Applied Microbiology and Biotechnology

, Volume 102, Issue 1, pp 447–459 | Cite as

Difference of nitrogen-cycling microbes between shallow bay and deep-sea sediments in the South China Sea

  • Tiantian Yu
  • Meng Li
  • Mingyang Niu
  • Xibei Fan
  • Wenyue Liang
  • Fengping WangEmail author
Environmental biotechnology


In marine sediments, microorganisms are known to play important roles in nitrogen cycling; however, the composition and quantity of microbes taking part in each process of nitrogen cycling are currently unclear. In this study, two different types of marine sediment samples (shallow bay and deep-sea sediments) in the South China Sea (SCS) were selected to investigate the microbial community involved in nitrogen cycling. The abundance and composition of prokaryotes and seven key functional genes involved in five processes of the nitrogen cycle [nitrogen fixation, nitrification, denitrification, dissimilatory nitrate reduction to ammonium (DNRA), and anaerobic ammonia oxidation (anammox)] were presented. The results showed that a higher abundance of denitrifiers was detected in shallow bay sediments, while a higher abundance of microbes involved in ammonia oxidation, anammox, and DNRA was found in the deep-sea sediments. Moreover, phylogenetic differentiation of bacterial amoA, nirS, nosZ, and nrfA sequences between the two types of sediments was also presented, suggesting environmental selection of microbes with the same geochemical functions but varying physiological properties.


Nitrogen cycling Microbes Marine sediments South China Sea Functional genes Abundance Phylogenetic differentiation 



We are grateful to all the staff at the Haiyang Sihao for providing help of collecting samples.


This study was funded by State Key R&D project of China (grant No. 2016YFA0601102), international IMBER project, National Special Project on Gas Hydrate of China (Grant, GZH201100311), Natural Science Foundation of China (grant no. 41525011, 91228201, 91428308, 41506163, 31622002, 31661143022), China Ocean Mineral Resources R&D Association (grant DY125-15-T-04).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Human and animal rights and informed consent

This article does not contain any studies with human participants or animals performed by any of the authors.

Supplementary material

253_2017_8594_MOESM1_ESM.pdf (1.5 mb)
ESM 1 (PDF 1552 kb)


