Deep-sea methane seep sediments in the Okhotsk Sea sustain diverse and abundant anammox bacteria

FEMS Microbiology Ecology

Volumn 87, Issue 2, 2014, Pages 503-516

  Shao, Sudong ^a,b,c   Luan, Xiwu ^d,e   Dang, Hongyue ^a,c   Zhou, Haixia ^c   Zhao, Yakun ^c   Liu, Haitao ^c   Zhang, Yunbo ^c   Dai, Lingqing ^a,b,c   Ye, Ying ^b   Klotz, Martin G ^a,c,f  

^a XIAMEN UNIVERSITY   (China)

^b ZHEJIANG UNIVERSITY   (China)

^c CHINA UNIVERSITY OF PETROLEUM   (China)

^d Chongqing Institute of Geology and Mineral Resources   (China)

^e QINGDAO INSTITUTE OF MARINE GEOLOGY   (China)

^f UNIVERSITY OF NORTH CAROLINA AT CHARLOTTE   (United States)

Author keywords

Anammox; Candidatus Scalindua; Cold seep; Hydrazine oxidoreductase gene hzo; Methane hydrate; Okhotsk Sea

Indexed keywords

AMMONIUM DERIVATIVE; METHANE; NITRIC ACID DERIVATIVE; NITRITE; OXIDOREDUCTASE; RNA 16S;

ANAMMOX; ARTICLE; BACTERIAL GENE; BACTERIUM; BIODIVERSITY; CANDIDATUS SCALINDUA; CHEMISTRY; CLASSIFICATION; COLD SEEP; GENETICS; HYDRAZINE OXIDOREDUCTASE GENE HZO; METHANE HYDRATE; MICROBIOLOGY; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; OKHOTSK SEA; PHYLOGENY; RNA GENE; SEA; SEDIMENT;

ANAMMOX; CANDIDATUS SCALINDUA; COLD SEEP; HYDRAZINE OXIDOREDUCTASE GENE HZO; METHANE HYDRATE; OKHOTSK SEA;

AMMONIUM COMPOUNDS; BACTERIA; BASE SEQUENCE; BIODIVERSITY; GENES, BACTERIAL; GENES, RRNA; GEOLOGIC SEDIMENTS; METHANE; MOLECULAR SEQUENCE DATA; NITRATES; NITRITES; OCEANS AND SEAS; OXIDOREDUCTASES; PHYLOGENY; RNA, RIBOSOMAL, 16S; WATER MICROBIOLOGY;

EID: 84895077467     PISSN: 01686496     EISSN: 15746941     Source Type: Journal    
DOI: 10.1111/1574-6941.12241     Document Type: Article

References (73)

