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Original Articles

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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Pages 779-800 | Received 01 Jul 2012, Accepted 01 Jan 2013, Published online: 17 Jul 2013

References

  • Allouc , J and Harmelin , J G . 2001 . Mn-Fe deposits in shallow cryptic marine environment: examples in northwestern Mediterranean submarine caves . B Soc Geol Fr , 172 : 765 – 778 .
  • Amann , R I , Ludwig , W and Schleifer , K-H . 1995 . Phylogenetic identification and in situ detection of individual microbial cells without cultivation . Microbiol Rev , 59 : 143 – 169 .
  • Angert , E R , Northup , D E , Reysenbach , A-L , Peek , A S , Goebel , B M and Pace , N R . 1998 . Molecular phylogenetic analysis of a bacterial community in Sulphur River, Parker Cave, Kentucky . Am Mineral , 83 : 1583 – 1592 .
  • Archibald , F S and Fridovich , I . 1981 . Manganese and defenses against oxygen toxicity in Lactobacillus plantarum . J Bacteriol , 145 : 442 – 451 .
  • Barton , H A and Jurado , V . 2007 . What's up down there? Microbial diversity in caves . Microbe , 2 : 132 – 138 .
  • Barton , H A and Luiszer , F . 2005 . Microbial metabolic structure in a sulfidic cave hot spring: potential mechanisms of biospeleogenesis . J Cave Karst Stud , 67 : 28 – 38 .
  • Barton , H A and Northup , D E . 2007 . Geomicrobiology in cave environments: past, current and future perspectives . J Cave Karst Stud , 69 : 163 – 178 .
  • Barton , H A , Taylor , M R and Pace , N R . 2004 . Molecular phylogenetic analysis of a bacterial community in an oligotrophic cave environment . Geomicrobiol J , 21 : 11 – 20 .
  • Barton , H A , Taylor , N M , Kreate , M P , Springer , A C , Oehrle , S A and Bertog , J L . 2007 . The impact of host rock geochemistry on bacterial community structure in oligotrophic cave environments . Int J Speleol , 36 : 93 – 104 .
  • Barton , H A , Taylor , N M , Lubbers , B R and Pemberton , A C . 2006 . DNA extraction from low-biomass carbonate rock: An imporved method with reduced contamination and the low-biomass contaminant database . J Microbiol Meth , 66 : 21 – 31 .
  • Borodina , E , Kelly , D P , Rainey , F A , Ward-Rainey , N L and Wood , A P . 2000 . Dimethylsulfone as a growth substrate for novel methylotrophic species of Hyphomicrobium and Arthrobacter . Arch Microbiol , 173 : 425 – 437 .
  • Borodina , E , Kelly , D P , Schumann , P , Rainey , F A , Ward-Rainey , N L and Wood , A P . 2002 . Enzymes of dimethylsulfone metabolism and the phylogenetic characterization of the facultative methylotrophs Arthrobacter sulfonivorans sp. nov., Arthrobacter methylotrophus sp. nov., and Hyphomicrobium sulfonivorans sp. nov . Arch Microbiol , 177 : 173 – 183 .
  • Boston , P J , Hose , L D , Northup , D E and Spilde , M N . 2006 . “ The microbial communities of sulfur caves: a newly appreciated geologically driven system on Earth and potential model for Mars ” . In Perspectives on Karst Geomorphology, Hydrology, and Geochemistry , Edited by: Harmon , R S and Wicks , C M . 331 – 344 . Boulder , Colorado : Geological Society of America .
  • Cadillo-Quiroz , H , Braüer , S , Yashiro , E , Sun , C , Yavitt , J and Zinder , S . 2006 . Vertical profiles of methanogenesis and mathanogens in two contrasting acidic peatlands in central New York State, USA . Environ Microbiol , 8 : 1428 – 1440 .
  • Campbell , J W , Watson , A , Watson , C , Ball , H and Pirkle , R . 2011 . Escherichia coli, other coliform, and environmental chemoheterotrophic bacteria in isolated water pools from six caves in northern Alabama and northwestern Georgia . J Cave Karst Stud , 73 : 75 – 82 .
