Microbial diversity in deep-sea sediment from the cobalt-rich crust deposit region in the Pacific Ocean
Li Liao
College of Life Sciences, Zhejiang University, Hangzhou, China
Search for more papers by this authorXue-Wei Xu
Laboratory of Marine Ecosystem and Biogeochemistry, State Oceanic Administration, Hangzhou, China
The Second Institute of Oceanography, State Oceanic Administration, Hangzhou, China
Search for more papers by this authorXia-Wei Jiang
College of Life Sciences, Zhejiang University, Hangzhou, China
Search for more papers by this authorChun-Sheng Wang
Laboratory of Marine Ecosystem and Biogeochemistry, State Oceanic Administration, Hangzhou, China
The Second Institute of Oceanography, State Oceanic Administration, Hangzhou, China
Search for more papers by this authorDong-Sheng Zhang
College of Life Sciences, Zhejiang University, Hangzhou, China
Laboratory of Marine Ecosystem and Biogeochemistry, State Oceanic Administration, Hangzhou, China
The Second Institute of Oceanography, State Oceanic Administration, Hangzhou, China
Search for more papers by this authorJian-Yu Ni
Laboratory of Marine Ecosystem and Biogeochemistry, State Oceanic Administration, Hangzhou, China
The Second Institute of Oceanography, State Oceanic Administration, Hangzhou, China
Search for more papers by this authorCorresponding Author
Min Wu
College of Life Sciences, Zhejiang University, Hangzhou, China
Correspondence: Min Wu, College of Life Sciences, Zhejiang University, Hangzhou 310058, China. Tel.: +86 571 88206595; fax: +86 571 88206048; e-mail: [email protected].Search for more papers by this authorLi Liao
College of Life Sciences, Zhejiang University, Hangzhou, China
Search for more papers by this authorXue-Wei Xu
Laboratory of Marine Ecosystem and Biogeochemistry, State Oceanic Administration, Hangzhou, China
The Second Institute of Oceanography, State Oceanic Administration, Hangzhou, China
Search for more papers by this authorXia-Wei Jiang
College of Life Sciences, Zhejiang University, Hangzhou, China
Search for more papers by this authorChun-Sheng Wang
Laboratory of Marine Ecosystem and Biogeochemistry, State Oceanic Administration, Hangzhou, China
The Second Institute of Oceanography, State Oceanic Administration, Hangzhou, China
Search for more papers by this authorDong-Sheng Zhang
College of Life Sciences, Zhejiang University, Hangzhou, China
Laboratory of Marine Ecosystem and Biogeochemistry, State Oceanic Administration, Hangzhou, China
The Second Institute of Oceanography, State Oceanic Administration, Hangzhou, China
Search for more papers by this authorJian-Yu Ni
Laboratory of Marine Ecosystem and Biogeochemistry, State Oceanic Administration, Hangzhou, China
The Second Institute of Oceanography, State Oceanic Administration, Hangzhou, China
Search for more papers by this authorCorresponding Author
Min Wu
College of Life Sciences, Zhejiang University, Hangzhou, China
Correspondence: Min Wu, College of Life Sciences, Zhejiang University, Hangzhou 310058, China. Tel.: +86 571 88206595; fax: +86 571 88206048; e-mail: [email protected].Search for more papers by this authorAbstract
Cobalt-rich crusts are important metallic mineral resources with great economic potential, usually distributed on seamounts located in the Pacific Ocean. Microorganisms are believed to play a role in the formation of crusts as well as in metal cycling. To explore the microbial diversity related to cobalt-rich crusts, 16S ribosomal RNA gene clone libraries were constructed from three consecutive sediment layers. In total, 417 bacterial clones were obtained from three bacterial clone libraries, representing 17 distinct phylogenetic groups. Proteobacteria dominated in the bacterial communities, followed by Acidobacteria and Planctomycetes. Compared with high bacterial diversity, archaea showed a remarkably low diversity, with all 137 clones belonging to marine archaeal group I except one novel euryarchaeotal clone. The microbial communities were potentially involved in sulfur, nitrogen and metal cycling in the area of cobalt-rich crusts. Sulfur oxidation and metal oxidation were potentially major sources of energy for this ecosystem. This is the first reported investigation of microbial diversity in sediments associated with cobalt-rich crusts, and it casts fresh light on the microbial ecology of these important ecosystems.
References
- Alonso A, Sanchez P & Martínez JL (2000) Stenotrophomonas maltophilia D457R contains a cluster of genes from gram-positive bacteria involved in antibiotic and heavy metal resistance. Antimicrob Agents Chemother 44: 1778–1782.
- Altschul SF, Gish W, Miller W, Myers EW & Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215: 403–410.
