Acta Oceanologica Sinica

, Volume 34, Issue 4, pp 92–113 | Cite as

Ecological functions of uncultured microorganisms in the cobalt-rich ferromanganese crust of a seamount in the central Pacific are elucidated by fosmid sequencing

  • Yingyi Huo
  • Hong Cheng
  • Anton F. Post
  • Chunsheng Wang
  • Xiawei Jiang
  • Jie Pan
  • Min Wu
  • Xuewei XuEmail author


Cobalt-rich ferromanganese is an important seafloor mineral and is abundantly present in the seamount crusts. Such crusts form potential hotspots for biogeochemical activity and microbial diversity, yet our understanding of their microbial communities is lacking. In this study, a cultivation-independent approach was used to recover genomic information and derive ecological functions of the microbes in a sediment sample collected from the cobalt-rich ferromanganese crust of a seamount region in the central Pacific. A total of 78 distinct clones were obtained by fosmid library screening with a 16S rRNA based PCR method. Proteobacteria and MGI Thaumarchaeota dominated the bacterial and archaeal 16S rRNA gene sequence results in the microbial community. Nine fosmid clones were sequenced and annotated. Numerous genes encoding proteins involved in metabolic functions and heavy metal resistance were identified, suggesting alternative metabolic pathways and stress responses that are essential for microbial survival in the cobalt-rich ferromanganese crust. In addition, genes that participate in the synthesis of organic acids and exoploymers were discovered. Reconstruction of the metabolic pathways revealed that the nitrogen cycle is an important biogeochemical process in the cobalt-rich ferromanganese crust. In addition, horizontal gene transfer (HGT) events have been observed, and most of them came from bacteria, with some occurring in archaea and plants. Clone W4-93a, belonging to MGI Thaumarchaeota, contained a region of gene synteny. Comparative analyses suggested that a high frequency of HGT events as well as genomic divergence play important roles in the microbial adaption to the deep-sea environment.

