Diversity, abundance and distribution of amoA-encoding archaea in deep-sea methane seep sediments of the Okhotsk Sea

FEMS Microbiology Ecology

Volumn 72, Issue 3, 2010, Pages 370-385

  Dang, Hongyue ^a   Luan, Xi Wu ^b   Chen, Ruipeng ^a,c   Zhang, Xiaoxia ^a   Guo, Lizhong ^c   Klotz, Martin G ^a,d  

^a CHINA UNIVERSITY OF PETROLEUM   (China)

^b INSTITUTE OF OCEANOLOGY   (China)

^c QINGDAO AGRICULTURAL UNIVERSITY   (China)

^d University of Louisville School of Medicine   (United States)

Author keywords

Ammonia oxidizing archaea; AmoA encoding archaea; Deep sea sediment; Gas hydrate; Methane seep; Okhotsk Sea

Indexed keywords

AMMONIA MONOOXYGENASE; ARCHAEAL DNA; METHANE; OXIDOREDUCTASE; RNA 16S; SEA WATER;

ABUNDANCE; CORRELATION; DEEP-SEA SEDIMENT; EVOLUTIONARY THEORY; GAS HYDRATE; GENETIC ANALYSIS; HYDROTHERMAL VENT COMMUNITY; METHANE; MICROBIAL COMMUNITY; POPULATION DISTRIBUTION; SPECIES DIVERSITY;

ARCHAEAL GENE; ARCHAEBACTERIUM; ARTICLE; BIODIVERSITY; CLASSIFICATION; DNA SEQUENCE; ENZYMOLOGY; GENE LIBRARY; GENETICS; ISOLATION AND PURIFICATION; MICROBIOLOGY; PHYLOGENY; SEDIMENT;

ARCHAEA; BIODIVERSITY; DNA, ARCHAEAL; GENE LIBRARY; GENES, ARCHAEAL; GEOLOGIC SEDIMENTS; METHANE; OXIDOREDUCTASES; PHYLOGENY; RNA, RIBOSOMAL, 16S; SEAWATER; SEQUENCE ANALYSIS, DNA; WATER MICROBIOLOGY;

PACIFIC OCEAN; SEA OF OKHOTSK;

ARCHAEA; BACTERIA (MICROORGANISMS); NITROSOMONADALES;

EID: 77951942938     PISSN: 01686496     EISSN: 15746941     Source Type: Journal    
DOI: 10.1111/j.1574-6941.2010.00870.x     Document Type: Article

References (72)