  • Cañaveras , J C , Cuezva , S , Sanchez-Moral , S , Lario , J , Laiz , L , Gonzalez , J M and Saiz-Jimenez , C . 2006 . On the origin of fiber calcite crystals in moonmilk deposits . Naturwissenschaften , 93 : 27 – 32 .
  • Carmichael , S , Carmichael , M , Strom , A , Johnson , K , Roble , L , Gao , Y and Bräuer , S . 2013. Sustained anthropogenic impact in Carter Saltpeter Cave, Carter County, Tennessee and the potential effects on Mn cycling . J Cave Karst Stud [accepted]. ,
  • Chelius , M K and Moore , J C . 2004 . Molecular phylogenetic analysis of Archaea and Bacteria in Wind Cave, South Dakota . Geomicrobiol J , 21 : 123 – 134 .
  • Christman , M C and Culver , D C . 2001 . The relationship between cave biodiversity and available habitat . J Biogeogr , 28 : 367 – 380 .
  • Cunningham , K I , Northup , D E , Pollastro , R M , Wright , W G and Larock , E J . 1995 . Bacteria, fungi and biokarst in Lechuguilla Cave, Carlsbad Caverns National Park, New Mexico . Environ Geol , 25 : 2 – 8 .
  • Daly , M J , Gaidamakova , E , Matrosova , V , Vasilenko , A , Zhai , M , Venkateswaran , A , Hess , M , Omeichenko , M V , Kostandarithes , H , Makarova , K , Wackett , L , Fredrickson , J K and Ghosal , D . 2004 . Accumulation of Mn(II) in Deinococcus radiodurans facilitates gamma-radiation resistance . Science , 306 : 1025 – 1028 .
  • de los Ríos , A , Bustillo , M , Ascaso , C and Carvalho , M R . 2011 . Bioconstructions in ocherous speleothems from lave tubes on Terceira Island (Azores) . Sediment Geol , 236 : 117 – 128 .
  • DeLong , EF. 1992 . Archaea in coastal marine environments . Proc Natl Acad Sci USA , 89 : 5685 – 5689 .
  • Dixon , J B and Skinner , H CW . 1992 . “ Manganese minerals in surface environments ” . In Biomineralization Processes of Iron and Manganese , Edited by: Skinner , H CW and Fitzpatrick , R W . 31 – 59 . Cremlingen , , Germany : Catena Verlag .
  • Edwards , K J , Bach , W and McCollum , T M . 2004 . Neutrophilic iron-oxidizing bacteria in the ocean: their habitats, diversity, and roles in mineral deposition, rock alteration, and biomass production in the deep sea . Geomicrobiol J , 21 : 393 – 404 .
  • Einen , J , Thorseth , I H and Øvreås , L . 2008 . Enumeration of Archaea and Bacteria in seafloor basalt using real-time quantitative PCR and fluorsecence microscopy . FEMS Microbiol Lett , 282 : 182 – 187 .
  • Emerson , D and Ghiorse , W C . 1992 . Isolation, cultural maintenance, and taxonomy of a sheath-forming strain of Leptothrix discophora and characterization of manganese-oxidizing activity associated with the sheath . Appl Environ Microbiol , 58 : 4001 – 4010 .
  • Emerson , D and Moyer , C L . 2002 . Neutrophilic Fe-oxidizing bacteria are abundant at the Loihi Seamount hydrothermal vents and play a major role in Fe oxide deposition . Appl Environ Microbiol , 68 : 3085 – 3093 .
  • 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) . ISME J , 4 : 98 – 110 .
  • Engel , A S , Porter , M L , Kinkle , B K and Kane , T C . 2001 . Ecological assessment and geological significance of microbial communities from Cesspool Cave, Virginia . Geomicrobiol J , 18 : 259 – 274 .