Key words

seamount cobalt-rich ferromanganese crust metagenome horizontal gene transfer 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Adachi O, Ano Y, Toyama H, et al. 2007. Biooxidation with PQQ- and FAD-dependent dehydrogenases. In: Schmid R D, Urlacher V B, eds. Modern Biooxidation: Enzymes, Reactions and Applications. Hoboken, NJ: John Wiley & Sons, Inc, 41Google Scholar
  2. Béjà O, Koonin E V, Aravind L, et al. 2002. Comparative genomic analysis of archaeal genotypic variants in a single population and in two different oceanic provinces. Applied and Environmental Microbiology, 68(1): 335–345CrossRefGoogle Scholar
  3. Beman J M, Popp B N, Alford S E. 2012. Quantification of ammonia oxidation rates and ammonia-oxidizing archaea and bacteria at high resolution in the Gulf of California and eastern tropical North Pacific Ocean. Limnology and Oceanography, 57(3): 711–726CrossRefGoogle Scholar
  4. Blainey P C, Mosier A C, Potanina A, et al. 2011. Genome of a low-salinity ammonia-oxidizing archaeon determined by single-cell and metagenomic analysis. PLoS One, 6(2): e16626CrossRefGoogle Scholar
  5. Candela T, Fouet A. 2006. Poly-gamma-glutamate in bacteria. Molecular Microbiology, 60(5): 1091–1098CrossRefGoogle Scholar
  6. Clark M R, Rowden A A, Schlacher T, et al. 2010. The ecology of seamounts: structure, function, and human impacts. Ann Rev Mar Sci, 2: 253–278CrossRefGoogle Scholar
  7. Craig J D, Andrews J E, Meylan M A. 1982. Ferromanganese deposits in the Hawaiian Archipelago. Marine Geology, 45(1–2): 127–157CrossRefGoogle Scholar
  8. Delaney M L. 1998. Phosphorus accumulation in marine sediments and the oceanic phosphorus cycle. Global Biogeochemical Cycles, 12(4): 563–572CrossRefGoogle Scholar
  9. Dell’Anno A, Danovaro R. 2005. Extracellular DNA plays a key role in deep-sea ecosystem functioning. Science, 309(5744): 2179CrossRefGoogle Scholar
  10. DeLong E F. 1992. Archaea in coastal marine environments. Proceedings of the National Academy of Sciences of the United States of America, 89(12): 5685–5689CrossRefGoogle Scholar
  11. Duffy E J. 2008. ‘Seamount”. CenSeam: a global census of marine life on seamounts content partner and national oceanic and atmospheric administration content source. In: Cleveland C J, ed. Encycleopedia of Earth. Washington DC: Environmental Information Coalition, National Council for Science and the EnvironmentGoogle Scholar
  12. Ehrhardt C J, Haymon R M, Lamontagne M G, et al. 2007. Evidence for hydrothermal Archaea within the basaltic flanks of the East Pacific Rise. Environmental Microbiology, 9(4): 900–912CrossRefGoogle Scholar
  13. Emerson D, Moyer C L. 2010. Microbiology of seamounts: common patterns observed in community structure. Oceanography, 23: 148–163CrossRefGoogle Scholar
  14. Finkel S E. 2006. Long-term survival during stationary phase: evolution and the GASP phenotype. Nat Rev Microbiol, 4(2): 113–120CrossRefGoogle Scholar
  15. Finkel S E, Kolter R. 2001. DNA as a nutrient: novel role for bacterial competence gene homologs. Journal of Bacteriology, 183(21): 6288–6293CrossRefGoogle Scholar
  16. Fu Yazhou, Peng Jiantang, Qu Wenjun, et al. 2005. Os isotopic compositions of a cobalt-rich ferromanganese crust profile in Central Pacific. Chin Sci Bull, 50(18): 2106–2112CrossRefGoogle Scholar
  17. Gadd G M. 2007. Geomycology: biogeochemical transformations of rocks, minerals, metals and radionuclides by fungi, bioweathering and bioremediation. Mycological Research, 111(Pt 1): 3–49CrossRefGoogle Scholar
  18. García-Martínez J, Martínez-Murcia A, Antón A I, et al. 1996. Comparison of the small 16S to 23S intergenic spacer region (ISR) of the rRNA operons of some Escherichia coli strains of the ECOR collection and E. coli K-12. Journal of Bacteriology, 178(21): 6374–6377Google Scholar
