Phylogenetic and functional diversity of nitrogen cycling microbes in coastal sediments

doi:10.3724/SP.J.1003.2013.12027

Abstract

Abstract:

The coastal zone contains diverse habitats which are usually characterized by strong environmental gradients (e.g. salinity, nutrients and pollutants). This makes the coastal zone an ideal experimental laboratory for describing microbial diversity and testing hypotheses on community structure, function and control. Coastal sediment is of significance in nutrient regeneration and transformation involving different assemblages of microbes in the nitrogen cycle. This review focuses on 16S rRNA gene-based phylogenetic diversity and the key enzyme encoding gene-based (e.g. nifH, amoA, narG, nirS, nirK, nosZ, nrfA, hzo and hzs) functional diversity of nitrogen fixing, ammonia oxidizing and anaerobic ammonia oxidation (Anammox) bacteria as well as bacteria and fungi involved in denitrification and dissimilatory nitrate reduction to ammonium (DNRA). Characteristics of community composition and diversity of nitrogen cycling microbes in different habitats (e.g. estuarine, intertidal flats, seagrass or seaweed beds, mangroves, salt marsh, coral reefs, and shallow seas), and their spatiotemporal patterns under benthic pollution or bioturbation are reviewed. Future directions for a better understanding diversity of nitrogen cycling microbes are suggested, such as culture methods and technologies, and single-cell sequencing, etc.

Key words: community composition, functional genes, functional diversity, marine benthos, molecular ecology, phylogenetic diversity, phylogenetic classification

Jun Gong,Yanjing Song,Xiaoli Zhang. Phylogenetic and functional diversity of nitrogen cycling microbes in coastal sediments[J]. Biodiv Sci, 2013, 21(4): 433-444.