  1. Abell GC, Revill AT, Smith C, Bissett AP, Volkman JK, Robert SS (2010) Archaeal ammonia oxidizers and nirS-type denitrifiers dominate sediment nitrifying and denitrifying populations in a subtropical macrotidal estuary. ISME J 4:286–300CrossRefPubMedGoogle Scholar
  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 25:3389–3402CrossRefPubMedPubMedCentralGoogle Scholar
  3. Babbin AR, Keil RG, Devol AH, Ward BB (2014) Organic matter stoichiometry, flux, and oxygen control nitrogen loss in the ocean. Science 344:406–408CrossRefPubMedGoogle Scholar
  4. Babbin AR, Jayakumar A, Ward BB (2016) Organic matter loading modifies the microbial community responsible for nitrogen loss in estuarine sediments. Microb Ecol 71:555–565CrossRefPubMedGoogle Scholar
  5. Bauer JE, Druffel ERM (1998) Ocean margins as a significant source of organic matter to the deep open ocean. Nature 392:482–485CrossRefGoogle Scholar
  6. Braker G, Ayala-del-Rio HL, Devol AH, Fesefeldt A, Tiedje JM (2001) Community structure of denitrifiers, bacteria, and archaea along redox gradients in Pacific Northwest marine sediments by terminal restriction fragment length polymorphism analysis of amplified nitrite reductase (nirS) and 16S rRNA genes. Appl Environ Microbiol 67:1893–1901CrossRefPubMedPubMedCentralGoogle Scholar
  7. Brandes JA, Devol AH (2002) A global marine-fixed nitrogen isotopic budget: implications for Holocene nitrogen cycling. Glob Biogeochem Cycles 16:1120CrossRefGoogle Scholar
  8. Brochier-Armanet C, Boussau B, Gribaldo S, Forterre P (2008) Mesophilic Crenarchaeota: proposal for a third archaeal phylum, the Thaumarchaeota. Nat Rev Microbiol 6:245–252CrossRefPubMedGoogle Scholar
  9. Caffrey JM, Bano N, Kalanetra K, Hollibaugh JT (2007) Ammonia oxidation and ammonia-oxidizing bacteria and archaea from estuaries with differing histories of hypoxia. ISME J 1:660–662CrossRefPubMedGoogle Scholar
  10. Canion A, Prakash O, Green SJ, Jahnke L, Kuypers MM, Kostka JE (2013) Isolation and physiological characterization of psychrophilic denitrifying bacteria from permanently cold Arctic fjord sediments (Svalbard, Norway). Environ Microbiol 15:1606–1618CrossRefPubMedGoogle Scholar
  11. Cao H, Hong Y, Li M, JD G (2012) Community shift of ammonia-oxidizing bacteria along an anthropogenic pollution gradient from the Pearl River Delta to the South China Sea. Appl Microbiol Biotechnol 94:247–259CrossRefPubMedGoogle Scholar
  12. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Peña AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Turnbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336CrossRefPubMedPubMedCentralGoogle Scholar
  13. Chen J, Wang F, Jiang L, Yin X, Xiao X (2013) Stratified communities of active archaea in shallow sediments of the Pearl River estuary, Southern China. Curr Microbiol 67:41–50CrossRefPubMedGoogle Scholar
  14. 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 48:1893–1902CrossRefGoogle Scholar
  15. Codispoti LA (2007) An oceanic fixed nitrogen sink exceeding 400 Tg N a−1 vs the concept of homeostasis in the fixed-nitrogen inventory. Biogeosciences 4:233–253CrossRefGoogle Scholar
  16. Criminger JD, Hazen TH, Sobecky PA, Lovell CR (2007) Nitrogen fixation by Vibrio parahaemolyticus and its implications for a new ecological niche. Appl Environ Microbiol 73:5959–5961CrossRefPubMedPubMedCentralGoogle Scholar
  17. Dalsgaard T, Thamdrup B, Farías L, Revsbech NP (2012) Anammox and dentrification in the oxygen minimum zone of the eastern South Pacific. Limnol Oceanogr 57:1331–1346CrossRefGoogle Scholar
  18. Dang H, Zhou H, Yang J, Ge H, Jiao N, Luan X, Zhang C, Klotz MG (2013a) Thaumarchaeotal signature gene distribution in sediments of the northern South China Sea: an indicator of the metabolic intersection of the marine carbon, nitrogen, and phosphorus cycles? Appl Environ Microbiol 79:2137–2147CrossRefPubMedPubMedCentralGoogle Scholar
