Environment-dependent distribution of the sediment nifH-harboring microbiota in the northern South China Sea

Applied and Environmental Microbiology

Volumn 79, Issue 1, 2013, Pages 121-132

  Dang, Hongyue ^a,b   Yang, Jinying ^a   Li, Jing ^a   Luan, Xiwu ^c,d   Zhang, Yunbo ^a   Gu, Guizhou ^a   Xue, Rongrong ^a   Zong, Mingyue ^a   Klotz, Martin G ^a,e  

^a CHINA UNIVERSITY OF PETROLEUM   (China)

^b XIAMEN UNIVERSITY   (China)

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

^d QINGDAO INSTITUTE OF MARINE GEOLOGY   (China)

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

Author keywords

[No Author keywords available]

Indexed keywords

ARCHAEAL; COMMUNITY STRUCTURES; DIAGNOSTIC TOOLS; ENVIRONMENTAL FACTORS; IN-SITU TEMPERATURE; MARGINAL SEAS; METHANE HYDRATES; METHANE SEEP; MICROBIAL ASSEMBLAGE; MICROBIOTAS; NORTHERN SOUTH CHINA SEA; OLIGOTROPHIC WATERS; POSITIVE CORRELATIONS; SAMPLING SITE; SEDIMENT ORGANIC CARBON; SEDIMENT PORE WATER; SOUTH CHINA SEA; WESTERN PACIFIC;

GAS HYDRATES; GENES; HYDRATION; METHANE; NITROGEN FIXATION; PETROLEUM RESERVOIR EVALUATION; PHOSPHORUS; SEDIMENTS; SOCIAL SCIENCES; SPATIAL DISTRIBUTION; WATER;

SEDIMENTOLOGY;

NITROGENASE REDUCTASE; OXIDOREDUCTASE;

BIOMARKER; COMMUNITY STRUCTURE; CONCENTRATION (COMPOSITION); GENE; HYDRATION; MARGINAL SEA; MARINE SEDIMENT; MICROORGANISM; NITROGEN FIXATION; OLIGOTROPHIC ENVIRONMENT; POREWATER; SAMPLING; STATISTICAL ANALYSIS;

ARTICLE; BIOTA; CHINA; DNA SEQUENCE; GENETIC VARIABILITY; GENETICS; METAGENOME; MICROBIOLOGY; MOLECULAR GENETICS; NITROGEN FIXATION; NUCLEOTIDE SEQUENCE; PHYLOGEOGRAPHY; SEDIMENT; TEMPERATURE;

BIOTA; CHINA; GENETIC VARIATION; GEOLOGIC SEDIMENTS; METAGENOME; MOLECULAR SEQUENCE DATA; NITROGEN FIXATION; OXIDOREDUCTASES; PHYLOGEOGRAPHY; SEQUENCE ANALYSIS, DNA; TEMPERATURE;

PACIFIC OCEAN; SOUTH CHINA SEA;

ARCHAEA;

EID: 84871957817     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.01889-12     Document Type: Article

References (75)