  • Engel , A S , Porter , M L , Stern , L A , Quinlan , S and Bennett , P C . 2004 . Bacterial diversity and ecosystem function of filamentous microbial mats from aphotic (cave) sulfidic springs dominated by chemolithoautotrophic “Epsilonproteobacteria . FEMS Microbiol Ecol , 51 : 31 – 53 .
  • Engel , A S , Stern , L A and Bennett , P C . 2004 . Microbial contributions to cave formation: New insights into sulfuric acid speleogenesis . Geology , 32 : 369 – 372 .
  • Felsenstein , J. 2004 . “ PHYLIP (Phylogeny Inference Package) version 3.68 ” . In Distributed by the author Department of Genome Sciences , University of Washington . Seattle
  • Fendorf , S E , Fendorf , M , Sparks , D L and Gronsky , R . 1992 . Inhibitory mechanisms of Cr(III) oxidation by δ-MnO2 . J Colloid Interface Sci , 153 : 37 – 54 .
  • Fierer , N and Lennon , J T . 2011 . The generation and maintenance of diversity in microbial communities . Am J Bot , 98 : 439 – 448 .
  • Fleming , E J , Langdon , A E , Martinez-Garcia , M , Stepanauskas , R , Poulton , N J , Masland , E DP and Emerson , D . 2011 . What's new is old: resolving the identity of Leptothrix ochracea using single cell genomics, pyrosequencing and FISH . PLoS ONE , 6 : e17769
  • Florea , L J , Noe-Stinson , C L , Brewer , J , Fowler , R , Kearns , J B and Greco , A M . 2011 . Iron oxide and calcite associated with Leptothrix sp. biofilms within an estavelle in the upper Floridan aquifer . Int J Speleol , 40 : 205 – 219 .
  • Fogel , G B , Collins , C R , Li , J and Brunk , C F . 1999 . Prokaryotic genome size and SSU rDNA copy number: estimation of microbial relative abundance form a mixed population . Microb Ecol , 38 : 93 – 113 .
  • Ford , T and Mitchell , R . 1990 . The ecology of microbial corrosion . Advances in Microbial Ecology , 11 : 231 – 262 .
  • Francis , C A and Tebo , B M . 2002 . Enzymatic manganese(II) oxidation by metabolically-dormant spores of diverse Bacillus species . Appl Environ Microbiol , 68 : 874 – 880 .
  • Frierdich , A J , Hasenmueller , E A and Catalano , J G . 2011 . Composition and structure of nanocrystalline Fe and Mn oxide cave deposits: Implications for trace element mobility in karst systems . Chem Geol , 284 : 82 – 96 .
  • Gadd , GM. 2007 . Geomycology: biogeochemical transformations of rocks, minerals, metals and radionuclides by fungi, bioweathering and bioremediation . Mycol Res , 111 : 3 – 49 .
  • Gao , Y , Benfield , R , Jones , S , Burnham , T and Gibson , N . 2006 . Groundwater tracing in the Rockhouse Cave System, Carter County, Tennessee. In: Proceedings of the Sixteenth Tennessee Water Resources Symposium. Burns, TN , 3B – 20 . Montgomery Bell State Park .
  • Gao , Y , Gibson , N , Burnham , T and Evanshen , B . 2006 . Water chemistry and quality changes in the Rockhouse Cave System, Carter County, Tennessee. In: Proceedings of the Sixteenth Tennessee Water Resources Symposium. Burns, TN , 1B – 3 . Montgomery Bell State Park .
  • Gázquez , F , Calaforra , J-M , Rull , F , Forti , P and García-Casco , A . 2012 . Organic matter of fossil origin in the amberine speleothems from El Soplao Cave (Cantabria, Northern Spain) . Int J Speleol , 41 : 113 – 123 .
  • Geszvain , K and Tebo , B M . 2010 . Identification of a two-component regulatory pathway essential for Mn(II) oxidation in Pseudomonas putida GB-1 . Appl Environ Microbiol , 76 : 1224 – 1231 .