1. Agogué H, Brink M, Dinasquet J Herndl GJ (2008) Major gradients in putatively nitrifying and non-nitrifying Archaea in the deep North Atlantic. Nature 456 : 788 791.
2. Altschul S, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W Lipman DJ (1997) Gapped BLAST and PSI-BLAST: A new generation of protein database search programs. Nucleic Acids Res 25 : 3389 3402. (Pubitemid 27359211)
3. Arakawa S, Sato T, Sato R et al 2006a) Molecular phylogenetic and chemical analyses of the microbial mats in deep-sea cold seep sediments at the northeastern Japan Sea. Extremophiles 10 : 311 319. (Pubitemid 44325661)
4. Arakawa S, Sato T, Yoshida Y, Usami R Kato C (2006b) Comparison of the microbial diversity in cold-seep sediments from different depths in the Nankai Trough. J Gen Appl Microbiol 52 : 47 54.
5. Beal EJ, House CH Orphan VJ (2009) Manganese- and iron-dependent marine methane oxidation. Science 325 : 184 187.
6. Beman JM, Popp BN Francis CA (2008) Molecular and biogeochemical evidence for ammonia oxidation by marine Crenarchaeota in the Gulf of California. ISME J 2 : 429 441.
7. Coolen MJ, Abbas B, van Bleijswijk J, Hopmans EC, Kuypers MM, Wakeham SG Sinninghe Damsté JS (2007) Putative ammonia-oxidizing Crenarchaeota in suboxic waters of the Black Sea: A basin-wide ecological study using 16S ribosomal and functional genes and membrane lipids. Environ Microbiol 9 : 1001 1016. (Pubitemid 46397097)
8. Dang H, Li J, Zhang X, Li T, Tian F Jin W (2009a) Diversity and spatial distribution of amoA-encoding archaea in the deep-sea sediments of the tropical West Pacific Continental Margin. J Appl Microbiol 106 : 1482 1493.
9. Dang HY Lovell CR (2000) Bacterial primary colonization and early succession on surfaces in marine waters as determined by amplified rRNA gene restriction analysis and sequence analysis of 16S rRNA genes. Appl Environ Microb 66 : 467 475.
10. Dang HY, Li TG, Chen MN Huang GQ (2008a) Cross-ocean distribution of Rhodobacterales bacteria as primary surface colonizers in temperate coastal marine waters. Appl Environ Microb 74 : 52 60.
11. Dang HY, Zhang XX, Sun J, Li TG, Zhang ZN Yang GP (2008b) Diversity and spatial distribution of sediment ammonia-oxidizing crenarchaeota in response to estuarine and environmental gradients in the Changjiang Estuary and East China Sea. Microbiology 154 : 2084 2095.
12. Dang HY, Luan XW, Zhao JY Li J (2009b) Diverse and novel nifH and nifH-like gene sequences in the deep-sea methane seep sediments of the Okhotsk Sea. Appl Environ Microb 75 : 2238 2245.
13. Dang HY, Wang CY, Li J, Li TG, Tian F, Jin W, Ding YS Zhang ZN (2009c) Diversity and distribution of sediment nirS-encoding bacterial assemblages in response to environmental gradients in the eutrophied Jiaozhou Bay, China. Microb Ecol 58 : 161 169.
14. Dekas AE, Poretsky RS Orphan VJ (2009) Deep-sea archaea fix and share nitrogen in methane-consuming microbial consortia. Science 326 : 422 426.
15. de la Torre JR, Walker CB, Ingalls AE, Könneke M Stahl DA (2008) Cultivation of a thermophilic ammonia oxidizing archaeon synthesizing crenarchaeol. Environ Microbiol 10 : 810 818. (Pubitemid 351160920)
16. DeLong EF (1992) Archaea in coastal marine environments. P Natl Acad Sci USA 89 : 5685 5689.
17. Erguder TH, Boon N, Wittebolle L, Marzorati M Verstraete W (2009) Environmental factors shaping the ecological niches of ammonia-oxidizing archaea. FEMS Microbiol Rev 33 : 855 869.
18. Felsenstein J (1989) PHYLIP- phylogeny inference package (Version 3.2). Cladistics 5 : 164 166.
19. Francis CA, Roberts KJ, Beman JM, Santoro AE Oakley BB (2005) Ubiquity and diversity of ammonia-oxidizing archaea in water columns and sediments of the ocean. P Natl Acad Sci USA 102 : 14683 14688.
