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Microbial Ecology

, Volume 51, Issue 1, pp 65–82 | Cite as

Microbial Diversity in Sediments of Saline Qinghai Lake, China: Linking Geochemical Controls to Microbial Ecology

  • Hailiang Dong
  • Gengxin Zhang
  • Hongchen Jiang
  • Bingsong Yu
  • Leah R. Chapman
  • Courtney R. Lucas
  • Matthew W. Fields
Article

Abstract

Saline lakes at high altitudes represent an important and extreme microbial ecosystem, yet little is known about microbial diversity in such environments. The objective of this study was to examine the change of microbial diversity from the bottom of the lake to sediments of 40 cm in depth in a core from Qinghai Lake. The lake is saline (12.5 g/L salinity) and alkaline (pH 9.4) and is located on the Qinghai–Tibetan Plateau at an altitude of 3196 m above sea level. Pore water chemistry of the core revealed low concentrations of sulfate and iron (<1 mM), but high concentrations of acetate (40–70 mM) and dissolved organic carbon (1596–5443 mg/L). Total organic carbon and total nitrogen contents in the sediments were ∼2 and <0.5%, respectively. Acridine orange direct count data indicated that cell numbers decreased from 4 × 109 cells/g at the water–sediment interface to 6× 107 cells/g wet sediment at the 40-cm depth. This change in biomass was positively correlated with acetate concentration in pore water. Phospholipid fatty acid (PLFA) community structure analyses determined decrease in the proportion of the Proteobacteria and increase in the Firmicutes with increased depth. Characterization of small subunit (SSU) rRNA genes amplified from the sediments indicated a shift in the bacterial community with depth. Whereas the α-, β-, and γ-Proteobacteria and the Cytophaga/Flavobacterium/Bacteroides (CFB) were dominant at the water–sediment interface, low G + C gram-positive bacteria (a subgroup of Firmicutes) became the predominant group in the anoxic sediments. Both PLFA and the sequence data showed similar trend. The Proteobacteria, CFB, and gram-positive bacteria are present in other saline lakes, but thepresence of Actinobacteria and Acidobacteria/Holophaga in significant proportions in the Qinghai Lake sediments appears to be unique. The archaeal diversity was much lower, and clone sequences could be grouped inthe Euryarchaeota and Crenarchaeota domains. The archaeal clones were not related to any known cultures but to sequences previously found in methane-rich sediments. Acetate-utilizing methanogens were isolated from sediment incubations, and α- and γ-proteobacterial isolates were obtained from a water sample from the lakebottom (23 m). Our data collectively showed that the observed diversity and shift in the community structure with depth was correlated with geochemical parameters (the redox state and availability of electron acceptor and donor). Heterotrophic methanogenesis is possibly adominant metabolic process in the Qinghai Lake sediments. These results reinforce the importance of geochemical controls on microbial ecology in saline and alkaline lake environments.

Keywords

Soda Lake Mono Lake Alkaline Lake Sediment Interface Archaeal Diversity 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgments

This work was supported by National Science Foundation grant EAR-0345307 and National Science Foundation of China grant 40228004 to HD. C.R. Lucas was supported by an undergraduate research grant from Miami University. We are grateful to W. Green for his help in the field sampling equipments, Dong Chen for doing DOC analysis, and John Morton for his help in cation and anion analyses. We are grateful to three anonymous reviewers for substantially improving the quality of this manuscript.