1. Zehr JP, Jenkins BD, Short SM, Steward GF. 2003. Nitrogenase gene diversity and microbial community structure: a cross-system comparison. Environ. Microbiol. 5:539-554.
2. Ward BB, Capone DG, Zehr JP. 2007. What's new in the nitrogen cycle?. Oceanography 20:101-109.
3. -1 versus the concept of homeostasis in the fixed-nitrogen inventory. Biogeosciences 4:233-253.
4. Fulweiler RW. 2009. Fantastic fixers. Science 326:377-378.
5. Bonnet S, Biegala IC, Dutrieux P, Slemons LO, Capone DG. 2009. Nitrogen fixation in the western equatorial Pacific: rates, diazotrophic cyanobacterial size class distribution, and biogeochemical significance. Global Biogeochem. Cycles 23:GB3012.
6. Grosse J, Bombar D, Doan HN, Nguyen LN, Voss M. 2010. The Mekong River plume fuels nitrogen fixation and determines phytoplankton species distribution in the South China Sea during low- and high-discharge season. Limnol. Oceanogr. 55:1668-1680.
7. 2 fixation domain. Science 327:1512-1514.
8. Fernandez C, Farías L, Ulloa O. 2011. Nitrogen fixation in denitrified marine waters. PLoS One 6:e20539. doi:10.1371/journal.pone.0020539.
9. Raymond J, Siefert JL, Staples CR, Blankenship RE. 2004. The natural history of nitrogen fixation. Mol. Biol. Evol. 21:541-554.
10. Zehr JP, Capone DG. 1996. Problems and promises of assaying the genetic potential for nitrogen fixation in the marine environment. Microb. Ecol. 32:263-281.
11. Lovell CR. 2002. Plant-microbe interactions in the marine environment, p 2539-2554. In Bitton G (ed), Encyclopedia of environmental microbiology, vol 5. Wiley, New York, NY.
12. Mehta MP, Butterfield DA, Baross JA. 2003. Phylogenetic diversity of nitrogenase (nifH) genes in deep-sea and hydrothermal vent environments of the Juan de Fuca Ridge. Appl. Environ. Microbiol. 69:960-970.
13. Mehta MP, Huber JA, Baross JA. 2005. Incidence of novel and potentially archaeal nitrogenase genes in the deep Northeast Pacific Ocean. Environ. Microbiol. 7:1525-1534.
14. 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. Proc. Natl. Acad. Sci. U. S. A. 105:7052-7057.
15. 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.
16. Dekas AE, Poretsky RS, Orphan VJ. 2009. Deep-sea archaea fix and share nitrogen in methane-consuming microbial consortia. Science 326:422-426.
17. 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.
18. Gaby JC, Buckley DH. 2011. A global census of nitrogenase diversity. Environ. Microbiol. 13:1790-1799.
19. Whitman WB, Coleman DC, Wiebe WJ. 1998. Prokaryotes: the unseen majority. Proc. Natl. Acad. Sci. U. S. A. 95:6578-6583.
20. Zehr JP, Kudela RM. 2011. Nitrogen cycle of the open ocean: from genes to ecosystems. Annu. Rev. Mar. Sci. 3:197-225.
21. Zehr JP, Mellon M, Braun S, Litaker W. 1995. Diversity of heterotrophic nitrogen fixation genes in a marine cyanobacterial mat. Appl. Environ. Microbiol. 61:2527-2532.
22. Burns JA, Zehr JP, Capone DG. 2002. Nitrogen-fixing phylotypes of Chesapeake Bay and Neuse River estuary sediments. Microb. Ecol. 44: 336-343.
23. Flores-Mireles AL, Winans SC, Holguin G. 2007. Molecular characterization of diazotrophic and denitrifying bacteria associated with mangrove roots. Appl. Environ. Microbiol. 73:7308-7321.
24. Charpy L, Palinska KA, Casareto B, Langlade MJ, Suzuki Y, Abed RM, Golubic S. 2010. Dinitrogen-fixing cyanobacteria in microbial mats of two shallow coral reef ecosystems. Microb. Ecol. 59:174-186.