  • Ghosal , D , Omelchenko , M V , Gaidamakova , E K , Matrosova , V Y , Vasilenko , A , Venkateswaran , A , Zhai , M , Kostandarithes , H M , Brim , H , Makarova , K S , Wackett , L P , Fredrickson , J K and Daly , M J . 2005 . How radiation kills cells: survival of Deinococcus radiodurans and Shewanella oneidensis under oxidative stress . FEMS Microbiol Rev , 29 : 361 – 375 .
  • Goldscheider , N , Hunkeler , D and Rossi , P . 2006 . Review: microbial biocenoses in pristine aquifers and an assessment of investigative methods . Hydrogeol J , 14 : 926 – 941 .
  • Gonzalez , J M , Portillo , M C and Saiz-Jimenez , C . 2006 . Metabolically active Crenarchaeota in Altamira Cave . Naturwissenschaften , 93 : 42 – 45 .
  • Good , IJ. 1953 . The population frequencies of species and the estimation of population parameters . Biometrika , 40 : 237 – 264 .
  • Gradziński , M , Banaś , M and Uchman , A . 1995 . Biogenic origin of manganese flowstones from Jaskinia Czarna Cave, Tatra Mts., Western Carpathians . Annales Societatis Geologorum Poloniae , 65 : 19 – 27 .
  • Grünke , S , Felden , J , Lichtschlag , A , Girnth , A-C , De Beer , D , Wenzhöfer , F and Boetius , A . 2011 . Niche differentiation among mat-forming, sulfide-oxidizing bacteria at cold seeps of the Nile Deep Sea Fan (Eastern Mediterranean Sea) . Geobiology , 9 : 330 – 348 .
  • Hara , S , Hashidoko , Y H , Desyatkin , R V , Hatano , R and Tahara , S . 2009 . High rate of N2 fixation by East Siberian Cryophilic soil bacteria as determined by measuring acetylene reduction in Nitrogen-poor medium solidified with Gellan Gum . Appl Environ Microbiol , 75 : 2811 – 2819 .
  • Hill , C and Forti , P . 1997 . “ Oxides and hydroxides ” . In Cave Minerals of the World , Edited by: Hill , C and Forti , P . 123 – 136 . Huntsville , , Alabama : National Speleological Society .
  • Hill , CA. 1982 . Origin of black deposits in caves . Natl Speleol Soc Bull , 44 : 15 – 19 .
  • Horner-Devine , M C , Silver , J M , Leibold , M A , Bohannan , B JM , Colwell , R K , Fuhrman , J A , Green , J L , Kuske , C R , Martiny , J BH , Muyzer , G , Øvreås , L , Reysenbach , A-L and Smith , V H . 2007 . A comparison of taxon co-occurence patterns for macro- and microorganisms . Ecology , 88 : 1345 – 1353 .
  • Hou , Y , Zhang , H , Miranda , L and Lin , S . 2010 . Serious overestimation in quantitative PCR by circular (supercoiled) plasmid standard: microalgal pcna as the model gene . PLoS ONE , 5 : e9545
  • Hunter , A J , Northup , D E , Dahm , C N and Boston , P J . 2004 . Persistent coliform contamination in Lechuguilla cave pools . J Cave Karst Stud , 66 : 102 – 110 .
  • 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 . Microb Ecol , 53 : 30 – 42 .
  • Johnson , K , Carmichael , M J , McDonald , W , Rose , N , Windelspecht , M , Pitchford , J , Karatan , E and Brauer , 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 . Geomicrobiol J , 29 : 124 – 138 .
  • Johnson , M , Zaretskaya , I , Raytselis , Y , Merezhuk , Y , McGinnis , S and Madden , T L . 2008 . NCBI BLAST: a better web interface . Nucleic Acids Res , 36 : W5 – W9 .
  • Jones , B. 2001 . Microbial activity in caves—A geological perspective . Geomicrobiol J , 18 : 345 – 357 .
  • Kay , J , Conklin , M , Fuller , C and O’Day , P . 2001 . Processes of nickel and cobalt uptake by a manganese oxide forming sediment in Pinal Creek, Globe Mining District, Arizona . Environ Sci Technol , 35 : 4719 – 4625 .