References

  1. 1.
    An, ZS 2003Scientific Drilling at Qinghai Lake on the Northwestern Tibetan Plateau: High-Resolution Paleoenvironmental Records of Eastern Asia and Their Significance for Global ChangeLake Qinghai Workshop, Institute of Earth Environment, Chinese Academy of SciencesXining, China12Google Scholar
  2. 2.
    Bidle, KA, Kastner, M, Bartlett, DH 1999A phylogenetic analysis of microbial communities associated with methane hydrate containing marine fluids and sediments in the Cascadia Margin (ODP8 site 892B)FEMS Microbiol Lett177101108PubMedCrossRefGoogle Scholar
  3. 3.
    Blanco, MM, Gibello, A, Vela, AI, Moreno, MA, Dominguez, L, Fernandez-Garayzabal, JF 2002PCR detection and PFGE DNA macrorestriction analyses of clinical isolates of Pseudomonas anguilliseptica from winter disease outbreaks in sea bream Sparus aurata Dis Aquat Org501927PubMedCrossRefGoogle Scholar
  4. 4.
    Blum, JS, Bindi, AB, Buzzelli, J, Stolz, JF, Oremland, RS 1998 Bacillus arsenicoselenatis, sp nov, and Bacillus selenitireducens, sp nov: two haloalkaliphiles from Mono Lake, California that respire oxyanions of selenium and arsenicArch Microbiol1711930CrossRefGoogle Scholar
  5. 5.
    Blum, JS, Stolz, JF, Oren, A, Oremland, RS 2001 Selenihalanaerobacter shriftii gen. nov., sp nov., a halophilic anaerobe from Dead Sea sediments that respires selenateArch Microbiol175208219PubMedCrossRefGoogle Scholar
  6. 6.
    Boga, HI, Brune, A 2003Hydrogen-dependent oxygen reduction by homoacetogenic bacteria isolated from termite gutsAppl Environ Microbiol69779786CrossRefPubMedGoogle Scholar
  7. 7.
    Bottomley, PJ 1994Light microscopic methods for studying soil microorganismsWeaver, RW eds. Methods of Soil Analysis, Part 2. Microbiological and Biochemical Properties-SSSA Book Series, No. 5Soil Science Society of American PublisherMadison, WI81105Google Scholar
  8. 8.
    Bowman, JP, McCammon, SA, Gibson, JAE, Robertson, L, Nichols, PD 2003Prokaryotic metabolic activity and community structure in Antarctic continental shelf sedimentsAppl Environ Microbiol6924482462PubMedCrossRefGoogle Scholar
  9. 9.
    Brettar, I, Christen, R, Hofle, MG 2002 Rheinheimera baltica gen. nov., sp nov., a blue-coloured bacterium isolated from the central Baltic SeaInt J Syst Evol Microbiol5218511857PubMedCrossRefGoogle Scholar
  10. 10.
    Castro, H, Ogram, A, Reddy, KR 2004Phylogenetic characterization of methanogenic assemblages in eutrophic and oligotrophic areas of the Florida EvergladesAppl Environ Microbiol7065596568CrossRefPubMedGoogle Scholar
  11. 11.
    Dabert, P, Sialve, B, Delgenes, JP, Moletta, R, Godon, JJ 2001Characterisation of the microbial 16S rDNA diversity of an aerobic phosphorus-removal ecosystem and monitoring of its transition to nitrate respirationAppl Microbiol Biotechnol55500509CrossRefPubMedGoogle Scholar
  12. 12.
    Demergasso, C, Casamayor, EO, Chong, G, Galleguillos, P, Escudero, L, Pedros-Alio, C 2004Distribution of prokaryotic genetic diversity in athalassohaline lakes of the Atacama Desert, Northern ChileFEMS Microbiol Ecol485769CrossRefGoogle Scholar
  13. 13.
    Dowling, NJE, Widdel, F, White, DC 1986Phospholipid ester-linked fatty acid biomarkers of acetate-oxidizing sulfate reducersand other sulfide forming bacteriaJ Gen Microbiol13218151825Google Scholar