25. Gamble MD, Bagwell CE, Larocque J, Bergholz PW, Lovell CR. 2010. Seasonal variability of diazotroph assemblages associated with the rhizosphere of the salt marsh cordgrass, Spartina alterniflora. Microb. Ecol. 59:253-265.
26. Severin I, Acinas SG, Stal LJ. 2010. Diversity of nitrogen-fixing bacteria in cyanobacterial mats. FEMS Microbiol. Ecol. 73:514-525.
27. Walsh JJ. 1991. Importance of continental margins in the marine biogeochemical cycling of carbon and nitrogen. Nature 350:53-55.
28. Bauer JE, Druffel ERM. 1998. Ocean margins as a significant source of organic matter to the deep open ocean. Nature 392:482-485.
29. Subramaniam A, Yager PL, Carpenter EJ, Mahaffey C, Björkman K, Cooley S, Kustka AB, Montoya JP, Sañudo-Wilhelmy SA, Shipe R, Capone DG. 2008. Amazon River enhances diazotrophy and carbon sequestration in the tropical North Atlantic Ocean. Proc. Natl. Acad. Sci. U. S. A. 105:10460-10465.
30. Capone DG, Burns JA, Michaels AF, Montoya JP, Subramaniam A, Carpenter EJ. 2005. Nitrogen fixation by Trichodesmium spp.: an important source of new nitrogen to the tropical and sub-tropical North Atlantic Ocean. Global Biogeochem. Cycles 19:GB2024.
31. Sohm JA, Webb EA, Capone DG. 2011. Emerging patterns of marine nitrogen fixation. Nat. Rev. Microbiol. 9:499-508.
32. Knittel K, Boetius A. 2009. Anaerobic oxidation of methane: progress with an unknown process. Annu. Rev. Microbiol. 63:311-334.
33. Hester KC, Brewer PG. 2009. Clathrate hydrates in nature. Annu. Rev. Mar. Sci. 1:303-327.
34. Moisander PH, Beinart RA, Voss M, Zehr JP. 2008. Diversity and abundance of diazotrophic microorganisms in the South China Sea during intermonsoon. ISME J. 2:954-967.
35. Wu J, Chung SW, Wen LS, Liu KK, Chen YL, Chen H, Karl DM. 2003. Dissolved inorganic phosphorus, dissolved iron, and Trichodesmium in the oligotrophic South China Sea. Global Biogeochem. Cycles 17:1008.
36. Yin KD, Qian Wu P-YMCS, Chen JC, Huang LM, Song XY, Jian WJ. 2001. Shift from P to N limitation of phytoplankton growth across the Pearl River estuarine plume during summer. Mar. Ecol. Prog. Ser. 221:17-28.
37. Chen YL, Chen H, Karl DM, Takahashi M. 2004. Nitrogen modulates phytoplankton growth in spring in the South China Sea. Cont. Shelf Res. 24:527-541.
38. Zhang Y, Zhao ZH, Sun J, Jiao NZ. 2011. Diversity and distribution of diazotrophic communities in the South China Sea deep basin with mesoscale cyclonic eddy perturbations. FEMS Microbiol. Ecol. 78:417-427.
39. Chou W, Chen YL, Sheu DD, Shih Y, Han C, Cho CL, Tseng C, Yang Y. 2006. Estimated net community production during the summertime at the SEATS time-series study site, northern South China Sea: implications for nitrogen fixation. Geophys. Res. Lett. 33:L22610.
40. Voss M, Bombar D, Natalie L, Dippner JW. 2006. Riverine influence on nitrogen fixation in the upwelling region off Vietnam, South China Sea. Geophys. Res. Lett. 33:L07604.
41. 2 fixation and nitrate uptake in the upstream Kuroshio and South China Sea basin. Limnol. Oceanogr. 53: 1705-1721.
42. Bombar D, Moisander PH, Dippner JW, Foster RA, Voss M, Karfeld B, Zehr JP. 2011. Distribution of diazotrophic microorganisms and nifH gene expression in the Mekong River plume during intermonsoon. Mar. Ecol. Prog. Ser. 424:39-52.