  • Klappenbach , J A , Dunbar , J M and Schmidt , T M . 2000 . rRNA operon copy number reflects ecological strategies of bacteria . Appl Environ Microbiol , 66 : 1328 – 1333 .
  • Klappenbach , J A , Saxman , P R , Cole , J R and Schmidt , T M . 2001 . rrndb: the Ribosomal RNA Operon Copy Number Database . Nucleic Acids Res , 29 : 181 – 184 .
  • Krumbein , W E and Altmann , H J . 1973 . A new method for the detection and enumeration of manganese oxidizing and reducing microorganisms . Helgölander Wissenschaftlichen Untersuchungen , 25 : 347 – 356 .
  • Krumbein , W E and Jens , K . 1981 . Biogenic rock varnishes of the Negev Desert (Israel) an ecological study of iron and manganese transformation by cyanobacteria and fungi . Oecologia , 50 : 25 – 38 .
  • Laiz , L , Groth , I , Schumann , P , Zezza , F , Felske , A , Hermosin , B and Saiz-Jimenez , C . 2000 . Microbiology of the stalactites from Grotta dei Cervi, Porto Badisco, Italy . Inter J Microbiol , 3 : 25 – 30 .
  • Lane , DJ. 1991 . “ 16S and 23S rRNA sequencing ” . In Nucleic Acid Techniques in Bacterial Systematics , Edited by: Stackebrandt , E and Goodfellow , M . 115 – 148 . New York : John Wiley .
  • Learman , D R , Voelker , B M , Vazquez-Rodriguez , A I and Hansel , C M . 2011 . Formation of manganese oxides by bacterially generated superoxide . Nat Geosci , 4 : 95 – 98 .
  • 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 . Geochim Cosmochim Acta , 75 : 6048 – 6063 .
  • Legatzki , A , Ortiz , M , Neilson , J W , Dominguez , S , Andersen , G L , Toomey , R S , Pryor , B M , Pierson , L S III and Maier , R M . 2011 . Bacterial and archaeal community structure of two adjacent calcite speleothems in Kartchner Caverns, Arizona, USA . Geomicrobiol J , 28 : 99 – 117 .
  • Link , D D , Walter , P J and Kingston , H M . 1998 . Development and validation of the new EPA microwave-assiste leach method 3051A . Environ Sci Technol , 32 : 3628 – 3632 .
  • Ludwig , W , Strunk , O , Westram , R , Richter , L , Yadhukumar , H M , Buchner , A , Lai , T , Steppi , S , Jobb , G , Förster , W , Brettske , I , Gerber , S , Ginhart , A W , Gross , O , Grumann , S , Hermann , S , Jost , R , König , A , Liss , T , Lümann , 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 . Nucl Acids Res , 32 : 1363 – 1371 .
  • Lueders , T and Friedrich , M . 2000 . Archaeal population dynamics during sequential reduction processes in rice field soil . Appl Environ Microbiol , 66 : 2732 – 2742 .
  • Macalady , J L , Dattagupta , S , Schaperdoth , I , Jones , D S , Druschel , G K and Eastman , D . 2008 . Niche differentiation among sulfur-oxidizing bacterial populations in cave waters . ISME J , 2 : 590 – 601 .
  • Macalady , J L , Jones , D S and Lyon , E H . 2007 . Extremely acidic, pendulous cave wall biofilms from the Frasassi cave system, Italy . Environ Microbiol , 9 : 1402 – 1414 .
  • Macalady , J L , Lyon , E H , Koffman , B , Albertson , L K , Meyer , K , Galdenzi , S and Mariani , S . 2006 . Dominant microbial Populations in limestone-corroding stream biofilms, Frasassi cave system, Italy . Appl Environ Microbiol , 72 : 5596 – 5609 .
  • Manceau , A N , Tamura , M A , MacDowell , M A , Celestre , R S , Soblett , R E , Sposito , G and Padmore , H A . 2002 . Deciphering Ni sequestration in soil ferromanganese modules by combining X-ray fluorescence, absorption, and diffraction at micrometer scales of resolution . Am Mineral , 87 : 1494 – 1499 .