  14. 14.
    Duckworth, AW, Grant, WD, Jones, BE, vanSteenbergen, R 1996Phylogenetic diversity of soda lake alkaliphilesFEMS Microbiol Ecol19181191CrossRefGoogle Scholar
  15. 15.
    Dungan, RS, Yates, SR, Frankenberger, WT,Jr 2003Transformations of selenate and selenite by Stenotrophomonas maltophilia isolated from a seleniferous agricultural drainage pond sedimentEnviron Microbiol5287295CrossRefPubMedGoogle Scholar
  16. 16.
    Edlund, A, Nichols, PD, Roffey, R, White, DC 1985Extractable and lipopolysaccharide fatty acid and hydroxy acid profiles from Desulfovibrio speciesJ Lipid Res26982988PubMedGoogle Scholar
  17. 17.
    Elshahed, MS, Najar, FZ, Roe, BA, Oren, A, Dewers, TA, Krumholz, LR 2004Survey of archaeal diversity reveals an abundance of halophilic Archaea in a low-salt, sulfide- and sulfur-rich springAppl Environ Microbiol7022302239CrossRefPubMedGoogle Scholar
  18. 18.
    Freitag, TE, Prosser, JI 2003Community structure of ammonia-oxidizing bacteria within anoxic marine sedimentsAppl Environ Microbiol6913591371CrossRefPubMedGoogle Scholar
  19. 19.
    Fries, MR, Zhou, J, Chee-Sanford, J, Tiedje, JM 1994Isolation, characterization, and distribution of denitrifying toluene degraders from a variety of habitatsAppl Environ Microbiol6028022810PubMedGoogle Scholar
  20. 20.
    Ghiorse, WC, Balkwill, DL 1983Enumeration and morphological characterization of bacteria indigenous to subsurface sedimentsDev Ind Microbiol24213224Google Scholar
  21. 21.
    Glockner, FO, Zaichikov, E, Belkova, N, Denissova, L, Pernthaler, J, Pernthaler, A, Amann, R 2000Comparative 16S rRNA analysis oflake bacterioplankton reveals globally distributed phylogenetic clusters including an abundant group of actinobacteriaAppl Environ Microbiol6650535065CrossRefPubMedGoogle Scholar
  22. 22.
    Grant, S, Sorokin, DY, Grant, WD, Jones, BE, Heaphy, S 2004A phylogenetic analysis of Wadi el Natrun soda lake cellulase enrichment cultures and identification of cellulase genes from these culturesExtremephiles8421429CrossRefGoogle Scholar
  23. 23.
    Guckert, JB, Antworth, CP, Nichols, PD, White, DC 1985Phospholipid ester-linked fatty acid profiles as reproducible assays for changes in prokaryotic community structure of estuarine sedimentsFEMS Microbiol Ecol31147158CrossRefGoogle Scholar
  24. 24.
    Guckert, JB, Hood, MA, White, DC 1986Phospholipid ester-linked fatty acid profile changes during nutrient deprivation of Vibrio cholerae: increases in the trans/cis ratio and proportions of cyclopropyl fatty acidsAppl Environ Microbiol52794801PubMedGoogle Scholar
  25. 25.
    Henderson, ACG, Holmes, JA, Zhang, J, Leng, MJ, Carvalho, LR 2003A carbon- and oxygen-isotope record of recent environmental change from Qinghai Lake, NE Tibetan PlateauChin Sci Bull4814631467CrossRefGoogle Scholar
  26. 26.
    Hinrichs, KU, Hayes, JM, Sylva, SP, Brewer, PG, DeLong, EF 1999Methane-consuming archaebacteria in marine sedimentsNature398802805PubMedCrossRefGoogle Scholar
  27. 27.
    Hirons, WD, Methe, BA, Nierzwicki-Bauer, SA, Zehr, JP 1997Bacterial diversity in Adirondack Mountain lakes as revealed by 16S rRNA gene sequencesAppl Environ Microbiol6329572960Google Scholar
  28. 28.