1. Altschul SF, Madden TL, Schäffer 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.
2. Amano T, Yoshinaga I, Okada K, Yamagishi T, Ueda S, Obuchi A, Sako Y & Suwa Y ( 2007) Detection of anammox activity and diversity of anammox bacteria-related 16S rRNA genes in coastal marine sediments in Japan. Microbes Environ 22: 232-242.
3. Amano T, Yoshinaga I, Yamagishi T, Thuoc CV, Thu PT, Ueda S, Kato K, Sako Y & Suwa Y (2011) Contribution of anammox bacteria to benthic nitrogen cycling in a mangrove forest and shrimp ponds, Haiphong, Vietnam. Microbes Environ 26: 1-6.
4. Ashelford KE, Chuzhanova NA, Fry JC, Jones AJ & Weightman AJ (2005) At least 1 in 20 16S rRNA sequence records currently held in public repositories is estimated to contain substantial anomalies. Appl Environ Microbiol 71: 7724-7736.
5. Bowles M & Joye S (2011) High rates of denitrification and nitrate removal in cold seep sediments. ISME J 5: 565-567.
6. Clark AG & Whittam TS (1992) Sequencing errors and molecular evolutionary analysis. Mol Biol Evol 9: 744-752.
7. 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. Nucleic Acids Res 31: 442-443.
8. Dale OR, Tobias CR & Song B (2009) Biogeographical distribution of diverse anaerobic ammonium oxidizing (anammox) bacteria in Cape Fear River Estuary. Environ Microbiol 11: 1194-1207.
9. Dalsgaard T, Thamdrup B & Canfield DE (2005) Anaerobic ammonium oxidation (anammox) in the marine environment. Res Microbiol 156: 457-464.
10. 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 Microbiol 66: 467-475.
11. 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 Microbiol 74: 52-60.
12. 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.
13. Dang HY, Luan XW, Zhao JY & Li J (2009) Diverse and novel nifH and nifH-like gene sequences in the deep-sea methane seep sediments of the Okhotsk Sea. Appl Environ Microbiol 75: 2238-2245.
14. Dang HY, Chen RP, Wang L, Guo LZ, Chen PP, Tang ZW, Tian F, Li SZ & Klotz MG (2010a) Environmental factors shape sediment anammox bacterial communities in hypernutrified Jiaozhou Bay, China. Appl Environ Microbiol 76: 7036-7047.
15. Dang HY, Luan XW, Chen RP, Zhang XX, Guo LZ & Klotz MG (2010b) Diversity, abundance and distribution of amoA-encoding archaea in deep-sea methane seep sediments of the Okhotsk Sea. FEMS Microbiol Ecol 72: 370-385.
16. Dang HY, Zhou HX, Zhang ZN, Yu ZS, Hua E, Liu XS & Jiao NZ (2013) Molecular detection of Candidatus Scalindua pacifica and environmental responses of sediment anammox bacterial community in the Bohai Sea, China. PLoS One 8: e61330.
17. Dekas AE, Poretsky RS & Orphan VJ (2009) Deep-sea archaea fix and share nitrogen in methane-consuming microbial consortia. Science 326: 422-426.
18. Eckert KA & Kunkel TA (1991) DNA polymerase fidelity and the polymerase chain reaction. PCR Methods Appl 1: 17-24.
19. Engström P, Penton CR & Devol AH (2009) Anaerobic ammonium oxidation in deep-sea sediments off the Washington margin. Limnol Oceanogr 54: 1643-1652.
20. Felsenstein J (1989) phylip - phylogeny inference package (Version 3.2). Cladistics 5: 164-166.
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. Glud RN, Thamdrup B, Stahl H, Wenzhoefer F, Glud A, Nomaki H, Oguri K, Revsbech NP & Kitazatoe H (2009) Nitrogen cycling in a deep ocean margin sediment (Sagami Bay, Japan). Limnol Oceanogr 54: 723-734.
23. Hamady M, Lozupone C & Knight R (2010) fast unifrac: facilitating high-throughput phylogenetic analyses of microbial communities including analysis of pyrosequencing and phylochip data. ISME J 4: 17-27.
24. Harhangi HR, Le Roy M, van Alen T, Hu BL, Groen J, Kartal B, Tringe SG, Quan ZX, Jetten MS & Op den Camp HJ (2012) Hydrazine synthase, a unique phylomarker with which to study the presence and biodiversity of anammox bacteria. Appl Environ Microbiol 78: 752-758.
25. Hirsch MD, Long ZT & Song B (2011) Anammox bacterial diversity in various aquatic ecosystems based on the detection of hydrazine oxidase genes (hzoA/hzoB). Microb Ecol 61: 264-276.