  • Melim , L A , Shinglman , K M , Boston , P J , Northup , D E , Spilde , M N and Queen , J M . 2001 . Evidence for microbial involvement in pool finger precipitation, Hidden Cave, New Mexico . Geomicrobiol J , 18 : 311 – 329 .
  • Mohandas , S. 1988 . Nitrogen fixation in tomato (Lycopersicon esculentum Mill ‘Pusa Ruby’) . Plant Soil , 107 : 219 – 225 .
  • Montañez , IP. 1994 . Late diagenetic dolomitization of the Lower Ordovician, Upper Knox Carbonates: a record of the hydrodynamic evolution of the southern Appalachian Basin . AAPG Bull , 78 : 1210 – 1239 .
  • Moore , GW. 1981 . Manganese deposition in limestone caves. In: Beck BF, ed. Proceedings of the International Congress of Speleology 2 . : 642 – 645 .
  • Nadkarni , M A , Martin , F E , Jacques , N A and Hunter , N . 2002 . Determination of bacterial load by real-time PCR using a broad-range (universal) probe and primers set . Microbology , 148 : 257 – 266 .
  • Nealson , KH. 1978 . “ The isolation and characterization of marine bacteria which catalyze manganese oxidation ” . In Environmental Biogeochemistry and Geomicrobiology , Edited by: Krumbein , W E . Vol. 3 , 847 – 858 . Ann Arbor , MI : Ann Arbor Science Publishers, Inc . Methods, Metals and Assessment
  • Nealson , K H , Tebo , B M and Rosson , R A . 1988 . Occurrence and mechanisms of microbial oxidation of manganese . Adv Appl Microbiol , 33 : 279 – 318 .
  • Nelson , Y M , Lion , L W , Shuler , M L and Ghiorse , W C . 1999 . Lead binding to metal oxide and organic phases of natural aquatic biofilms . Limnol Oceanogr , 4 : 1715 – 1729 .
  • Nitahara , S , Kato , S , Urabe , T , Usui , A and Yamagishi , A . 2011 . Molecular characterization of the microbial community in hydrogenetic ferromanganese crusts of the Takuyo-Daigo Seamount, northwest Pacific . FEMS Microbiol Lett , 321 : 121 – 129 .
  • 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 . Environ Microbiol , 5 : 1071 – 1086 .
  • Northup , D E , Dahm , C N , Melim , L A , Spilde , M N , Crossey , L J , Lavoie , K H , Mallory , L M , Boston , P J , Cunningham , K I and Barns , S M . 2000 . Evidence for geomicrobiological interactions in Guadalupe Caves . J Cave Karst Stud , 62 : 80 – 90 .
  • Northup , D E and Lavoie , K H . 2001 . Geomicrobiology of caves: a review . Geomicrobiol J , 18 : 199 – 222 .
  • Northup , D E , Reysenbach , A-L and Pace , N R . 1997 . “ Microorganisms and speleothems ” . In Cave Minerals of the World. Huntsville , Edited by: Hill , C and Forti , P . 261 – 266 . Alabama : National Speleological Society .
  • Northup , D E , Snider , J R , Spilde , M N , Porter , M L , van de Kamp , J L , Boston , P J , Nyberg , A M and Bargar , J R . 2010 . Diversity of rock varnish bacterial communities from Black Canyon, New Mexico . J Geophys Res , 115 ( G2 )
  • Oder , CRL. 1934 . Preliminary subdivision of the knox dolomite in East Tennessee . J Geol , 42 : 469 – 497 .
  • Onac , B P and Forti , P . 2011 . State of the art and challenges in cave mineral studies . Studia UBB Geologia , 56 : 29 – 38 .
  • Onac , B P , Pedersen , R B and Tysseland , M . 1997 . Presence of rare-earth elements in black ferromanganese coatings from Vântului Cave (Romania) . J Cave Karst Stud , 59 : 128 – 131 .