20. Francis CA, Beman JM Kuypers MMM (2007) New processes and players in the nitrogen cycle: the microbial ecology of anaerobic and archaeal ammonia oxidation. ISME J 1 : 19 27.
21. Ginsburg GD, Soloviev VA, Cranston RE, Lorenson TD Kvenvolden KA (1993) Gas hydrates from the continental slope, offshore Sakhalin Island, Okhotsk Sea. Geo-Mar Lett 13 : 41 48.
22. Haeckel M, Boudreau BP Wallmann K (2007) Bubble-induced porewater mixing: A 3-D model for deep porewater irrigation. Geochim Cosmochim Acta 71 : 5135 5154. (Pubitemid 350002225)
23. Hallam SJ, Mincer TJ, Schleper C, Preston CM, Roberts K, Richardson PM DeLong EF (2006) Pathways of carbon assimilation and ammonia oxidation suggested by environmental genomic analyses of marine Crenarchaeota. PLoS Biol 4 : E95.
24. Hatzenpichler R, Lebedeva EV, Spieck E, Stoecker K, Richter A, Daims H Wagner M (2008) A moderately thermophilic ammonia-oxidizing crenarchaeote from a hot spring. P Natl Acad Sci USA 105 : 2134 2139. (Pubitemid 351439477)
25. Heijs SK, Haese RR, van der Wielen PW, Forney LJ van Elsas JD (2007) Use of 16S rRNA gene based clone libraries to assess microbial communities potentially involved in anaerobic methane oxidation in a Mediterranean cold seep. Microb Ecol 53 : 384 398.
26. Hubert C, Loy A, Nickel M et al 2009) A constant flux of diverse thermophilic bacteria into the cold Arctic seabed. Science 325 : 1541 1544.
27. Inagaki F, Takai K, Komatsu T, Kanamatsu T, Fujioka K Horikoshi K (2001) Archaeology of Archaea: geomicrobiological record of Pleistocene thermal events concealed in a deep-sea subseafloor environment. Extremophiles 5 : 385 392. (Pubitemid 33737388)
28. Inagaki F, Suzuki M, Takai K, Oida H, Sakamoto T, Aoki K, Nealson KH Horikoshi K (2003) Microbial communities associated with geological horizons in coastal subseafloor sediments from the Sea of Okhotsk. Appl Environ Microb 69 : 7224 7235. (Pubitemid 38585373)
29. Inagaki F, Nunoura T, Nakagawa S et al 2006) Biogeographical distribution and diversity of microbes in methane hydrate-bearing deep marine sediments on the Pacific Ocean Margin. P Natl Acad Sci USA 103 : 2815 2820. (Pubitemid 43306632)
30. Jackson CR Weeks AQ (2008) Influence of particle size on bacterial community structure in aquatic sediments as revealed by 16S rRNA gene sequence analysis. Appl Environ Microb 74 : 5237 5240.
31. Jørgensen BB Boetius A (2007) Feast and famine - microbial life in the deep-sea bed. Nat Rev Microbiol 5 : 770 781. (Pubitemid 47423765)
32. Jurgens G, Glöckner F, Amann R, Saano A, Montonen L, Likolammi M Münster U (2000) Identification of novel Archaea in bacterioplankton of a boreal forest lake by phylogenetic analysis and fluorescent in situ hybridization. FEMS Microbiol Ecol 34 : 45 56.
33. Kato S, Kobayashi C, Kakegawa T Yamagishi A (2009) Microbial communities in iron-silica-rich microbial mats at deep-sea hydrothermal fields of the Southern Mariana Trough. Environ Microbiol 11 : 2094 2111.
34. Kendall MM, Wardlaw GD, Tang CF, Bonin AS, Liu Y Valentine DL (2007) Diversity of Archaea in marine sediments from Skan Bay, Alaska, including cultivated methanogens, and description of Methanogenium boonei sp. nov. Appl Environ Microb 73 : 407 414. (Pubitemid 46147569)
35. Kennett JP, Cannariato KG, Hendy IL Behl RJ (2003) Methane Hydrates in Quaternary Climate Change: The Clathrate Gun Hypothesis. Special Publication 54. American Geophysical Union
36. Knittel K, Lösekann T, Boetius A, Kort R Amann R (2005) Diversity and distribution of methanotrophic archaea at cold seeps. Appl Environ Microb 71 : 467 479. (Pubitemid 40116303)