- Amaral-Zettler LA, Rocca JD, Lamontagne MG, Dennett MR & Gast RJ (2008) Changes in microbial community structure in the wake of Hurricanes Katrina and Rita. Environ Sci Technol 42: 9072–9078.
- Amaral-Zettler LA, McCliment EA, Ducklow HW & Huse SM (2009) A method for studying protistan diversity using massively parallel sequencing of V9 hypervariable regions of small-subunit ribosomal RNA genes. PLoS ONE 4: 6372.
- Anzai Y, Kim H, Park JY, Wakabayashi H & Oyaizu H (2000) Phylogenetic affiliation of the pseudomonads based on 16S rRNA sequence. Int J Syst Evol Microbiol 50: 1563–1589.
- Baker GC, Smith JJ & Cowan DA (2003) Review and re-analysis of domain-specific 16S primers. J Microbiol Methods 55: 541–555.
- Chao A & Lee SM (1992) Estimating the number of classes via sample coverage. J Am Stat Assoc 87: 210–217.
- Church MJ, DeLong EF, Ducklow HW, Karner MB, Preston CM & Karl DM (2003) Abundance and distribution of planktonic archaea and bacteria in the waters west of the Antarctic Peninsula. Limnol Oceanogr 48: 1893–1902.
- Cole JR, Chai B, Marsh TL et al. (2003) The Ribosomal Database Project (RDP-II): previewing a new autoaligner that allows regular updates and the new prokaryotic taxonomy. Nucl Acids Res 31: 442–443.
- Delong EF (1992) Archaea in coastal marine environments. P Natl Acad Sci USA 89: 5685–5689.
- Dojka MA, Hugenholtz P, Haack SK & Pace NR (1998) Microbial diversity in a hydrocarbon- and chlorinated-solvent-contaminated aquifer undergoing intrinsic bioremediation. Appl Environ Microbiol 64: 3869–3877.
- Edwards KJ, Rogers DR, Wirsen CO & McCollom TM (2003) Isolation and characterization of novel psychrophilic, neutrophilic, Fe-oxidizing, chemolithoautotrophic α- and γ-Proteobacteria from the Deep Sea. Appl Environ Microbiol 69: 2906–2913.
- Emerson D & Moyer C (1997) Isolation and characterization of novel iron-oxidizing bacteria that grow at circumneutral pH. Appl Environ Microbiol 63: 4784–4792.
- Francis CA, Co E-M & Tebo BM (2001) Enzymatic manganese(II) oxidation by a marine α-Proteobacterium. Appl Environ Microbiol 67: 4024–4029.
- Gao HC, Obraztova A, Stewart N et al. (2006) Shewanella loihica sp. nov., isolated from iron-rich microbial mats in the Pacific Ocean. Int J Syst Evol Microbiol 56: 1911–1916.
- Gillan DC & Danis B (2007) The archaebacterial communities in Antarctic bathypelagic sediments. Deep Sea Res Part 2 Top Stud Oceanogr 54: 1682–1690.
- Glasby GP (2000) Economic geology: lessons learned from deep-sea mining. Science 289: 551–553.
- Glasby G, Stoffers P, Sioulas A, Thijssen T & Friedrich G (1982) Manganese nodule formation in the Pacific Ocean: a general theory. Geo-Mar Lett 2: 47–53.
- Glasby GP, Ren XW, Shi XF & Pulyaeva IA (2007) Co-rich Mn crusts from the Magellan Seamount cluster: the long journey through time. Geo-Mar Lett 27: 315–323.
- Halfar J & Fujita RM (2002) Precautionary management of deep-sea mining. Mar Policy 26: 103–106.
- Hauben L, Vauterin L, Moore ERB, Hoste B & Swings J (1999) Genomic diversity of the genus Stenotrophomonas. Int J Syst Bacteriol 49: 1749–1760.
- Heijs SK, Laverman AM, Forney LJ, Hardoim PR & van Elsas JD (2008) Comparison of deep-sea sediment microbial communities in the Eastern Mediterranean. FEMS Microbiol Ecol 64: 362–377.
- Hein JR, Koschinsky A, Bau M, Manheim FT, Kang JK & Roberts L (2000) Cobalt-rich ferromanganese crusts in the Pacific. Handbook of Marine Mineral Deposits ( DS Cronan, ed.), pp. 239–279. CRC Press, Boca Raton, FL.
- Karner MB, DeLong EF & Karl DM (2001) Archaeal dominance in the mesopelagic zone of the Pacific Ocean. Nature 409: 507–510.
- Kemp PF & Aller JY (2004) Bacterial diversity in aquatic and other environments: what 16S rDNA libraries can tell us. FEMS Microbiol Ecol 47: 161–177.
