v. 44, p. 351-356.
63. Robertson, W., Schiff, S., and Ptacek, C., 1998, Review of phosphate mobility and persistence in 10 septic system plumes: Ground Water, v. 36, no. 6, p. 1000-1010.
64. Roslev, P., and Bukh, A.S., 2011, State of the art molecular markers for fecal pollution source tracking in water: Applied Microbiology and Biotechnology, v. 89, p. 1341-1355.
65. Rusterholtz, K.J., and Mallory, L.M., 1994, Density, activity, and diversity of bacteria indigenous to a karstic aquifer: Microbial Ecology, v. 28, no. 1, p. 79-99.
66. Santelli, C.M., Webb, S.M., Dohnalkova, A.C., and Hansel, C.M., 2011, Diversity of Mn oxides produced by Mn(II)-oxidizing fungi: Geochimica et Cosmochimica Acta, v. 75, no. 10, p. 2762-2776.
67. Schloss, P.D., and Handelsman, J., 2005, Introducing DOTUR, a computer program for defining operational taxonomic units and estimating species richness: Applied and Environmental Microbiology, v. 71, p. 1501-1506.
68. Shabarova, T., and Pernthaler, J., 2010, Karst pools in subsurface environments: collectors of microbial diversity or temporary residence between habitat types: Environmental Microbiology, v. 12, p. 1061-1074.
69. Shah, H.N., and Collins, D.M., 1990, NOTES: Prevotella, a new genus to include Bacteroides melaninogenicus and related species formerly classified in the genus Bacteroides: International Journal of Systematic Bacteriology, v. 40, no. 2, p. 205-208.
70. Simon, K.S., and Buikema, A.L., 1997, Effects of organic pollution on an Appalachian cave: Changes in macroinvertebrate populations and food supplies: American Midland Naturalist, v. 138, no. 2, p. 387-401.
71. Simpson, J.M., Santo Domingo, J.W., and Reasoner, D.J., 2004, Assessment of equine fecal contamination: the search for alternative bacterial source-tracking targets: FEMS Microbiology Ecology, v. 47, no. 1, p. 65-75.
72. Spiro, T.G., Bargar, J.R., Sposito, G., and Tebo, B.M., 2010, Bacteriogenic manganese oxides: Accounts of Chemical Research, v. 43, no. 1, p. 2-9.
73. Ueki, A., Akasaka, H., Satoh, A., Suzuki, D., and Ueki, K., 2007, Prevotella paludivivens sp. nov., a novel strictly anaerobic, Gramnegative, hemicellulose-decomposing bacterium isolated from plant residue and rice roots in irrigated rice-field soil: International Journal of Systematic and Evolutionary Microbiology, v. 57, no. 8, p. 1803-1809.
74. van Beynen, P., and Townsend, K., 2005, A disturbance index for karst environments: Environmental Management, v. 36, p. 101-116.
75. Vesper, D.J., Loop, C.M., and White, W.B., 2001, Contaminant transport in karst aquifers: Theoretical and Applied Karstology, v. 13, p. 63-73.
76. Walker, A., Sanderson, J., Churcher, C., Parkes, G., Hudspith, B., Rayment, N., Brostoff, J., Parkhill, J., Dougan, G., and Petrovska, L., 2011, High-throughput clone library analysis of the mucosa-associated microbiota reveals dysbiosis and differences between inflamed and non-inflamed regions of the intestine in inflammatory bowel disease: BMC Microbiology, v. 11, no. 1, 7 p.
77. Worthington, S.R.H., 2011, Management of carbonate aquifers, in van Beynen, P., ed., Karst Management, New York, Springer, p. 243-261.
78. Zhu, M., Ginder-Vogel, M., Parikh, S.J., Feng, X.-H., and Sparks, D.L., 2010, Cation Effects on the Layer Structure of Biogenic Mn-Oxides: Environmental Science and Technology, v. 44, no. 12, p. 4465-4471.