43. Zhu YH, Wu BH, Lu ZQ. 2001. The prospecting for gas hydrate offshore China. Mineral Deposits 20:174-180. (In Chinese with English abstract.)
44. Chen DF, Huang YY, Yuan XL, Cathles LM III. 2005. Seep carbonates and preserved methane oxidizing archaea and sulfate reducing bacteria fossils suggest recent gas venting on the seafloor in the northeastern South China Sea. Mar. Petrol. Geol. 22:613-621.
45. Han XQ, Suess E, Huang YY, Wu NY, Bohrmann G, Su X, Eisenhauer A, Rehder G, Fang YX. 2008. Jiulong methane reef: microbial mediation of seep carbonates in the South China Sea. Mar. Geol. 249:243-256.
46. Wu NY, Zhang HQ, Yang SX, Zhang GX, Liang JQ, Lu JA, Su X, Schultheiss P, Holland M, Zhu YH. 2011. Gas hydrate system of Shenhu area, northern South China Sea: geochemical results. J. Geol. Res. 2011: 370298.
47. Zhou MY, Chen XL, Zhao HL, Dang HY, Luan XW, Zhang XY, He HL, Zhou BC, Zhang YZ. 2009. Diversity of both the cultivable proteaseproducing bacteria and their extracellular proteases in the sediments of the South China Sea. Microb. Ecol. 58:582-590.
48. Danovaro R. 2009. Methods for the study of deep-sea sediments, their functioning, and biodiversity. CRC Press, Boca Raton, FL.
49. Grasshoff K, Kremling K, Ehrhardt M. 1999. Methods of seawater analysis. Wiley-Verlag Chemie, Weinheim, Germany.
50. Dang HY, Zhang XX, Sun J, Li TG, Zhang ZN, Yang GP. 2008. 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.
51. Dang HY, Li TG, Chen MN, Huang GQ. 2008. Cross-ocean distribution of Rhodobacterales bacteria as primary surface colonizers in temperate coastal marine waters. Appl. Environ. Microbiol. 74:52-60.
52. 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.
53. 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.
54. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG. 2007. CLUSTALWand CLUSTAL X version 2.0. Bioinformatics 23:2947-2948.
55. Felsenstein J. 1989. PHYLIP: phylogeny inference package (version 3.2). Cladistics 5:164-166.
56. Dang HY, Luan XW, Chen RP, Zhang XX, Guo LZ, Klotz MG. 2010. Diversity, abundance and distribution of amoA-encoding archaea in deep-sea methane seep sediments of the Okhotsk Sea. FEMS Microbiol. Ecol. 72:370-385.
57. Dang HY, Chen RP, Wang L, Guo LZ, Chen PP, Tang ZW, Tian F, Li SZ, Klotz MG. 2010. Environmental factors shape sediment anammox bacterial communities in hypernutrified Jiaozhou Bay, China. Appl. Environ. Microbiol. 76:7036-7047.
58. 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.
59. 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.
60. Eiler A, Beier S, Säwström C, Karlsson J, Bertilsson S. 2009. High ratio of bacteriochlorophyll biosynthesis genes to chlorophyll biosynthesis genes in bacteria of humic lakes. Appl. Environ. Microbiol. 75:7221-7228.
61. Galagan JE, Nusbaum C, Roy A, Endrizzi MG, Macdonald P, FitzHugh W, Calvo S, Engels R, Smirnov S, Atnoor D, Brown A, Allen N, Naylor J, Stange-Thomann N, DeArellano K, Johnson R, Linton L, McEwan P, McKernan K, Talamas J, Tirrell A, Ye W, Zimmer A, Barber RD, Cann I, Graham DE, Grahame DA, Guss AM, Hedderich R, Ingram-Smith C, Kuettner HC, Krzycki JA, Leigh JA, Li W, Liu J, Mukhopadhyay B, Reeve JN, Smith K, Springer TA, Umayam LA, White O, White RH, Conway DE Macario E, Ferry JG, Jarrell KF, Jing H, Macario AJ, Paulsen I, Pritchett M, Sowers KR, Swanson RV, Zinder SH, Lander E, Metcalf WW, Birren B. 2002. The genome of Methanosarcina acetivorans reveals extensive metabolic and physiological diversity. Genome Res. 12: 532-542.