- Konishi Y, Asai S & Sawada Y (1997) Leaching of marine manganese nodules by acidophilic bacteria growing on elemental sulfur. Metallurg Mater Trans B 28: 25–32.
- Konneke M, Bernhard AE, de la Torre JR, Walker CB, Waterbury JB & Stahl DA (2005) Isolation of an autotrophic ammonia-oxidizing marine archaeon. Nature 437: 543–546.
- Krishnan KP, Fernandes CEG, Fernandes SO & Bharathi PAL (2006) Tolerance and immobilization of cobalt by some bacteria from ferromanganese crusts of the Afanasiy Nikitin Seamounts. Geomicrobiol J 23: 31–36.
- Kurata A (1974) Cobalt content in the shallow sea sediments. J Oceanogr 30: 199–202.
- Lee Y & Tebo BM (1994) Cobalt(II) oxidation by the marine manganese(II)-oxidizing Bacillus sp. strain SG-1. Appl Environ Microbiol 60: 2949–2957.
- Li H, Yu Y, Luo W, Zeng Y & Chen B (2008a) Bacterial diversity in surface sediments from the Pacific Arctic Ocean. Extremophiles 13: 233–246.
- Li YX, Li FC, Zhang XW, Qin S, Zeng ZG, Dang HY & Qin YS (2008b) Vertical distribution of bacterial and archaeal communities along discrete layers of a deep-sea cold sediment sample at the East Pacific Rise (approximately 13 degrees N). Extremophiles 12: 573–585.
- Liang DH & Zhu B (2000) Distribution and classification of cobalt-rich crust. J China Univ Geosci 11: 146–149.
- Liao L, Xu XW, Wang CS, Zhang DS & Wu M (2009) Bacterial and archaeal communities in the surface sediment from the northern slope of the South China Sea. J Zhejiang Univ Sci B 10: 890–901.
- Ling HF, Jiang SY, Frank M et al. (2005) Differing controls over the Cenozoic Pb and Nd isotope evolution of deepwater in the central North Pacific Ocean. Earth Planet Sci Lett 232: 345–361.
- Mason OU, Stingl U, Wilhelm LJ, Moeseneder MM, Meo-Savoie CAD, Fisk MR & Giovannoni SJ (2007) The phylogeny of endolithic microbes associated with marine basalts. Environ Microbiol 9: 2539–2550.
- McCallum JAF & Davis AA (1992) Novel major archaebacterial group from marine plankton. Nature 356: 148–149.
- Murray KJ, Webb SM, Bargar JR & Tebo BM (2007) Indirect oxidation of Co(II) in the presence of the marine Mn(II)-oxidizing bacterium Bacillus sp strain SG-1. Appl Environ Microbiol 73: 6905–6909.
- Nealson KH (2006) The manganese-oxidizing bacteria. Prokaryotes, vol. 5 ( M Dworkin, S Falkow, E Rosenberg, KH Schleifer & E Stackebrandt, eds), pp. 222–231. Springer, New York, NY.
- Nicholls GD & Islam MR (1971) Geochemical investigations of basalts and associated rocks from the ocean floor and their implications. Philos Trans R Soc Lond A 268: 469–486.
- Northup DE, Barns SM, Yu LE et al. (2003) Diverse microbial communities inhabiting ferromanganese deposits in Lechuguilla and Spider Caves. Environ Microbiol 5: 1071–1086.
- Pages D, Rose J, Conrod S, Cuine S, Carrier P, Heulin T & Achouak W (2008) Heavy metal tolerance in Stenotrophomonas maltophilia. PLoS ONE 3: e1539.
- Palleroni NJ & Bradbury JF (1993) Stenotrophomonas, a new bacterial genus for Xanthomonas maltophilia (Hugh 1980) Swings et al. 1983. Int J Syst Bacteriol 43: 606–609.
- Polymenakou PN, Bertilsson S, Tselepides A & Stephanou EG (2005) Bacterial community composition in different sediments from the Eastern Mediterranean Sea: a comparison of four 16S ribosomal DNA clone libraries. Microb Ecol 50: 447–462.
10.1007/s00248-005-0005-6 Google Scholar
- Reynolds JR, Langmuir CH, Bender JF, Kastens KA & Ryan WBF (1992) Spatial and temporal variability in the geochemistry of basalts from the East Pacific Rise. Nature 359: 493–499.
- Roh Y, Gao HC, Vali H et al. (2006) Metal reduction and iron biomineralization by a psychrotolerant Fe(III)-reducing bacterium, Shewanella sp. Strain PV-4. Appl Environ Microbiol 72: 3236–3244.
- Rosson RA & Nealson KH (1982) Manganese binding and oxidation by spores of a marine bacillus. J Bacteriol 151: 1027–1034.
- Saitou N & Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4: 406–425.