37. Könneke 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. (Pubitemid 41613550)
38. Lam P, Jensen MM, Lavik G, McGinnis DF, Muller B, Schubert CJ, Amann R, Thamdrup B Kuypers MM (2007) Linking crenarchaeal and bacterial nitrification to anammox in the Black Sea. P Natl Acad Sci USA 104 : 7104 7109. (Pubitemid 47186016)
39. Lam P, Lavik G, Jensen MM, van de Vossenberg J, Schmid M, Woebken D, Gutiérrez D, Amann R, Jetten MS Kuypers MM (2009) Revising the nitrogen cycle in the Peruvian oxygen minimum zone. P Natl Acad Sci USA 106 : 4752 4757.
40. Larkin MA, Blackshields G, Brown NP et al 2007) Clustal W and Clustal X version 2.0. Bioinformatics 23 : 2947 2948. (Pubitemid 350162903)
41. Levin LA (2005) Ecology of cold seep sediments: interactions of fauna with flow, chemistry and microbes. Oceanogr Mar Biol 43 : 1 46.
42. Lloyd KG, Lapham L Teske A (2006) An anaerobic methane-oxidizing community of ANME-1b archaea in hypersaline Gulf of Mexico sediments. Appl Environ Microb 72 : 7218 7230. (Pubitemid 44748436)
43. Lösekann T, Knittel K, Nadalig T, Fuchs B, Niemann H, Boetius A Amann R (2007) Diversity and abundance of aerobic and anaerobic methane oxidizers at the Haakon Mosby Mud Volcano, Barents Sea. Appl Environ Microb 73 : 3348 3362. (Pubitemid 46834988)
44. Lozupone CA, Hamady M, Kelley ST Knight R (2007) Quantitative and qualitative β diversity measures lead to different insights into factors that structure microbial communities. Appl Environ Microb 73 : 1576 1585. (Pubitemid 46417883)
45. Luan XW, Jin YK, Anatoly O Yue BJ (2008) Characteristics of shallow gas hydrate in Okhotsk Sea. Sci China Ser D 51 : 415 421.
46. Martens-Habbena W, Berube PM, Urakawa H, de la Torre JR Stahl DA (2009) Ammonia oxidation kinetics determine niche separation of nitrifying Archaea and Bacteria. Nature 461 : 976 979.
47. Meyerdierks A, Kube M, Lombardot T, Knittel K, Bauer M, Glöckner FO, Reinhardt R Amann R (2005) Insights into the genomes of archaea mediating the anaerobic oxidation of methane. Environ Microbiol 7 : 1937 1951. (Pubitemid 41752383)
48. Miyazaki J, Higa R, Toki T, Ashi J, Tsunogai U, Nunoura T, Imachi H Takai K (2009) Molecular characterization of potential nitrogen fixation by anaerobic methane-oxidizing archaea in the methane seep sediments at the number 8 Kumano Knoll in the Kumano Basin, offshore of Japan. Appl Environ Microb 75 : 7153 7162.
49. Moissl C, Rudolph C, Rachel R, Koch M Huber R (2003) In situ growth of the novel SM1 euryarchaeon from a string-of-pearls-like microbial community in its cold biotope, its physical separation and insights into its structure and physiology. Arch Microbiol 180 : 211 217. (Pubitemid 37102719)
50. Naehr TH, Eichhubl P, Orphan VJ, Hovland M, Paull CK, Ussler III W, Lorenson TD Greene HG (2007) Authigenic carbonate formation at hydrocarbon seeps in continental margin sediments: A comparative study. Deep-Sea Res Pt II 54 : 1268 1291. (Pubitemid 47238619)
51. Nakagawa T, Mori K, Kato C, Takahashi R Tokuyama T (2007) Distribution of cold-adapted ammonia-oxidizing microorganisms in the deep-ocean of the northeastern Japan Sea. Microbes Environ 22 : 365 372.
52. Obzhirov A, Shakirov R, Salyuk A, Suess E, Biebow M Salomatin A (2004) Relations between methane venting, geological structure and seismo-tectonics in the Okhotsk Sea. Geo-Mar Lett 24 : 135 139. (Pubitemid 39000889)
53. Orphan VJ, Hinrichs KU, Ussler W III., Paull CK, Taylor LT, Sylva SP, Hayes JM Delong EF (2001) Comparative analysis of methane-oxidizing archaea and sulfate-reducing bacteria in anoxic marine sediments. Appl Environ Microb 67 : 1922 1934. (Pubitemid 33644967)