  • Peck , SB. 1986 . Bacterial deposition of iron and manganese oxides in North American caves . Natl Speleol Soc Bull , 48 : 26 – 30 .
  • Portillo , M C and Gonzalez , J M . 2009 . Sulfate-reducing bacteria are common members of bacterial communities in Altamira Cave (Spain) . Sci Total Environ , 407 : 1114 – 1122 .
  • Portillo , M C , Gonzalez , J M and Saiz-Jimenez , C . 2008 . Metabolically active microbial communities of yellow and grey colonizations on the walls of Altamira Cave, Spain . J Appl Microbiol , 104 : 681 – 691 .
  • Post , JE. 1999 . Manganese oxide minerals: crystal structures and economic and environmental significance . Proc Natl Acad Sci USA , 96 : 3447 – 3454 .
  • Pruesse , E , Quast , C , Knittel , K , Fuchs , B M , Ludwig , W , Peplies , J and Glöckner , F . 2007 . SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB . Nucl Acids Res , 35 : 7188 – 7196 .
  • Rossi , C , Lozano , R P , Isanta , N and Hellstrom , J . 2010 . Manganese stromatolites in caves: El Soplao (Cantabria, Spain) . Geology , 38 : 1119 – 1122 .
  • Rossmassler , K , Engel , A S , Twing , K I , Hanson , T E and Campbell , B J . 2012 . Drivers of Episilonproteobacterial community composition in sulfidic caves and springs . FEMS Microbiol Ecol , 79 : 421 – 432 .
  • Santelli , C , Pfister , D , Lazarus , D , Sun , L , Burgos , W and Hansel , C . 2010 . Promotion of Mn(II) Oxidation and Remediation of Coal Mine Drainage in Passive Treatment Systems by Diverse Fungal and Bacterial Communities . Appl Environ Microbiol , 76 : 4871 – 4875 .
  • Santelli , C , Webb , S M , Dohnalkova , A and Hansel , C . 2011 . Diversity of Mn oxides produced by Mn(II)-oxidizing fungi . Geochim Cosmochim Acta , 75 : 2762 – 2776 .
  • Schloss , P D and Handelsman , J . 2005 . Introducing DOTUR, a computer program for defining operational taxonomic units and estimating species richness . Appl Environ Microbiol , 71 : 1501 – 1506 .
  • Schweisfurth , R , Eleftheriadis , D , Gundlach , H , Jacobs , M and Jung , W . 1978 . “ Microbiology of the precipitation of manganese ” . In Environmental Biogeochemistry and Geomicrobiology Volume 3: Methods, Metals, and Assessment , Edited by: Krumbein , W . 923 – 928 . Ann Arbor , MI : Ann Arbor Science Publishers Inc .
  • Shabarova , T and Pernthaler , J . 2010 . Karst pools in subsurface environments: collectors of microbial diversity or temporary residence between habitat types . Environ Microbiol , 12 : 1061 – 1074 .
  • Shapiro , J and Pringle , A . 2010 . Anthropogenic influences on the diversity of fungi isolated from caves in Kentucky and Tennessee . Am Midl Nat , 163 : 76 – 86 .
  • Simon , K S , Benfield , E F and Macko , S A . 2003 . Food web structure and the role of epilithic biofilms in cave streams . Ecology , 84 : 2395 – 2406 .
  • Simon , K S and Buikema , A L Jr. 1997 . Effects of organic pollution on an Appalachian cave: Changes in macroinvertebrate populations and food supplies . Am Midl Nat , 138 : 387 – 401 .
  • Spilde , M N , Northup , D E and Boston , P J . 2006 . Ferromanganese deposits in the caves of the Guadalupe Mountains . : 161 – 166 . In: Land L, Lueth VW, Raatz W, Boston PJ, Love DW, eds. The New Mexico Geological Society Guidebook, 57th Field Conference, Caves and Karst of Southeast New Mexico
  • Spilde , M N , Northup , D E , Boston , P J , Schelble , R T , Dano , K E , Crossey , L J and Dahm , C N . 2005 . Geomicrobiology of cave ferromanganese deposits: a field and laboratory investigation . Geomicrobiol J , 22 : 99 – 116 .