  19. Dang H, Yang J, Li J, Luan X, Zhang Y, Gu G, Xue R, Zong M, Klotz MG (2013b) Environment-dependent distribution of the sediment nifH-harboring microbiota in the Northern South China Sea. Appl Environ Microbiol 79:121–132CrossRefPubMedPubMedCentralGoogle Scholar
  20. Dou Y, Li J, Zhao J, Hu B, Yang S (2013) Distribution, enrichment and source of heavy metals in surface sediments of the eastern Beibu Bay, South China Sea. Mar Pollut Bull 67:137–145CrossRefPubMedGoogle Scholar
  21. Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27:2194–2200CrossRefPubMedPubMedCentralGoogle Scholar
  22. Einsle O, Messerschmidt A, Stach P, Bourenkov GP, Bartunik HD, Huber R, Kroneck PM (1999) Structure of cytochrome c nitrite reductase. Nature 400:476–480CrossRefPubMedGoogle Scholar
  23. Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791CrossRefPubMedGoogle Scholar
  24. Gaby JC, Buckley DH (2012) A comprehensive evaluation of PCR primers to amplify the nifH gene of nitrogenase. PLoS One 7:e42149CrossRefPubMedPubMedCentralGoogle Scholar
  25. Gruber N (2004) The dynamics of the marine nitrogen cycle and its influence on atmospheric CO2. In: Follows M, Oguz T (eds) The ocean carbon cycle and climate. Kluwer Academic, Dordrecht, pp 97–148CrossRefGoogle Scholar
  26. Handley KM, Lloyd JR (2013) Biogeochemical implications of the ubiquitous colonization of marine habitats and redox gradients by Marinobacter species. Front Microbiol 4:136CrossRefPubMedPubMedCentralGoogle Scholar
  27. Harhangi HR, Le Roy M, van Alen T, BL H, 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 78:752–758CrossRefPubMedPubMedCentralGoogle Scholar
  28. 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. Proc Natl Acad Sci U S A 105:2134–2139CrossRefPubMedPubMedCentralGoogle Scholar
  29. Hong YG, Li M, Cao H, JD G (2011) 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 62:36–47CrossRefPubMedPubMedCentralGoogle Scholar
  30. Jiang H, Dong H, Ji S, Ye Y, Wu N (2007) Microbial diversity in the deep marine sediments from the Qiongdongnan Basin in South China Sea. Geomicrobiol J 24:505–517CrossRefGoogle Scholar
  31. Jiang L, Zheng Y, Chen J, Xiao X, Wang F (2011) Stratification of archaeal communities in shallow sediments of the Pearl River estuary, Southern China. Antonie Van Leeuwenhoek 99:739–751CrossRefPubMedGoogle Scholar
  32. Jin T, Zhang T, Ye L, Lee OO, Wong YH, Qian PY (2011) Diversity and quantity of ammonia-oxidizing archaea and bacteria in sediment of the Pearl River estuary, China. Appl Microbiol Biotechnol 90:1137–1145CrossRefPubMedPubMedCentralGoogle Scholar
  33. Jin R, Liu T, Liu G, Zhou J, Huang J, Wang A (2015) Simultaneous heterotrophic nitrification and aerobic denitrification by the marine origin bacterium Pseudomonas sp. ADN-42. Appl Biochem Biotechnol 175:2000–2011CrossRefPubMedGoogle Scholar
  34. Kallmeyer J, Pockalny R, Adhikari RR, Smith DC, D’Hondtc S (2012) Global distribution of microbial abundance and biomass in subseafloor sediment. Proc Natl Acad Sci U S A 109:16213–16216CrossRefPubMedPubMedCentralGoogle Scholar
  35. Kandeler E, Deiglmayr K, Tscherko D, Bru D, Philippot L (2006) Abundance of narG, nirS, nirK, and nosZ genes of denitrifying bacteria during primary successions of a glacier foreland. Appl Environ Microbiol 72:5957–5962CrossRefPubMedPubMedCentralGoogle Scholar
  36. Kang SR, Srinivasan S, Lee SS (2015) Vibrio oceanisediminis sp. nov., a nitrogen-fixing bacterium isolated from an artificial oil-spill marine sediment. Int J Syst Evol Microbiol 65:3552–3557CrossRefPubMedGoogle Scholar
  37. Karner MB, DeLong EF, Karl DM (2001) Archaeal dominance in the mesopelagic zone of the Pacific Ocean. Nature 409:507–510CrossRefPubMedGoogle Scholar