- Santelli CM, Orcutt BN, Banning E et al. (2008) Abundance and diversity of microbial life in ocean crust. Nature 453: 653–657.
- Schloss PD & Handelsman J (2005) Introducing DOTUR, a computer program for defining operational taxonomic units and estimating species richness. Appl Environ Microbiol 71: 1501–1506.
- Schloss PD, Westcott SL, Ryabin T et al. (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75: 7537–7541.
- Sørensen KB, Lauer A & Teske A (2004) Archaeal phylotypes in a metal-rich and low-activity deep subsurface sediment of the Peru Basin, ODP Leg 201, Site 1231. Geobiology 2: 151–161.
- Sorokin DY, Tourova TP, Kolganova TV, Sjollema KA & Kuenen JG (2002) Thioalkalispira microaerophila gen. nov., sp. nov., a novel lithoautotrophic, sulfur-oxidizing bacterium from a soda lake. Int J Syst Evol Microbiol 52: 2175–2182.
- Stein LY, Duc MTL, Grundl TJ & Nealson KH (2001) Bacterial and archaeal populations associated with freshwater ferromanganous micronodules and sediments. Environ Microbiol 3: 10–18.
- Tamura K, Dudley J, Nei M & Kumar S (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 24: 1596–1599.
- Tebo BM, Ghiorse WC, van Waasbergen LG, Siering PL & Caspi R (1997) Bacterially mediated mineral formation; insights into manganese(II) oxidation from molecular genetic and biochemical studies. Rev Miner Geochem 35: 225–266.
- Templeton A, Staudigel H & Tebo BM (2005) Diverse Mn(II)-oxidizing bacteria isolated from submarine basalts at Loihi Seamount. Geomicrobiol J 22: 127–139.
- Tourova TP, Spiridonova EM, Berg IA, Slobodova NV, Boulygina ES & Sorokin DY (2007) Phylogeny and evolution of the family Ectothiorhodospiraceae based on comparison of 16S rRNA, cbbL and nifH gene sequences. Int J Syst Evol Microbiol 57: 2387–2398.
- Wang XH & Müller WEG (2009) Marine biominerals: perspectives and challenges for polymetallic nodules and crusts. Trends Biotechnol 27: 375–383.
- Wang XH, Schloßmacher U, Wiens M, Schröder HC & Müller WEG (2009a) Biogenic origin of polymetallic nodules from the Clarion-Clipperton Zone in the Eastern Pacific Ocean: electron microscopic and EDX evidence. Mar Biotechnol 11: 99–108.
- Wang XH, Schloßmacher U, Natalio F, Schröder HC, Wolf SE, Tremel W & Müller WEG (2009b) Evidence for biogenic processes during formation of ferromanganese crusts from the Pacific Ocean: implications of biologically induced mineralization. Micron 40: 526–535.
- Wang CS, Liao L, Xu HX, Xu XW, Wu M & Zhu LZ (2010) Bacterial diversity in the sediment from polymetallic nodule fields of the Clarion-Clipperton Fracture Zone. J Microbiol 48: 573–585.
- Wedepohl KH (1995) The composition of the continental crust. Geochim Cosmochim Acta 59: 1217–1232.
- Weidler GW, Dornmayr-Pfaffenhuemer M, Gerbl FW, Heinen W & Stan-Lotter H (2007) Communities of Archaea and Bacteria in a subsurface radioactive thermal spring in the Austrian Central Alps, and evidence of ammonia-oxidizing Crenarchaeota. Appl Environ Microbiol 73: 259–270.
- Weinberger J, Proops DW & Hawke M (1986) Casts and crusts of the tympanic membrane. Acta Otolaryngol 102: 44–51.
- Xu MX, Wang P, Wang FP & Xiao X (2005) Microbial diversity at a deep-sea station of the Pacific Nodule Province. Biodivers Conserv 14: 3363–3380.
- Xu MX, Wang FP, Meng J & Xiao X (2007) Construction and preliminary analysis of a metagenomic library from a deep-sea sediment of east Pacific Nodule Province. FEMS Microbiol Ecol 62: 233–241.
- Xu HX, Wu M, Wang XG, Yang JY & Wang CS (2008) Bacterial diversity in deep-sea sediment from northeastern Pacific Ocean. Acta Ecol Sinica 28: 479–485.
- Zhang W, Ki JS & Qian PY (2008) Microbial diversity in polluted harbor sediments I: bacterial community assessment based on four clone libraries of 16S rDNA. Estuar Coast Shelf Sci 76: 668–681.
- Zuo Y, Xing D, Regan JM & Logan BE (2008) Isolation of the exoelectrogenic bacterium ochrobactrum anthropi YZ-1 by using a U-tube microbial fuel cell. Appl Environ Microbiol 74: 3130–3137.