26. Hong YG, Li M, Cao HL & Gu JD (2011a) Residence of habitat-specific anammox bacteria in the deep-sea subsurface sediments of the South China Sea: analyses of marker gene abundance with physical chemical parameters. Microb Ecol 62: 36-47.
27. Hong YG, Yin B & Zheng TL (2011b) Diversity and abundance of anammox bacterial community in the deep-ocean surface sediment from equatorial Pacific. Appl Microbiol Biotechnol 89: 1233-1241.
28. Hu BL, Shen LD, Xu XY & Zheng P (2011) Anaerobic ammonium oxidation (anammox) in different natural ecosystems. Biochem Soc Trans 39: 1811-1816.
29. Huber T, Faulkner G & Hugenholtz P (2004) Bellerophon: a program to detect chimeric sequences in multiple sequence alignments. Bioinformatics 20: 2317-2319.
30. Hulth S, Aller RC, Canfield DE, Dalsgaard T, Engström P, Gilbert F, Sundback K & Thamdrup B (2005) Nitrogen removal in marine environments: recent findings and future research challenges. Mar Chem 94: 125-145.
31. Jaeschke A, Abbas B, Zabel M, Hopmans EC, Schouten S & Sinninghe Damsté JS (2010) Molecular evidence for anaerobic ammonium-oxidizing (anammox) bacteria in continental shelf and slope sediments off northwest Africa. Limnol Oceanogr 55: 365-376.
32. Jensen MM, Lam P, Revsbech NP, Nagel B, Gaye B, Jetten MS & Kuypers MM (2011) Intensive nitrogen loss over the Omani Shelf due to anammox coupled with dissimilatory nitrite reduction to ammonium. ISME J 5: 1660-1670.
33. Jetten MSM, van Niftrik L, Strous M, Kartal B, Keltjens JT & Op den Camp HJM (2009) Biochemistry and molecular biology of anammox bacteria. Crit Rev Biochem Mol Biol 44: 65-84.
34. Jørgensen BB & Boetius A (2007) Feast and famine - microbial life in the deep-sea bed. Nat Rev Microbiol 5: 770-781.
35. Kalvelage T, Jensen MM, Contreras S, Revsbech NP, Lam P, Günter M, LaRoche J, Lavik G & Kuypers MM (2011) Oxygen sensitivity of anammox and coupled N-cycle processes in oxygen minimum zones. PLoS One 6: e29299.
36. Klotz MG & Stein LY (2011) Genomics of ammonia-oxidizing bacteria and insights to their evolution. Nitrification (Ward BB, Arp DJ, & Klotz MG, eds), pp. 57-93. ASM Press, Washington, D.C.
37. Kuenen JG (2008) Anammox bacteria: from discovery to application. Nat Rev Microbiol 6: 320-326.
38. Kwiatowski J, Skarecky D, Hernandez S, Pham D, Quijas F & Ayala FJ (1991) High fidelity of the polymerase chain reaction. Mol Biol Evol 8: 884-887.
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.
41. Lee JI, Kim YJ, Bae H, Cho SS, Lee JH & Kwon ST (2010) Biochemical properties and PCR performance of a family B DNA polymerase from hyperthermophilic Euryarchaeon Thermococcus peptonophilus. Appl Biochem Biotechnol 160: 1585-1599.
42. Li M, Hong YG, Klotz MG & Gu JD (2010) A comparison of primer sets for detecting 16S rRNA and hydrazine oxidoreductase genes of anaerobic ammonium-oxidizing bacteria in marine sediments. Appl Microbiol Biotechnol 86: 781-790.
43. Li M, Cao HL, Hong YG & Gu JD (2011) Seasonal dynamics of anammox bacteria in estuarial sediment of the Mai Po Nature Reserve revealed by analyzing the 16S rRNA and hydrazine oxidoreductase (hzo) genes. Microbes Environ 26: 15-22.
44. Luan XW, Jin YK, Anatoly O & Yue BJ (2008) Characteristics of shallow gas hydrate in Okhotsk Sea. Sci China Ser D Earth Sci 51: 415-421.
45. Meyer RL, Risgaard-Petersen N & Allen DE (2005) Correlation between anammox activity and microscale distribution of nitrite in a subtropical mangrove sediment. Appl Environ Microbiol 71: 6142-6149.
46. 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 Microbiol 75: 7153-7162.
47. Mullins TD, Britschgi TB, Krest RL & Giovannoni SJ (1995) Genetic comparisons reveal the same unknown bacterial lineages in Atlantic and Pacific bacterioplankton communities. Limnol Oceanogr 40: 148-158.
48. Nicholls JC & Trimmer M (2009) Widespread occurrence of the anammox reaction in estuarine sediments. Aquat Microb Ecol 55: 105-113.
49. Penton CR, Devol AH & Tiedje JM (2006) Molecular evidence for the broad distribution of anaerobic ammonium-oxidizing bacteria in freshwater and marine sediments. Appl Environ Microbiol 72: 6829-6832.
50. 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.
51. Reeburgh WS (2007) Oceanic methane biogeochemistry. Chem Rev 107: 486-513.