  19. Ghiorse W C. 1984. Biology of iron- and manganese-depositing bacteria. Annu Rev Microbiol, 38: 515–550CrossRefGoogle Scholar
  20. Gillan D C, Danis B. 2007. The archaebacterial communities in Antarctic bathypelagic sediments. Deep-Sea Research Part II: Topical Studies in Oceanography, 54(16–17): 1682–1690CrossRefGoogle Scholar
  21. Guibaud G, van Hullebusch E, Bordas F, et al. 2009. Sorption of Cd(II) and Pb(II) by exopolymeric substances (EPS) extracted from activated sludges and pure bacterial strains: Modeling of the metal/ligand ratio effect and role of the mineral fraction. Bioresource Technology, 100(12): 2959–2968CrossRefGoogle Scholar
  22. Heijs S K, Haese R R, van der Wielen P W, et al. 2007. Use of 16S rRNA gene based clone libraries to assess microbial communities potentially involved in anaerobic methane oxidation in a Mediterranean cold seep. Microbial Ecology, 53(3): 384–398CrossRefGoogle Scholar
  23. Hillier J K, Watts A B. 2007. Global distribution of seamounts from ship-track bathymetry data. Geophysical Research Letters, 34(13): L13304CrossRefGoogle Scholar
  24. Ito M, Tsunekawa M, Yamaguchi E, et al. 2008. Estimation of degree of liberation in a coarse crushed product of cobalt-rich ferromanganese crust/nodules and its gravity separation. International Journal of Mineral Processing, 87(3–4): 100–105CrossRefGoogle Scholar
  25. Iyer S D, Mehta M C, Das P, et al. 2012. Seamounts—characteristics, formation, mineral deposits and biodiversity. Geologica Acta, 10(3): 295–308Google Scholar
  26. Jiang Xiawei, Xu Xuewei, Huo Yingyi, et al. 2012. Identification and characterization of novel esterases from a deep-sea sediment metagenome. Archives of Microbiology, 194(3): 207–214CrossRefGoogle Scholar
  27. Könneke M, Bernhard A E, de la Torre J R, et al. 2005. Isolation of an autotrophic ammonia-oxidizing marine archaeon. Nature, 437(7058): 543–546CrossRefGoogle Scholar
  28. Kanehisa M, Goto S. 2000. KEGG: kyoto encyclopedia of genes and genomes. Nucleic Acids Research, 28(1): 27–30CrossRefGoogle Scholar
  29. Kato S, Kobayashi C, Kakegawa T, et al. 2009. Microbial communities in iron-silica-rich microbial mats at deep-sea hydrothermal fields of the Southern Mariana Trough. Environmental Microbiology, 11(8): 2094–2111CrossRefGoogle Scholar
  30. Kato S, Yanagawa K, Sunamura M, et al. 2009. Abundance of Zetaproteobacteria within crustal fluids in back-arc hydrothermal fields of the Southern Mariana Trough. Environmental Microbiology, 11(12): 3210–3222CrossRefGoogle Scholar
  31. Koschinsky A, Hein J R. 2003. Uptake of elements from seawater by ferromanganese crusts: solid-phase associations and seawater speciation. Marine Geology, 198(3–4): 331–351CrossRefGoogle Scholar
  32. Li Meng, Gu Jidong. 2013. Community structure and transcript responses of anammox bacteria, AOA, and AOB in mangrove sediment microcosms amended with ammonium and nitrite. Applied Microbiology and Biotechnology, 97(22): 9859–9874CrossRefGoogle Scholar
  33. Li Youxun, Li Fuchao, Zhang Xiaowen, et al. 2008. Vertical distribution of bacterial and archaeal communities along discrete layers of a deep-sea cold sediment sample at the East Pacific Rise (∼13°N). Extremophiles, 12(4): 573–585CrossRefGoogle Scholar
  34. Liao L, Xu X W, Jiang X W, et al. 2011. Microbial diversity in deep-sea sediment from the cobalt-rich crust deposit region in the Pacific Ocean. FEMS Microbiology Ecology, 78(3): 565–585CrossRefGoogle Scholar
  35. Lopez-Diaz I, Clarke S, Mandelstam J. 1986. spoIID Operon of Bacillus subtilis: cloning and sequence. Journal of General Microbiology, 132(2): 341–354Google Scholar