62. Callaghan AV, Morris BE, Pereira IA, McInerney MJ, Austin RN, Groves JT, Kukor JJ, Suflita JM, Young LY, Zylstra GJ, Wawrik B. 2012. The genome sequence of Desulfatibacillum alkenivorans AK-01: a blueprint for anaerobic alkane oxidation. Environ. Microbiol. 14:101-113.
63. Kapatral V, Anderson I, Ivanova N, Reznik G, Los T, Lykidis A, Bhattacharyya A, Bartman A, Gardner W, Grechkin G, Zhu L, Vasieva O, Chu L, Kogan Y, Chaga O, Goltsman E, Bernal A, Larsen N, D'Souza M, Walunas T, Pusch G, Haselkorn R, Fonstein M, Kyrpides N, Overbeek R. 2002. Genome sequence and analysis of the oral bacterium Fusobacterium nucleatum strain ATCC 25586. J. Bacteriol. 184:2005-2018.
64. Staples CR, Lahiri S, Raymond J, Von Herbulis L, Mukhophadhyay B, Blankenship RE. 2007. Expression and association of group IV nitrogenase NifD and NifH homologs in the non-nitrogen-fixing archaeon Methanocaldococcus jannaschii. J. Bacteriol. 189:7392-7398.
65. Heidelberg JF, Seshadri R, Haveman SA, Hemme CL, Paulsen IT, Kolonay JF, Eisen JA, Ward N, Methe B, Brinkac LM, Daugherty SC, Deboy RT, Dodson RJ, Durkin AS, Madupu R, Nelson WC, Sullivan SA, Fouts D, Haft DH, Selengut J, Peterson JD, Davidsen TM, Zafar N, Zhou L, Radune D, Dimitrov G, Hance M, Tran K, Khouri H, Gill J, Utterback TR, Feldblyum TV, Wall JD, Voordouw G, Fraser CM. 2004. The genome sequence of the anaerobic, sulfate-reducing bacterium Desulfovibrio vulgaris Hildenborough. Nat. Biotechnol. 22:554-559.
66. 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. Proc. Natl. Acad. Sci. U. S. A. 104:7104-7109.
67. Webster G, Newberry CJ, Fry JC, Weightman AJ. 2003. Assessment of bacterial community structure in the deep sub-seafloor biosphere by 16S rDNA-based techniques: a cautionary tale. J. Microbiol. Methods 55:155-164.
68. Acinas SG, Marcelino LA, Klepac-Ceraj V, Polz MF. 2004. Divergence and redundancy of 16S rRNA sequences in genomes with multiple rrn operons. J. Bacteriol. 186:2629-2635.
69. Lipp JS, Morono Y, Inagaki F, Hinrichs KU. 2008. Significant contribution of archaea to extant biomass in marine subsurface sediments. Nature 454:991-994.
70. Stal LJ. 2009. Is the distribution of nitrogen-fixing cyanobacteria in the oceans related to temperature? Environ. Microbiol. 11:1632-1645.
71. Xu J, Yin KD, He L, Yuan XC, Ho AYT, Harrison PJ. 2008. Phosphorus limitation in the northern South China Sea during late summer: influence of the Pearl River. Deep Sea Res. 55:1330-1342.
72. Ning X, Lin C, Hao Q, Liu C, Le F, Shi J. 2009. Long term changes in the ecosystem in the northern South China Sea during 1976-2004. Biogeosciences 6:2227-2243.
73. Levin LA. 2005. Ecology of cold seep sediments: interactions of fauna with flow, chemistry and microbes. Oceanogr. Mar. Biol. Annu. Rev. 43:1-46.
74. Stams AJ, Plugge CM. 2009. Electron transfer in syntrophic communities of anaerobic bacteria and archaea. Nat. Rev. Microbiol. 7:568-577.
75. Chen Z, Yan W, Chen MH, Wang SH, Lu J, Zhang F, Xiang R, Xiao SB, Yan B, Gu SC. 2006. Discovery of seep carbonate nodules as new evidence for gas venting on the northern continental slope of South China Sea.Chin. Sci. Bull. 51:1228-1237.