  38. Kartal B, Rattray J, van Niftrik LA, van de Vossenberg J, Schmid MC, Webb RI, Schouten S, Fuerst JA, Damste JS, Jetten MS, Strous M (2007) Candidatus “Anammoxoglobus propionicus” a new propionate oxidizing species of anaerobic ammonium oxidizing bacteria. Syst Appl Microbiol 30:39–49CrossRefPubMedGoogle Scholar
  39. Kartal B, van Niftrik L, Rattray J, van de Vossenberg JL, Schmid MC, Sinninghe Damste J, Jetten MS, Strous M (2008) Candidatus “Brocadia fulgida”: an autofluorescent anaerobic ammonium oxidizing bacterium. FEMS Microbiol Ecol 63:46–55CrossRefPubMedGoogle Scholar
  40. Kloos K, Mergel A, Rosch C, Bothe H (2001) Denitrification within the genus Azospirillum and other associative bacteria. Aust J Plant Physiol 28:991–998Google Scholar
  41. Könneke M, Bernhard AE, de la Torre JR, Walker CB, Waterbury JB, Stahl DA (2005) Isolation of an autotrophic ammonia- oxidizing marine archaeon. Nature 437:543–546CrossRefPubMedGoogle Scholar
  42. Kraft B, Tegetmeyer HE, Meier D, Geelhoed JS, Strous M (2014) Rapid succession of uncultured marine bacterial and archaeal populations in a denitrifying continuous culture. Environ Microbiol 16:3275–3286CrossRefPubMedGoogle Scholar
  43. Kuenen JG (2008) Anammox bacteria: from discovery to application. Nat Rev Microbiol 6:320–326CrossRefPubMedGoogle Scholar
  44. Lehtovirta LE, Prosser JI, Nicol GW (2009) Soil pH regulates the abundance and diversity of group 1.1c Crenarchaeota. FEMS Microbiol Ecol 70:367–376CrossRefPubMedGoogle Scholar
  45. Li M, Hong Y, Cao H, Klotz MG, JD G (2013a) Diversity, abundance, and distribution of NO-forming nitrite reductase-encoding genes in deep-sea subsurface sediments of the South China Sea. Geobiology 11:170–179CrossRefPubMedGoogle Scholar
  46. Li R, Zi X, Wang X, Zhang X, Gao H, Hu N (2013b) Marinobacter hydrocarbonoclasticus NY-4, a novel denitrifying, moderately halophilic marine bacterium. Spring 2:346CrossRefGoogle Scholar
  47. Liu Y, Ai GM, Miao LL, Liu ZP (2016) Marinobacter strain NNA5, a newly isolated and highly efficient aerobic denitrifier with zero N2O emission. Bioresour Technol 206:9–15CrossRefPubMedGoogle Scholar
  48. Lovell CR (2002) Plant-microbe interactions in the marine environment. In: Bitton G (ed) Encyclopedia of environmental microbiology, vol 5. Wiley, New York, pp 2539–2554Google Scholar
  49. Magoč T, Salzberg SL (2011) FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27:2957–22963CrossRefPubMedPubMedCentralGoogle Scholar
  50. Mohan SB, Schmid M, Jetten M, Cole J (2004) Detection and widespread distribution of the nrfA gene encoding nitrite reduction to ammonia, a short circuit in the biological nitrogen cycle that competes with denitrification. FEMS Microbiol Ecol 49:433–443CrossRefPubMedGoogle Scholar
  51. Moin NS, Nelson KA, Bush A, Bernhard AE (2009) Distribution and diversity of archaeal and bacterial ammonia oxidizers in salt marsh sediments. Appl Environ Microbiol 75:7461–7468CrossRefPubMedPubMedCentralGoogle Scholar
  52. Mosier AC, Francis CA (2008) Relative abundance and diversity of ammonia-oxidizing archaea and bacteria in the San Francisco Bay estuary. Environ Microbiol 10:3002–3016CrossRefPubMedGoogle Scholar
  53. 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 22:365–372CrossRefGoogle Scholar
  54. Nunoura T, Nishizawa M, Kikuchi T, Tsubouchi T, Hirai M, Koide O, Miyazaki J, Hirayama H, Koba K, Takai K (2013) Molecular biological and isotopic biogeochemical prognoses of the nitrification-driven dynamic microbial nitrogen cycle in hadopelagic sediments. Environ Microbiol 15:3087–3107PubMedGoogle Scholar
  55. Oakley BB, Francis CA, Roberts KJ, Fuchsman CA, Srinivasan S, Staley JT (2007) Analysis of nitrite reductase (nirK and nirS) genes and cultivation reveal depauperate community of denitrifying bacteria in the Black Sea suboxic zone. Environ Microbiol 9:118–130CrossRefPubMedGoogle Scholar
  56. Ochsenreiter T, Selezi D, Quaiser A, Bonch-Osmolovskaya L, Schleper C (2003) Diversity and abundance of Crenarchaeota in terrestrial habitats studied by 16S RNA surveys and real time PCR. Environ Microbiol 5:787–797CrossRefPubMedGoogle Scholar