    Humayoun, SB, Bano, N, Hollibaugh, JT 2003Depth distribution of microbial diversity in Mono Lake, a meromictic soda lake in CaliforniaAppl Environ Microbiol6910301042CrossRefPubMedGoogle Scholar
  29. 29.
    Inagaki, F, Suzuki, M, Takai, K, Oida, H, Sakamoto, T, Aoki, K, Nealson, KH, Horikoshi, K 2003Microbial communities associated with geological horizons in coastal subseafloor sediments from the Sea of OkhotskAppl Environ Microbiol6972247235CrossRefPubMedGoogle Scholar
  30. 30.
    Jones, BE, Grant, WD, Duckworth, AW, Owenson, GG 1998Microbial diversity of soda lakesExtremephiles2191200CrossRefGoogle Scholar
  31. 31.
    Jurgens, G, Glockner, FO, Amann, R, Saano, A, Montonen, L, Likolammi, M, Munster, U 2000Identification of novel Archaea in bacterioplankton of a boreal forest lake by phylogenetic analysis and fluorescent in situ hybridizationFEMS Microbiol Ecol344556PubMedGoogle Scholar
  32. 32.
    Knittel, K, Boetius, A, Lemke, A, Eilers, H, Lochte, K, Pfannkuche, O, Linke, P 2003Activity, distribution, and diversity of sulfate reducers and other bacteria in sediments above gas hydrate (Cascadia Margin, Oregon)Geomicrobiol J2013623087CrossRefGoogle Scholar
  33. 33.
    Koizumi, Y, Kojima, H, Fukui, M 2004Dominant microbial composition and its vertical distribution in saline meromictic Lake Kaiike (Japan) as revealed by quantitative oligonucleotide probe membrane hybridizationAppl Environ Microbiol7049304940CrossRefPubMedGoogle Scholar
  34. 34.
    Koizumi, Y, Kojima, H, Oguri, K, Kitazato, H, Fukui, M 2004Vertical and temporal shifts in microbial communities in the water column and sediment of saline meromictic Lake Kaiike (Japan), as determined by a 16S rDNA-based analysis, and related to physicochemical gradientsEnviron Microbiol6622637CrossRefPubMedGoogle Scholar
  35. 35.
    Kostka, JE, Nealson, KH 1998Isolation, cultivation, and characterization of iron- and manganese-reducing bacteriaBurlage, RS eds. Techniques in Microbial EcologyOxford University PressOxford5878Google Scholar
  36. 36.
    Kuo, S 1996Phosphorus, Methods of Soil Analysis. Part 3: Chemical MethodsSoil Science Society of AmericaMadison, WI, USA894895Google Scholar
  37. 37.
    Lanoil, BD, Sassen, R, Duc, MT, Sweet, ST, Nealson, KH 2001Bacteria and Archaea physically associated with Gulf of Mexico Gas HydrateAppl Environ Microbiol6751435153CrossRefPubMedGoogle Scholar
  38. 38.
    Li, L, Kato, C, Horikoshi, K 1999Bacterial diversity in deep-sea sediments from different depthsBiodivers Conserv8659677CrossRefGoogle Scholar
  39. 39.
    Lizama, C, Monteoliva-Sanchez, M, Prado, B, Ramos-Cormenzana, A, Weckesser, J, Campos, V 2001Taxonomic study of extreme halophilic archaea isolated from the “Salar de Atacama”, ChileSyst Appl Microbiol24464474CrossRefPubMedGoogle Scholar
  40. 40.
    Ma, YH, Zhang, WZ, Xue, YF, Zhou, PJ, Ventosa, A, Grant, WD 2004Bacterial diversity of the Inner Mongolian Baer Soda Lake as revealed by 16S rRNA gene sequence analysesExtremephiles84551CrossRefGoogle Scholar
  41. 41.
    MacGregor, BJ, Moser, DP, Alm, EW, Nealson, KH, Stahl, DA 1997Crenarchaeota in Lake Michigan SedimentAppl Environ Microbiol6311781181PubMedGoogle Scholar
  42. 42.
    Marchesi, JR, Weightman, AJ, Cragg, BA, Parkes, RJ, Fry, JC 2001Methanogen and bacterial diversity and distribution indeep gas hydrate sediments from the Cascadia Margin as revealed by 16S rRNA molecular analysisFEMS Microbiol Ecol34221228PubMedCrossRefGoogle Scholar