Add to citation manager EndNote|Ris|BibTeX

URL: https://www.biodiversity-science.net/EN/10.3724/SP.J.1003.2013.12027

https://www.biodiversity-science.net/EN/Y2013/V21/I4/433

Figures/Tables 1

References 113

79	Risgaard-Petersen N, Langezaal AM, Ingvardsen S, Schmid MC, Jetten MSM, Op den Camp HJM, Derksen JWM, Piña-Ochoa E, Eriksson SP, Nielsen LP, Revsbech NP, Cedhagen T, van der Zwaan GJ (2006) Evidence for complete denitrification in a benthic foraminifer.Nature, 443, 93-96.
80	Rohwer F, Seguritan V, Azam F, Knowlton N (2002) High diversity and species-specific distribution of coral-asso- ciated bacteria.Marine Ecology Progress Series, 243, 1-10.
81	Sahan E, Muyzer G (2008) Diversity and spatio-temporal distribution of ammonia-oxidizing Archaea and Bacteria in sediments of the Westerschelde estuary.FEMS Microbiology Ecology, 64, 175-186.
82	Santoro AE, Boehm AB, Francis CA (2006) Denitrifier community composition along a nitrate and salinity gradient in a coastal aquifer.Applied and Environmental Microbiology, 72, 2102-2109.
83	Sayama M (2001) Presence of nitrate-accumulating sulfur bacteria and their influence on nitrogen cycling in a shallow coastal marine sediment.Applied and Environmental Microbiology, 67, 3481-3487.
84	Schleper C, Jurgens G, Jonuscheit M (2005) Genomic studies of uncultivated archaea.Nature Reviews Microbiology, 3, 479-488.
85	Schmid MC, Hooper AB, Klotz MG, Woebken D, Lam P, Kuypers MM, Pommerening-Roeser A, Op den Camp HJ, Jetten MS (2008) Environmental detection of octahaem cytochrome c hydroxylamine/hydrazine oxidoreductase genes of aerobic and anaerobic ammonium-oxidizing bacteria.Environmental Microbiology, 10, 3140-3149.
86	Schmid MC, Risgaard-Petersen N, van de Vossenberg J, Kuypers MMM, Lavik G, Petersen J, Hulth S, Thamdrup B, Canfield D, Dalsgaard T, Rysgaard S, Sejr MK, Strous M, den Camp HJ, Jetten MSM (2007) Anaerobic ammonium-oxidizing bacteria in marine environments: widespread occurrence but low diversity.Environmental Microbiology, 9, 1476-1484.
87	Severin I, Acinas SG, Stal LJ (2010) Diversity of nitrogen-fixing bacteria in cyanobacterialmats.FEMS Microbiology Ecology, 73, 514-525.
88	Shen JP (沈菊培), He JZ (贺纪正) (2011) Responses of microbes-mediated carbon and nitrogen cycles to global climate change.Acta Ecologica Sinica(生态学报), 31, 2957-2967. (in Chinese with English abstract)
89	Short SM, Zehr JP (2007) Nitrogenase gene expression in the Chesapeake Bay Estuary.Environmental Microbiology, 9, 1591-1596.
90	Shoun H, Kim DH, Uchiyama H, Sugiyama J (1992) Denitrification by fungi.FEMS Microbiology Letters, 94, 277-281.
1	Abell GC, Revill AT, Smith C, Bissett AP, Volkman JK, Robert SS (2009) Archaeal ammonia oxidizers and nirS-type denitrifiers dominate sediment nitrifying and denitrifying populations in a subtropical macrotidal estuary.The ISME Journal, 4, 286-300.
2	Achá D, Iñiguez V, Roulet M, Guimarães JRD, Luna R, Alanoca L, Sanchez S (2005) Sulfate-reducing bacteria in floating macrophyte rhizospheres from an Amazonian floodplain lake in Bolivia and their association with Hg methylation.Applied and Environmental Microbiology, 71, 7531-7535.
3	Adame MF, Virdis B, Lovelock CE (2010) Effect of geomorphological setting and rainfall on nutrient exchange in mangroves during tidal inundation.Marine and Freshwater Research, 61, 1197-1206.
91	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.Applied and Environmental Microbiology, 73, 3612-3622.
92	Smith AC, Kostka JE, Devereux R, Yates DF (2004) Seasonal composition and activity of sulfate-reducing prokaryotic communities in seagrass bed sediments.Aquatic Microbial Ecology, 37, 183-195.
4	Affourtit J, Zehr JP, Paerl HW (2001) Distribution of nitrogen-fixing microorganisms along the Neuse River Estuary, North Carolina.Microbial Ecology, 41, 114-123.
5	Alikunhi NM, Narayanasamy R, Kandasamy K (2010) Fatty acids in an estuarine mangrove ecosystem.Revista de Biología Tropical, 58, 577-587.
6	Bagwell CE, Lovell CR (2000) Persistence of selected Spartina alterniflora rhizoplane diazotrophs exposed to natural and manipulated environmental variability.Applied and Environmental Microbiology, 66, 4625-4633.
7	Beltrán Y, Centeno CM, García-Oliva F, Legendre P, Falcón LI (2012) N2 fixation rates and associated diversity (nifH) of microbialite and mat-forming consortia from different aquatic environments in Mexico.Aquatic Microbial Ecology, 67, 15-24.
93	Stepanauskas R, Sieracki ME (2007) Matching phylogeny and metabolism in the uncultured marine bacteria, one cell at a time. Proceedings of the National Academy of Sciences,USA, 104, 9052-9057.