52. Rysgaard S, Glud RN, Risgaard-Petersen N & Dalsgaard T (2004) Denitrification and anammox activity in Arctic marine sediments. Limnol Oceanogr 49: 1493-1502.
53. 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 Part 1 Oceanogr Res Pap 50: 1391-1409.
54. 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.
55. Schmid M, Walsh K, Webb R et al. (2003) Candidatus 'Scalindua brodae', sp. nov., Candidatus 'Scalindua wagneri', sp. nov., two new species of anaerobic ammonium oxidizing bacteria. Syst Appl Microbiol 26: 529-538.
56. Schmid MC, Hooper AB, Klotz MG, Woebken D, Lam P, Kuypers MMM, Pommerening-Roeser A & op den Camp HJM & Jetten MSM (2008) Environmental detection of octahaem cytochrome c hydroxylamine/hydrazine oxidoreductase genes of aerobic and anaerobic ammonium-oxidizing bacteria. Environ Microbiol 10: 3140-3149.
57. Shimamura M, Nishiyama T, Shigetomo H, Toyomoto T, Kawahara Y, Furukawa K & Fujii T (2007) Isolation of a multiheme protein with features of a hydrazine-oxidizing enzyme from an anaerobic ammonium-oxidizing enrichment culture. Appl Environ Microbiol 73: 1065-1072.
58. Shu QL & Jiao NZ (2008) Profiling Planctomycetales diversity with reference to anammox-related bacteria in a South China Sea, deep-sea sediment. Mar Ecol 29: 413-420.
59. Sokoll S, Holtappels M, Lam P, Collins G, Schlüter M, Lavik G & Kuypers MM (2012) Benthic nitrogen loss in the Arabian Sea off Pakistan. Front Microbiol 3: 395.
60. Strous M & Jetten MSM (2004) Anaerobic oxidation of methane and ammonium. Annu Rev Microbiol 58: 99-117.
61. Strous M, Fuerst JA, Kramer EH, Logemann S, Muyzer G, van de Pas-Schoonen KT, Webb R, Kuenen JG & Jetten MS (1999) Missing lithotroph identified as new planctomycete. Nature 400: 446-449.
62. Strous M, Pelletier E, Mangenot S et al. (2006) Deciphering the evolution and metabolism of an anammox bacterium from a community genome. Nature 440: 790-794.
63. ter Braak CJF & Šmilauer P (2002) canoco Reference Manual and CanoDraw for Windows user's Guide: Software for Canonical Community Ordination (Version 4.5). Ithaca, NY: Microcomputer Power.
64. Tindall KR & Kunkel TA (1988) Fidelity of DNA synthesis by the Thermus aquaticus DNA polymerase. Biochemistry 27: 6008-6013.
65. Trimmer M & Nicholls JC (2009) Production of nitrogen gas via anammox and denitrification in intact sediment cores along a continental shelf to slope transect in the North Atlantic. Limnol Oceanogr 54: 577-589.
66. Trimmer M, Nicholls JC, Morley N, Davies CA & Aldridge J (2005) Biphasic behavior of anammox regulated by nitrite and nitrate in an estuarine sediment. Appl Environ Microbiol 71: 1923-1930.
67. Trimmer M, Engström P & Thamdrup B (2013) Stark contrast in denitrification and anammox across the deep Norwegian Trench: The Skagerrak. Appl Environ Microbiol 79: 7381-7389.
68. van de Vossenberg J, Woebken D, Maalcke WJ et al. (2013) The metagenome of the marine anammox bacterium 'Candidatus Scalindua profunda' illustrates the versatility of this globally important nitrogen cycle bacterium. Environ Microbiol 15: 1275-1289.
69. van Niftrik L & Jetten MS (2012) Anaerobic ammonium-oxidizing bacteria: unique microorganisms with exceptional properties. Microbiol Mol Biol Rev 76: 585-596.
70. Vanreusel A, Andersen AC, Boetius A et al. (2009) Biodiversity of cold seep ecosystems along the European margins. Oceanography 22: 110-127.
71. Woebken D, Fuchs BM, Kuypers MM & Amann R (2007) Potential interactions of particle-associated anammox bacteria with bacterial and archaeal partners in the Namibian upwelling system. Appl Environ Microbiol 73: 4648-4657.
72. Woebken D, Lam P, Kuypers MMM, Naqvi SW, Kartal B, Strous M, Jetten MS, Fuchs BM & Amann R (2008) A microdiversity study of anammox bacteria reveals a novel Candidatus Scalindua phylotype in marine oxygen minimum zones. Environ Microbiol 10: 3106-3119.
73. Yan J, Op den Camp HJ, Jetten MS, Hu YY & Haaijer SC (2010) Induced cooperation between marine nitrifiers and anaerobic ammonium-oxidizing bacteria by incremental exposure to oxygen. Syst Appl Microbiol 33: 407-415.