  43. 43.
    Mills, HJ, Hodges, C, Wilson, K, MacDonald, IR, Sobecky, PA 2003Microbial diversity in sediments associated with surface-breaching gas hydrate mounds in the Gulf of MexicoFEMS Microbiol Ecol463952CrossRefGoogle Scholar
  44. 44.
    Moser, DP, Onstott, TC, Fredrickson, JK, Brockman, FJ, Balkwill, DL, Drake, GR, Pfiffner, SM, White, DC, Takai, K, Pratt, LM, Fong, J, Lollar, BS, Slater, G, Phelps, TJ, Spoelstra, N, Deflaun, M, Southam, G, Welty, AT, Baker, BJ, Hoek, J 2003Temporal shifts in the geochemistry and microbial community structure of an ultradeep mine borehole following isolationGeomicrobiol J20517548CrossRefGoogle Scholar
  45. 45.
    Nelson, K, Fisher, CR 2000Absence of cospeciation in deep-sea vestimentiferan tube worms and their bacterial endosymbiontsSymbiosis28115Google Scholar
  46. 46.
    Nold, SC, Kopczynski, ED, Ward, DM 1996Cultivation of aerobic chemoorganotrophic proteobacteria and gram-positive bacteria from a hot spring microbial matAppl Environ Microbiol6239173921PubMedGoogle Scholar
  47. 47.
    Nusslein, B, Chin, KJ, Eckert, W, Conrad, R 2001Evidence for anaerobic syntrophic acetate oxidation during methane production in the profundal sediment of subtropical Lake Kinneret (Israel)Environ Microbiol3460470CrossRefPubMedGoogle Scholar
  48. 48.
    Ollivier, B, Hatchikian, CE, Prensier, G, Guezennec, J, Garcia, JL 1991 Desulfohalobium retbaense gen. nov., sp. nov., a halophilic sulfate-reducing bacterium from sediments of a hypersaline lake in SenegalInt J Sys Bacteriol417481Google Scholar
  49. 49.
    Onstott, TC, Phelps, TJ, Kieft, T, Colwell, FS, Balkwill, DL, Fredrickson, JK, Brockman, FJ 1999. A global perspective on the microbial abundance and activity in the deep subsurface. In: Seckbach, J (Ed.) Enigmatic Microorganisms and Life in Extreme Environments. Kluwer Academic Publishers, pp 489–499Google Scholar
  50. 50.
    Orphan, VJ, House, CH, Hinrichs, KU, McKeegan, KD, DeLong, EF 2001Methane-consuming archaea revealed by directly coupled isotopic and phylogenetic analysisScience293484 487CrossRefPubMedGoogle Scholar
  51. 51.
    Phelps, CD, Kerkhof, LJ, Young, LY 1998Molecular characterization of a sulfate-reducing consortium which mineralizes benzeneFEMS Microbiol Ecol27269279CrossRefGoogle Scholar
  52. 52.
    Prowe, SG, Antranikian, G 2001 Anaerobranca gottschalkii sp nov., a novel thermoalkaliphilic bacterium that grows anaerobically at high pH and temperatureInt J Syst Evol Microbiol51457465PubMedGoogle Scholar
  53. 53.
    Reed, DW, Fujita, Y, Delwiche, ME, Blackwelder, DB, Sheridan, PP, Uchida, T, Colwell, FS 2002Microbial communities from methane hydrate-bearing deep marine sediments in a forearc basinAppl Environ Microbiol6837593770PubMedCrossRefGoogle Scholar
  54. 54.
    Rees, HC, Grant, WD, Jones, BE, Heaphy, S 2004Diversity of Kenyan soda lake alkaliphiles assessed by molecular methodsExtremephiles86371CrossRefGoogle Scholar
  55. 55.
    Ringelberg, DB, Townsend, GT, DeWeerd, KA, Sulita, JM, White, DC 1994Detection of the anaerobic dechlorinating microorganism Desulfomonile tiedjei in environmental matrices by its signature lipopolysaccharide branch-long-chain hydroxy fatty acidsFEMS Microbiol Ecol14918CrossRefGoogle Scholar