  36. Lösekann T, Knittel K, Nadalig T, et al. 2007. Diversity and abundance of aerobic and anaerobic methane oxidizers at the Haakon Mosby Mud Volcano, Barents Sea. Applied and Environmental Microbiology, 73(10): 3348–3362CrossRefGoogle Scholar
  37. Martín-Cuadrado A B, López-García P, Alba J C, et al. 2007. Metagenomics of the deep Mediterranean, a warm bathypelagic habitat. PLoS One, 2(9): e914CrossRefGoogle Scholar
  38. Martin-Cuadrado A B, Rodriguez-Valera F, Moreira D, et al. 2008. Hindsight in the relative abundance, metabolic potential and genome dynamics of uncultivated marine archaea from comparative metagenomic analyses of bathypelagic plankton of different oceanic regions. The ISME Journal, 2(8): 865–886CrossRefGoogle Scholar
  39. Menard H W. 1964. Marine Geology of the Pacific. New York: Mc-Graw-HillGoogle Scholar
  40. Miroshnichenko M, Hippe H, Stackebrandt E, et al. 2001. Isolation and characterization of Thermococcus sibiricus sp. nov. from a Western Siberia high-temperature oil reservoir. Extremophiles, 5(2): 85–91CrossRefGoogle Scholar
  41. Muiños S B, Hein J R, Frank M, et al. 2013. Deep-sea Fe-Mn crusts from the Northeast Atlantic Ocean: composition and resource considerations. Marine Georesources & Geotechnology, 31(1): 40–70CrossRefGoogle Scholar
  42. Nies D H. 1992. Resistance to cadmium, cobalt, zinc, and nickel in microbes. Plasmid, 27(1): 17–28CrossRefGoogle Scholar
  43. Norton J M, Klotz M G, Stein L Y, et al. 2008. Complete genome sequence of Nitrosospira multiformis, an ammonia-oxidizing bacterium from the soil environment. Applied and Environmental Microbiology, 74(11): 3559–3572CrossRefGoogle Scholar
  44. Rowden A A, Dower J F, Schlacher T A, et al. 2010. Paradigms in seamount ecology: fact, fiction and future. Marine Ecology, 31(Supp): 226–241CrossRefGoogle Scholar
  45. Santelli C M, Orcutt B N, Banning E, et al. 2008. Abundance and diversity of microbial life in ocean crust. Nature, 453(7195): 653–656CrossRefGoogle Scholar
  46. Santelli C M, Webb S M, Dohnalkova A C, et al. 2011. Diversity of Mn oxides produced by Mn(II)-oxidizing fungi. Geochimica et Cosmochimica Acta, 75(10): 2762–2776CrossRefGoogle Scholar
  47. Schauer R, Bienhold C, Ramette A, et al. 2009. Bacterial diversity and biogeography in deep-sea surface sediments of the South Atlantic Ocean. The ISME Journal, 4(2): 159–170CrossRefGoogle Scholar
  48. Schenau S J, De Lange G J. 2001. Phosphorus regeneration vs. burial in sediments of the Arabian Sea. Marine Chemistry, 75(3): 201–217CrossRefGoogle Scholar
  49. Schlacher T A, Rowden A A, Dower J F, et al. 2010. Seamount science scales undersea mountains: new research and outlook. Marine Ecology, 31(Supp): 1–13CrossRefGoogle Scholar
  50. Staudigel H, Koppers A A P, Plank T A, et al. 2010. Seamounts in the subduction factory. Oceanography, 23(1): 176–181CrossRefGoogle Scholar
  51. Tamura K, Peterson D, Peterson N, et al. 2011. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution, 28(10): 2731–2739CrossRefGoogle Scholar
  52. Tatusov R L, Galperin M Y, Natale D A, et al. 2000. The COG database: a tool for genome-scale analysis of protein functions and evolution. Nucleic Acids Research, 28(1): 33–36CrossRefGoogle Scholar
  53. Tebo B M, Bargar J R, Clement B G, et al. 2004. Biogenic manganese oxides: properties and mechanisms of formation. Annual Review of Earth and Planetary Sciences, 32: 287–328CrossRefGoogle Scholar
  54. Verlaan P A. 1992. Benthic recruitment and manganese crust formation on seamounts. Marine Biology, 113(1): 171–174CrossRefGoogle Scholar
  55. Walker C B, de la Torre J R, Klotz M G, et al. 2010. Nitrosopumilus maritimus genome reveals unique mechanisms for nitrification and autotrophy in globally distributed marine crenarchaea. Proceedings of the National Academy of Sciences of the United States of America, 107(19): 8818–8823CrossRefGoogle Scholar