  57. 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 12:605–615CrossRefPubMedGoogle Scholar
  58. Peng D, Chen C, Pang X, Zhu M, Yang F (2004) Discovery of deep-water fan system in South China Sea. Acta Petrol Sin 25:17–23 (in Chinese with English abstract)Google Scholar
  59. Pester M, Schleper C, Wagner M (2011) The Thaumarchaeota: an emerging view of their phylogeny and ecophysiology. Curr Opin Microbiol 14:300–306CrossRefPubMedPubMedCentralGoogle Scholar
  60. Reigstad LJ, Richter A, Daims H, Urich T, Schwark L, Schleper C (2008) Nitrification in terrestrial hot springs of Iceland and Kamchatka. FEMS Microbiol Ecol 64:167–174CrossRefPubMedGoogle Scholar
  61. Russ L, Kartal B, Op den Camp HJ, Sollai M, Le Bruchec J, Caprais JC, Godfroy A, Sinninghe Damsté JS, Jetten MS (2013) Presence and diversity of anammox bacteria in cold hydrocarbon-rich seeps and hydrothermal vent sediments of the Guaymas Basin. Front Microbiol 4:219CrossRefPubMedPubMedCentralGoogle Scholar
  62. Santoro AE, Boehm AB, Francis CA (2006) Denitrifier community composition along a nitrate and salinity gradient in a coastal aquifer. Appl Environ Microbiol 72:2102–2109CrossRefPubMedPubMedCentralGoogle Scholar
  63. Santoro AE, Francis CA, de Sieyes NR, Boehm AB (2008) Shifts in the relative abundance of ammonia oxidizing bacteria and archaea across physicochemical gradients in a subterranean estuary. Environ Microbiol 10:1068–1079CrossRefPubMedGoogle Scholar
  64. Schmid M, Walsh K, Webb R, Rijpstra WI, van de Pas-Schoonen K, Verbruggen MJ, Hill T, Moffett B, Fuerst J, Schouten S, Damste JS, Harris J, Shaw P, Jetten M, Strous M (2003) Candidatus “Scalindua brodae”, sp. nov., Candidatus “Scalindua wagneri”, sp. nov., two new species of anaerobic ammonium oxidizing. Syst Appl Microbiol 26:529–538CrossRefPubMedGoogle Scholar
  65. Segawa T, Ishii S, Ohte N, Akiyoshi A, Yamada A, Maruyama F, Li Z, Hongoh Y, Takeuchi N (2014) The nitrogen cycle in cryoconites: naturally occurring nitrification-denitrification granules on a glacier. Environ Microbiol 16:3250–3262CrossRefPubMedGoogle Scholar
  66. Shieh WY, Simidu U, Maruyama Y (1990) A Photobacterium-like bacterium able to fix nitrogen. Antonie Van Leeuwenhoek 57:51–54CrossRefPubMedGoogle Scholar
  67. Smith CJ, Nedwell DB, Dong LF, Osborn AM (2007) Diversity and abundance of nitrate reductase genes (narG and napA), nitrite reductase genes (nirS and nrfA), and their transcripts in estuarine sediments. Appl Environ Microbiol 73:3612–3622CrossRefPubMedPubMedCentralGoogle Scholar
  68. Solorzano L (1969) Determination of ammonia in natural waters by the phenol hypochlorite method. Limnol Oceanogr 14:799–801CrossRefGoogle Scholar
  69. Song Z, Wang F, Zhi X, Chen J, Zhou E, Liang F, Xiao X, Tang S, Jiang H, Zhang C, Dong H, Li W (2013) Bacterial and archaeal diversities in Yunnan and Tibetan hot springs, China. Environ Microbiol 15:1160–1175CrossRefPubMedGoogle Scholar
  70. Sonthiphand P, Hall MW, Neufeld JD (2014) Biogeography of anaerobic ammonia-oxidizing (anammox) bacteria. Front Microbiol 5:399CrossRefPubMedPubMedCentralGoogle Scholar
  71. Stieglmeier M, Klingl A, Alves RJ, Rittmann SK, Melcher M, Leisch N, Schleper C (2014) Nitrososphaera viennensis sp. nov., an aerobic and mesophilic ammonia-oxidizing archaeon from soil and member of the archaeal phylum Thaumarchaeota. Int J Syst Evol Microbiol 64:2738–2752CrossRefPubMedPubMedCentralGoogle Scholar
  72. 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 105:10460–10465CrossRefPubMedPubMedCentralGoogle Scholar
  73. Tamegai H, Aoki R, Arakawa S, Kato C (2007) Molecular analysis of the nitrogen cycle in deep-sea microorganisms from the Nankai Trough: genes for nitrification and denitrification from deep-sea environmental DNA. Extremophiles 11:269–275CrossRefPubMedGoogle Scholar