  56. 56.
    Romanenko, L, Uchino, M, Falsen, E, Zhukova, NV, Mikhailov, VV, Uchimura, T 2003 Rheinheimera pacifica sp. nov., a novel halotolerant bacterium isolated from deep sea water of the PacificInt J Syst Evol Microbiol5319731977PubMedCrossRefGoogle Scholar
  57. 57.
    Schnell, S, Schink, B 1991Anaerobic aniline degradation via reductive deamination of 4-aminobenzoyl-coa in Desulfobacterium anilini Arch Microbiol152183190CrossRefGoogle Scholar
  58. 58.
    Sciences1979Comprehensive Survey Report of Qinghai LakeScientific Publishing HouseBeijingChineseGoogle Scholar
  59. 59.
    Selenska-Pobell, S, Kampf, G, Flemming, K, Radeva, G, Satchanska, G 2001Bacterial diversity in soil samples from uranium waste piles as determined by rep-APD, RISA, and 16S rDNA retrievalAntonie van Leeuwenhoek79149161CrossRefPubMedGoogle Scholar
  60. 60.
    Sorokin, DY, Gorlenko, VM, Namsaraev, BB, Namsaraev, ZB, Lysenko, AM, Eshinimaev, BT, Khmelenina, VN, Trotsenko, YA, Kuenen, JG 2004Prokaryotic communities of the north-eastern Mongolian soda lakesHydrobiologia522235248CrossRefGoogle Scholar
  61. 61.
    Spring, S, Schulze, R, Overmann, J, Schleifer, K-H 2000Identification and characterization of ecologically significant prokaryotes in the sediment of freshwater lakes: molecular and cultivation studiesFEMS Microbiol Rev24573590PubMedCrossRefGoogle Scholar
  62. 62.
    Stackbrandt, E, Brambilla, E 2002Life in cold lakesHorneck, GBaumstark-Khan, C eds. Astrobiology: The Quest for the Conditions of LifeSpringerKoln, Germany161168Google Scholar
  63. 63.
    Stein, LY, Jones, G, Alexander, B, Elmund, K, Wright-Jones, C, Nealson, KH 2002Intriguing microbial diversity associated with metal-rich particles from a freshwater reservoirFEMS Microbiol Ecol42431440CrossRefGoogle Scholar
  64. 64.
    Stougaard, P, Jorgensen, F, Johnsen, MG, Hansen, OC 2002Microbial diversity in ikaite tufa columns: an alkaline, cold ecological niche in GreenlandEnviron Microbiol4487493CrossRefPubMedGoogle Scholar
  65. 65.
    Takai, K, Horikoshi, K 1999Genetic diversity of archaea in deep-sea hydrothermal vent environmentsGenetics15212851297PubMedGoogle Scholar
  66. 66.
    Takai, K, Moser, DP, DeFlaun, DF, Onstott, TC, Fredrickson, JK 2001Archaeal diversity in waters from deep South African gold minesAppl Environ Microbiol6757505760PubMedCrossRefGoogle Scholar
  67. 67.
    Teske, AP, Hinrichs, K-U, Edgcomb, VP, Gomez, A, Kysela, DT, Sogin, ML, Jannasch, HW 2002Microbial diversity of hydrothermal sediments in the Guaymas Basin: evidence for anaerobic methanotrophic communitiesAppl Environ Microbiol6819942007CrossRefPubMedGoogle Scholar
  68. 68.
    Thompson, JD, Higgins, DG, Gibson, TJ 1994Clustal-w— improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choiceNucleic Acid Res2246374680Google Scholar
  69. 69.
    Thomsen, TR, Finster, K, Ramsing, NB 2001Biogeochemical and molecular signatures of anaerobic methane oxidation in a marine sedimentAppl Environ Microbiol6716461656CrossRefPubMedGoogle Scholar
  70. 70.
    Tindall, BJ 2004Prokaryotic diversity in the Antarctic: the tip of the icebergMicrob Ecol47271283CrossRefPubMedGoogle Scholar
  71. 71.