54. Ouverney CC Fuhrman JA (2000) Marine planktonic archaea take up amino acids. Appl Environ Microb 66 : 4829 4833.
55. Park SJ, Park BJ Rhee SK (2008) Comparative analysis of archaeal 16S rRNA and amoA genes to estimate the abundance and diversity of ammonia-oxidizing archaea in marine sediments. Extremophiles 12 : 605 615.
56. Pernthaler A, Dekas AE, Brown CT, Goffredi SK, Embaye T Orphan VJ (2008) Diverse syntrophic partnerships from deep-sea methane vents revealed by direct cell capture and metagenomics. P Natl Acad Sci USA 105 : 7052 7057. (Pubitemid 351754528)
57. Poret-Peterson AT, Graham JE, Gulledge J Klotz MG (2008) Transcription of nitrification genes by the methane-oxidizing bacterium, Methylococcus capsulatus strain Bath. ISME J 2 : 1213 1220.
58. Prosser JI Nicol GW (2008) Relative contributions of archaea and bacteria to aerobic ammonia oxidation in the environment. Environ Microbiol 10 : 2931 2941.
59. Reeburgh WS (2007) Oceanic methane biogeochemistry. Chem Rev 107 : 486 513.
60. Sahling H, Galkin SV, Salyuk A, Greinert J, Foerstel H, Piepenburg D Suess E (2003) Depth-related structure and ecological significance of cold-seep communities - a case study from the Sea of Okhotsk. Deep-Sea Res Pt I 50 : 1391 1409. (Pubitemid 37537869)
61. Schleper C, Jurgens G Jonuscheit M (2005) Genomic studies of uncultivated archaea. Nat Rev Microbiol 3 : 479 488. (Pubitemid 40716174)
62. Schloss PD Handelsman J (2005) Introducing DOTUR, a computer program for defining operational taxonomic units and estimating species richness. Appl Environ Microb 71 : 1501 1506. (Pubitemid 40396689)
63. Schmidt I (2009) Chemoorganoheterotrophic growth of Nitrosomonas europaea and Nitrosomonas eutropha. Curr Microbiol 59 : 130 138.
64. Shinkai T Kobayashi Y (2007) Localization of ruminal cellulolytic bacteria on plant fibrous materials as determined by fluorescence in situ hybridization and real-time PCR. Appl Environ Microb 73 : 1646 1652. (Pubitemid 46417891)
65. Stephen JR, Chang YJ, Macnaughton SJ, Kowalchuk GA, Leung KT, Flemming CA White DC (1999) Effect of toxic metals on indigenous soil β-subgroup proteobacterium ammonia oxidizer community structure and protection against toxicity by inoculated metal-resistant bacteria. Appl Environ Microb 65 : 95 101.
66. Teira E, van Aken H, Veth C Herndl GJ (2006) Archaeal uptake of enantiomeric amino acids in the meso- and bathypelagic waters of the North Atlantic. Limnol Oceanogr 51 : 60 69. (Pubitemid 43259693)
67. Urakawa H, Tajima Y, Numata Y Tsuneda S (2008) Low temperature decreases the phylogenetic diversity of ammonia-oxidizing archaea and bacteria in aquarium biofiltration systems. Appl Environ Microb 74 : 894 900. (Pubitemid 351225745)
68. Vetriani C, Tran HV Kerkhof LJ (2003) Fingerprinting microbial assemblages from the oxic/anoxic chemocline of the Black Sea. Appl Environ Microb 69 : 6481 6488. (Pubitemid 37420180)
69. Wallmann K, Aloisi G, Haeckel M, Obzhirov A, Pavlova G Tishchenko P (2006) Kinetics of organic matter degradation, microbial methane generation, and gas hydrate formation in anoxic marine sediments. Geochim Cosmochim Acta 70 : 3905 3927. (Pubitemid 44111664)
70. You J, Das A, Dolan EM Hu Z (2009) Ammonia-oxidizing archaea involved in nitrogen removal. Water Res 43 : 1801 1809.
71. Zhang CL Lanoil B (2004) Geomicrobiology and biogeochemistry of gas hydrates and cold seeps. Chem Geol 205 : 187 194.
72. Zhang CL, Ye Q, Huang Z et al 2008) Global occurrence of archaeal amoA genes in terrestrial hot springs. Appl Environ Microb 74 : 6417 6426.