  74. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729CrossRefPubMedPubMedCentralGoogle Scholar
  75. Taylor B, Hayes DE (1983) Origin and history of the South China Sea basin. In: Hayes DE (ed) The tectonic and geologic evolution of southeast Asian seas and islands. AUG, Washington, DC, pp 23–56CrossRefGoogle Scholar
  76. Thröback IN, Enwall K, Jarvis A, Hallin S (2004) Reassessing PCR primers targeting nirS, nirK and nosZ genes for community surveys of denitrifying bacteria with DGGE. FEMS Microbiol Ecol 49:401–417CrossRefPubMedGoogle Scholar
  77. Trimmer M, Engström P (2011) The environmental distribution, activity and ecology of anammox. In: Ward BB, Klotz MG, Arp DJ (eds) Nitrification. ASM Press, Washington, DC, pp 201–235CrossRefGoogle Scholar
  78. Welsh A, Chee-Sanford JC, Connor LM, Löffler FE, Sanford RA (2014) Refined NrfA phylogeny improves PCR-based nrfA gene detection. Appl Environ Microbiol 80:2110–2119CrossRefPubMedPubMedCentralGoogle Scholar
  79. Xie W, Zhang C, Zhou X, Wang P (2014) Salinity-dominated change in community structure and ecological function of archaea from the lower Pearl River to coastal South China Sea. Appl Microbiol Biotechnol 98:7971–7982CrossRefPubMedGoogle Scholar
  80. Yoshinari T (1980) N2O reduction by Vibrio succinogenes. Appl Environ Microbiol 39:81–84PubMedPubMedCentralGoogle Scholar
  81. Zehr JP, Capone DG (1996) Problems and promises of assaying the genetic potential for nitrogen fixation in the marine environment. Microb Ecol 32:263–281CrossRefPubMedGoogle Scholar
  82. Zehr JP, Turner PJ (2001) Nitrogen fixation: nitrogenase genes and gene expression. In: Paul JH (ed) Methods in microbiology. Academic Press, New York, pp 271–285Google Scholar
  83. Zehr JP, Jenkins BD, Short SM, Steward GF (2003) Nitrogenase gene diversity and microbial community structure: a cross-system comparison. Environ Microbiol 5:539–554CrossRefPubMedGoogle Scholar
  84. Zhalnina KV, Dias R, Leonard MT, Dorr de Quadros P, Camargo FA, Drew JC, Farmerie WG, Daroub SH, Triplett EW (2014) Genome sequence of Candidatus Nitrososphaera evergladensis from group I.1b enriched from Everglades soil reveals novel genomic features of the ammonia-oxidizing archaea. PLoS One 9:e101648CrossRefPubMedPubMedCentralGoogle Scholar
  85. Zhang CL, Ye Q, Huang ZY, Li WJ, Chen JQ, Song ZQ, Zhao WD, Bagwell C, Inskeep WP, Ross C, Gao L, Wiegel J, Romanek CS, Shock EL, Hedlund BP (2008) Global occurrence of archaeal amoA genes in terrestrial hot springs. Appl Environ Microbiol 74:6417–6426CrossRefPubMedPubMedCentralGoogle Scholar
  86. Zhang Y, Su X, Chen F, Wang Y, Jiao L, Dong H, Huang Y, Jiang H (2012) Microbial diversity in cold seep sediments from the northern South China Sea. Geosci Front 3:301–316CrossRefGoogle Scholar
  87. Zhu D, Tanabe SH, Yang C, Zhang W, Sun J (2013) Bacterial community composition of South China Sea sediments through pyrosequencing-based analysis of 16S rRNA genes. PLoS One 8:e78501CrossRefPubMedPubMedCentralGoogle Scholar
  88. Zumft WG (1997) Cell biology and molecular basis of denitrification. Microbiol Mol Biol Rev 61:533–616PubMedPubMedCentralGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany 2017

Authors and Affiliations

  • Tiantian Yu
    • 1
    • 2
    • 3
  • Meng Li
    • 4
  • Mingyang Niu
    • 1
    • 2
  • Xibei Fan
    • 1
    • 2
  • Wenyue Liang
    • 1
    • 2
  • Fengping Wang
    • 1
    • 2
    Email author
  1. 1.State Key Laboratory of Microbial Metabolism, School of Life Sciences and Biotechnology 3-211Shanghai Jiao Tong UniversityShanghaiChina
  2. 2.State Key Laboratory of Ocean EngineeringShanghai Jiao Tong UniversityShanghaiChina
  3. 3.College of Pharmacy and Life ScienceJiujiang UniversityJiujiangChina
  4. 4.Institute for Advanced StudyShenzhen UniversityShenzhenChina

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