    Tsitko, IV, Zaitsev, GM, Lobanok, AG, Salkinoja-Salonen, MS 1999Effect of aromatic compounds on cellular fatty acid composition of Rhodococcus opacus Appl Environ Microbiol65853855PubMedGoogle Scholar
  72. 72.
    White, DC, Davis, WM, Nickels, JS, King, JD, Bobbie, RJ 1979Determination of the sedimentary microbial biomass by extractable lipid phosphateOecologia405162CrossRefGoogle Scholar
  73. 73.
    White, DC, Pinkart, HC, Ringelberg, DB 1997Biomass measurements: biochemical approachesHurst, CJKnudsen, GRMcInerney, MJStetzenbach, LDWalter, MV eds. Manual of Environmental MicrobioASM PressWashington91101Google Scholar
  74. 74.
    White, DC, Ringelberg, DB 1995Utility of signature lipid biomarker analysis in determining in situ viable biomass, community structure, and nutritional/physiological status of the deep subsurface microbiotaAmy, PSHalderman, DL eds. The Microbiology of the Terrestrial SubsurfaceCRC PressBoca Raton119136Google Scholar
  75. 75.
    White, DC, Stair, JO, Ringelberg, DB 1996Quantitative comparisons of in situ microbial biodiversity by signature biomarker analysisJ Ind Microbiol17185196CrossRefGoogle Scholar
  76. 76.
    Xie, SC, Lai, XL, Yi, Y, Gu, YS, Liu, YY, Wang, XY, Liu, G, Liang, B 2003Molecular fossils in a Pleistocene river terrace in southern China related to paleoclimate variationOrg Geochem34789797CrossRefGoogle Scholar
  77. 77.
    Ye, Q, Roh, Y, Blair, BB, Zhang, C, Zhou, J, Fields, MW 2004Alkaline anaerobic respiration: isolation and characterization of a novel, alkaliphilic and metal-reducing bacteriumAppl Environ Microbiol7055955602PubMedCrossRefGoogle Scholar
  78. 78.
    Zengler, K, Toledo, G, Rappe, M, Elkins, J, Mathur, EJ, Short, JM, Keller, M 2002Cultivating the unculturedProc Natl Acad Sci991568115686CrossRefPubMedGoogle Scholar
  79. 79.
    Zhang, CL, Fouke, BW, Bonheyo, G, Peacock, A, White, DC, Huang, Y, Romanek, CS 2004Lipid biomarkers and carbon-isotopes of modern travertine deposits (Yellowstone National Park, USA): implications for biogeochemical dynamics in hot-spring systemsGeochim Cosmochim Acta6831573169CrossRefGoogle Scholar
  80. 80.
    Zhang, CL, Li, Y, Wall, JD, Larsen, L, Sassen, R, Huang, Y, Wang, Y, Peacock, A, White, DC, Horita, J, Cole, DR 2002Lipid and carbon isotopic evidence of methane-oxidizing and sulfate-reducing bacteria in association with gas hydrates from the Gulf of MexicoGeology30239242CrossRefGoogle Scholar
  81. 81.
    Zhang, CLL, Li, YL, Ye, Q, Fong, J, Peacock, AD, Blunt, E, Fang, JS, Lovley, DR, White, DC 2003Carbon isotope signatures of fatty acids in Geobacter metallireducens and Shewanella algae Chem Geol1951728CrossRefGoogle Scholar
  82. 82.
    Zinder, SH 1998MethanogensBurlage, RS eds. Techniques in Microbial EcologyOxford University PressOxford113136Google Scholar

Copyright information

© Springer Science+Business Media, Inc. 2006

Authors and Affiliations

  • Hailiang Dong
    • 1
  • Gengxin Zhang
    • 1
  • Hongchen Jiang
    • 1
  • Bingsong Yu
    • 2
  • Leah R. Chapman
    • 3
  • Courtney R. Lucas
    • 3
  • Matthew W. Fields
    • 3
  1. 1.Department of GeologyMiami UniversityOxfordUSA
  2. 2.School of Earth SciencesChina University of GeosciencesBeijingPR China
  3. 3.Department of MicrobiologyMiami UniversityOxfordUSA

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