  • Spring , S. 2006 . “ The genera Leptothrix and Sphaerotilus ” . In The Prokaryotes Volume 5: Proteobacteria: The Alpha and Beta Subclasses , Edited by: Dworkin , M , Falkow , S , Rosenberg , E , Schleifer , K-H and Stackebrandt , E . p758 – 777 . New York : Springer .
  • Stein , L Y , La Duc , M T , Grundi , T J and Nealson , K H . 2001 . Bacterial and archaeal populations associated with freshwater ferromanganous micronodules and sediments . Environ Microbiol , 3 : 10 – 18 .
  • Sunda , W G and Kieber , D J . 1994 . Oxidation of humic substances by manganese oxides yields low-molecular-weight organic substrates . Nature , 367 : 62 – 64 .
  • SW-846 EPA Method 3051A . 2007 . “ Microwave assisted acid digestion of sediments, sludges, soils, and oils ” . In Test Methods for Evaluating Solid Waste, 3rd Edition, Update IIIB , Washington , DC : US Environmental Protection Agency .
  • Taboroši , D. 2006 . “ Biologically influenced carbonate speleothems ” . In Perspectives on karst geomorphology, hydrology, and geochemistry , Edited by: Harmon , R S and Wicks , C . 307 – 317 . Geological Society of America .
  • Tebo , B M , Clement , B G and Dick , G J . 2007 . “ Biotransformations of Manganese ” . In Manual of Environmental Microbiology , Edited by: Hurst , C J , Crawford , R L , Garland , J L , Lipson , D A , Mills , A L and Stetzenbach , L D . 1223 – 1238 . Washington , DC : ASM Press .
  • Tebo , B M , Johnson , H A , McCarthy , J K and Templeton , A S . 2005 . Geomicrobiology of manganese(II) oxidation . Trends Microbiol , 13 : 421 – 428 .
  • Toner , B , Manceau , A , Webb , S M and Sposito , G . 2006 . Zinc sorption to biogenic hexagonal-birnessite particles within a hydrated bacterial biofilm . Geochim Cosmochim Acta , 70 : 27 – 43 .
  • Torsvik , V , Øvreås , L and Thingstad , T F . 2002 . Prokaryotic diversity- magnitude, dynamics, and controlling factors . Science , 296 : 1064 – 1066 .
  • Turekian , K K and Wedepohl , K H . 1961 . Distribution of the elements in some major units of the Earth's crust . Geol Soc Am Bull , 72 : 175 – 192 .
  • van Veen , W L , Mulder , E G and Deinema , M H . 1978 . The Sphaerotilus-Leptothrix Group of Bacteria . Microbiol Rev , 42 : 329 – 356 .
  • Villalobos , M , Bargar , J and Sposito , G . 2005 . Mechanisms of Pb(II) sorption on a biogenic manganese oxide . Environ Sci Technol , 39 : 569 – 576 .
  • Warren , L A and Kauffman , M E . 2003 . Microbial geoengineers . Science , 299 : 1027 – 1029 .
  • Webb , S M , Tebo , B M and Bargat , J R . 2005 . Structural characterization of biogenic Mn oxides produced in seawater by the marine Bacillus sp. strain SG-1 . Am Mineral , 90 : 1342 – 1357 .
  • Wedepohl , KH. 1995 . The composition of the continental crust . Geochim Cosmochim Acta , 59 : 1217 – 1232 .
  • White , W B , Culver , D C , Herman , J S , Kane , T C and Mylroie , J E . 1995 . Karst lands . Am Sci , 83 : 450 – 459 .
  • White , W B , Vito , C and Scheetz , B E . 2009 . The mineralogy and trace element chemistry of black Manganese oxide deposits from caves . J Cave Karst Stud , 71 : 136 – 143 .
  • Whitman , W B , Coleman , D C and Wiebe , W J . 1998 . Prokaryotes: the unseen majority . Proc Natl Acad Sci USA , 95 : 6578 – 6583 .