  56. Wang Xiaohong, Müller W E G. 2009. Marine biominerals: perspectives and challenges for polymetallic nodules and crusts. Trends in Biotechnology, 27(6): 375–383CrossRefGoogle Scholar
  57. Wang Xiaohong, Schlossmacher U, Natalio F, et al. 2009. Evidence for biogenic processes during formation of ferromanganese crusts from the Pacific Ocean: implications of biologically induced mineralization. Micron, 40(5–6): 526–535CrossRefGoogle Scholar
  58. Wang Xiaohong, Wiens M, Schröder H, et al. 2011. Molecular biomineralization: toward an understanding of the biogenic origin of polymetallic nodules, seamount crusts, and hydrothermal vents. In: Müller W E G, ed. Molecular Biomineralization. Berlin Heidelberg: Springer, 77–110CrossRefGoogle Scholar
  59. Wedepohl K H. 1995. The composition of the continental crust. Geochimica et Cosmochimica Acta, 59(7): 1217–1232CrossRefGoogle Scholar
  60. Wessel P, Sandwell D T, Kim S S. 2010. The global seamount census. Oceanography, 23(1): 24–33CrossRefGoogle Scholar
  61. Wright J J, Konwar K M, Hallam S J. 2012. Microbial ecology of expanding oxygen minimum zones. Nat Rev Microbiol, 10(6): 381–394Google Scholar
  62. Wu Yuehong, Liao Li, Wang Chunsheng, et al. 2013. A comparison of microbial communities in deep-sea polymetallic nodules and the surrounding sediments in the Pacific Ocean. Deep-Sea Research Part I: Oceanographic Research Papers, 79: 40–49CrossRefGoogle Scholar
  63. Xu Meixiang, Wang Peng, Wang Fengping, et al. 2005. Microbial diversity at a deep-sea station of the Pacific nodule province. Biodiversity & Conservation, 14(14): 3363–3380CrossRefGoogle Scholar
  64. Yesson C, Clark M R, Taylor M L, et al. 2011. The global distribution of seamounts based on 30 arc seconds bathymetry data. Deep-Sea Research Part I: Oceanographic Research Papers, 58(4): 442–453CrossRefGoogle Scholar
  65. Zhang Hui, Sekiguchi Y, Hanada S, et al. 2003. Gemmatimonas aurantiaca gen. nov., sp. nov., a Gram-negative, aerobic, polyphosphate-accumulating micro-organism, the first cultured representative of the new bacterial phylum Gemmatimonadetes phyl. nov. International Journal of Systematic and Evolutionary Microbiology, 53(4): 1155–1163CrossRefGoogle Scholar
  66. Zhang Fuyuan, Zhang Weiyan, Zhu Kechao, et al. 2008. Distribution characteristics of cobalt-rich ferromanganese crust resources on submarine seamounts in the Western Pacific. Acta Geologica Sinica, 82(4): 796–803Google Scholar
  67. Zhao Qiyuan. 1988. Ocean Geochemistry. Beijing: The Geological Publishing HouseGoogle Scholar
  68. Zhu Wenhan, Lomsadze A, Borodovsky M. 2010. Ab initio gene identification in metagenomic sequences. Nucleic Acids Research, 38(12): e132CrossRefGoogle Scholar

Copyright information

© The Chinese Society of Oceanography and Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • Yingyi Huo
    • 1
    • 2
  • Hong Cheng
    • 3
  • Anton F. Post
    • 4
  • Chunsheng Wang
    • 1
    • 2
  • Xiawei Jiang
    • 5
  • Jie Pan
    • 3
  • Min Wu
    • 3
  • Xuewei Xu
    • 1
    • 2
    Email author
  1. 1.Laboratory of Marine Ecosystem and Biogeochemistry, Second Institute of OceanographyState Oceanic AdministrationHangzhouChina
  2. 2.State Key Laboratory of Satellite Ocean Environment DynamicsSecond Institute of OceanographyHangzhouChina
  3. 3.College of Life SciencesZhejiang UniversityHangzhouChina
  4. 4.Marine Biology LaboratoryThe Josephine Bay Paul Center for Comparative Molecular Biology and EvolutionWoods HoleUSA
  5. 5.State Key Laboratory for Diagnosis and Treatment of Infectious Diseases, the First Affiliated Hospital, School of MedicineZhejiang UniversityHangzhouChina

Personalised recommendations