94	Steppe TF, Paerl HW (2005) Nitrogenase activity and nifH expression in a marine intertidal microbial mat.Microbial Ecology, 49, 315-324.
95	Sengupta A, Chaudhuri S (1991) Ecology of heterotrophic dinitrogen fixation in the rhizosphere of mangrove plant community at the Ganges river estuary in India.Oecologia, 87, 560-564.
8	Beman JM, Francis CA (2006) Diversity of ammonia-oxidizing archaea and bacteria in the sediments of a hypernutrified subtropical estuary: Bahía del Tóbari, Mexico.Applied and Environmental Microbiology, 72, 7767-7777.
9	Beman JM, Roberts KJ, Wegley L, Rohwer F, Francis CA (2007) Distribution and diversity of archaeal ammonia monooxygenase genes associated with corals. Applied and Environmental Microbiology, 73, 5642-5647.
10	Bergholz PW, Bagwell CE, Lovell CR (2001) Physiological diversity of rhizoplane diazotrophs of the salt-meadow cordgrass, Spartina patens: implications for host specific ecotypes.Microbial Ecology, 42, 466-473.
11	Bernhard AE, Donn T, Giblin AE, Stahl DA (2005) Loss of diversity of ammonia-oxidizing bacteria correlates with increasing salinity in an estuary system.Environmental Microbiology, 7, 1289-1297.
96	Takeuchi J (2006) Habitat segregation of a functional gene encoding nitrate ammonification in estuarine sediments.Geomicrobiology Journal, 23, 75-87.
97	Taroncher-Oldenburg G, Griner EM, Francis CA, Ward BB (2003) Oligonucleotide microarray for the study of functional gene diversity in the nitrogen cycle in the environment.Applied and Environmental Microbiology, 69, 1159-1171.
98	Thatoi H, Behera BC, Mishra RR, Dutta SK (2013) Biodiversity and biotechnological potential of microorganisms from mangrove ecosystems: a review.Annals of Microbiology, 63, 1-19.
12	Bolhuis H, Stal LJ (2011) Analysis of bacterial and archaeal diversity in coastal microbial mats using massive parallel 16S rRNA gene tag sequencing.The ISME Journal, 5, 1701-1712.
13	Brito Â, Ramos V, Seabra R, Santos A, Santos CL, Lopo M, Ferreira S, Martins A, Mota R, Frazäo B, Martins R, Vasconcelos V, Tamagnini P (2012) Culture-dependent characterization of cyanobacterial diversity in the intertidal zones of the Portuguese coast: a polyphasic study.Systematic and Applied Microbiology, 35, 110-119.
14	Burns JA, Zehr JP, Capone DG (2002) Nitrogen fixing phylotypes of Chesapeake Bay and Neuse River Estuary sediments.Microbial Ecology, 44, 336-343.
15	Cao H, Li M, Hong Y, Gu JD (2011) Diversity and abundance of ammonia-oxidizing archaea and bacteria in polluted mangrove sediment.Systematic and Applied Microbiology, 34, 513-523.
16	Capone DG, Carpenter EJ (1982) Nitrogen fixation in the marine environment.Science, 217, 1140-1142.
17	Cathrine SJ, Raghukumar C (2009) Anaerobic denitrification in fungi from the coastal marine sediments off Goa, India.Mycological Research, 113, 100-109.
18	Dale OR, Tobias CR, Song B (2009) Biogeographical distribution of diverse anaerobic ammonium oxidizing (anammox) bacteria in Cape Fear River Estuary.Environmental Microbiology, 11, 1194-1207.
99	Tiquia SM, Masson SA, Devo A (2006) Vertical distribution of nitrite reductase genes (nirS) in continental margin sediments of the Gulf of Mexico.FEMS Microbiology Ecology, 58, 464-475.
100	Venter JC, Remington K, Heidelberg JF, Halpern AL, Rusch D, Eisen JA, Wu D, Paulsen I, Nelson KE, Nelson W, Fouts DE, Levy S, Knap AH, Lomas MW, Nealson K, White O, Peterson J, Hoffman J, Parsons R, Baden-Tillson H, Pfannkoch C, Rogers YH, Smith HO (2004) Environmental genome shotgun sequencing of the Sargasso Sea.Science, 304, 66-74.
101	Wang BJ (王保军), Liu SJ (刘双江) (2013) Perspectives on the cultivability of environmental microorganisms.Microbiology China(微生物学通报), 40, 6-17. (in Chinese with English abstract)
19	Dang H, Chen R, Wang L, Guo L, Chen P, Tang Z, Tian F, Li S, Klotz MG (2010) Environmental factors shape sediment anammox bacterial communities in hypernutrified Jiaozhou Bay, China.Applied and Environmental Microbiology, 76, 7036-7047.
20	Davis CS, McGillicuddy DJ (2006) Transatlantic abundance of the N2-fixing colonial cyanobacterium Trichodesmium.Science, 312, 1517-1520.
21	Driscoll CT, Whitall D, Aber J, Boyer E, Castro M, Cronan C, Goodale CL, Groffman P, Hopkinson C, Lambert K, Lawrence G, Ollinger S (2003) Nitrogen pollution in the northeastern United States: sources, effects, and management options.BioScience, 53, 357-374.
22	Du JG (杜建国), Cheung WWL, Chen B (陈彬), Zhou QL (周秋麟), Yang SY (杨圣云), Ye G (2012) Progress and prospect of climate change and marine biodiversity.Biodiversity Science(生物多样性), 20, 745-754. (in Chinese with English abstract)
23	Enwall K, Philippot L, Hallin S (2005) Activity and composition of the denitrifying bacterial community respond differently to long-term fertilization.Applied and Environmental Microbiology, 71, 8335-8343.
24	Fernàndez-Guerra A, Casamayor EO (2012) Habitat-asso- ciated phylogenetic community patterns of microbial ammonia oxidizers.PLoS ONE, 7, e47330.
102	Wang S, Zhu G, Peng Y, Jetten MSM, Yin C (2012) Anammox bacterial abundance, activity, and contribution in riparian sediments of the Pearl River Estuary.Environmental Science and Technology, 46, 8834-8842.
103	Wankel SD, Mosier AC, Hansel CM, Paytan A, Francis CA (2011) Spatial variability in nitrification rates and ammonia-oxidizing microbial communities in the agriculturally impacted Elkhorn Slough estuary, California.Applied and Environmental Microbiology, 77, 269-280.
104	Ward BB, Eveillard D, Kirshtein JD, Nelson JD, Voytek MA, Jackson GA (2007) Ammonia-oxidizing bacterial community composition in estuarine and oceanic environments assessed using a functional gene microarray.Environmental Microbiology, 9, 2522-2538.
25	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. Proceedings of the National Academy of Sciences,USA, 102, 14683-14688.
26	Gaby JC, Buckley DH (2011) A global census of nitrogenase diversity.Environmental Microbiology, 13, 1790-1799.
27	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.Microbial Ecology, 59, 253-265.
28	Gilbertson WW, Solan M, Prosser JI (2012) Differential effects of microorganisminvertebrate interactions on benthic nitrogen cycling.FEMS Microbiology Ecology, 82, 11-22.
105	Whigham DF, Verhoeven JTA, Samarkin V, Megonigal PJ (2009) Responses of Avicennia germinans (Black Mangrove) and the soil microbial community to nitrogen addition in a hypersaline wetland.Estuaries and Coasts, 32, 926-936.
106	Zehr JP (2001) Unicellular cyanobacteria fix N2 in the subtropical North Pacific Ocean.Nature, 412, 635-638.
107	Zehr JP, Jenkins BD, Short SM, Steward GF (2003) Nitrogenase gene diversity and microbial community structure: a cross-system comparison.Environmental Microbiology, 5, 539-554.
29	Gong J (龚骏), Zhang XL (张晓黎) (2013) Contribution and mechanism of microbe-driving nitrogen cycling processes in coastal ecosystem.Microbiology China(微生物学通报), 40, 44-58. (in Chinese with English abstract)
30	Guo LD (郭良栋) (2012) Progress of microbial species diversity research in China.Biodiversity Science(生物多样性), 20, 572-580. (in Chinese with English abstract)
31	Groβkopf T, Mohr W, Baustian T, Schunck H, Gill D, Kuypers MMM, Lavik G, Schmitz RA, Wallace DWR, LaRoche J (2012) Doubling of marine dinitrogen-fixation rates based on direct measurements.Nature, 488, 361-364.
32	Harhangi HR, Roy ML, van Alen T, Hu B, Groen J, Kartal B, Tringe SG, Quan Z, Jetten MSM, Op den Camp HJ (2012) Hydrazine synthase, a unique phylomarker with which to study the presence and biodiversity of anammox bacteria.Applied and Environmental Microbiology, 78, 752-758.
108	Zehr JP, Kudela RM (2011) Nitrogen cycle of the open ocean: from genes to ecosystems.Annual Review of Marine Science, 3, 197-225.
109	Zehr JP, Mellon M, Braun S, Litaker W, Steppe T, Paerl HW (1995) Diversity of heterotrophic nitrogen fixation genes in a marine cyanobacterial mat.Applied and Environmental Microbiology, 61, 2527-2532.
110	Zhang LM (张丽梅), He JZ (贺纪正) (2012) A novel archaeal phylum: Thaumarchaeota—A review.Acta Microbiologica Sinica(微生物学报), 52, 411-421. (in Chinese with English abstract)
33	He Z, Gentry TJ, Schadt CW, Wu L, Liebich J, Chong SC, Huang Z, Wu W, Gu B, Jardine P, Criddle C, Zhou J (2007) GeoChip: a comprehensive microarray for investigating biogeochemical, ecological and environmental processes.The ISME Journal, 1, 67-77.
34	Herbert RA (1999) Nitrogen cycling in coastal marine ecosystems.FEMS Microbiology Reviews, 23, 563-590.
35	Hewson I, Fuhrman JA (2006) Spatial and vertical biogeography of coral reef sediment bacterial and diazotroph communities.Marine Ecology Progress Series, 306, 79-86.
111	Zhang QG (张全国), Zhang DY (张大勇) (2003) Biodiversity and ecosystem functioning: recent advances and trends.Biodiversity Science(生物多样性), 11, 351-363. (in Chinese with English abstract)
112	Zhou Z, Takaya N, Nakamura A, Yamaguchi M, Takeo K, Shoun H (2002) Ammonia fermentation, a novel anoxic metabolism of nitrate by fungi.Journal of Biological Chemistry, 227, 1892-1896.
36	Hewson I, Moisander PH, Morrison AE, Zehr JP (2007) Diazotrophic bacterioplankton in a coral reef lagoon: phylogeny, diel nitrogenase expression and response to phosphate enrichment.The ISME Journal, 1, 78-91.
37	Hu B, Shen L, Du P, Zheng P, Xu X, Zeng J (2012) The influence of intense chemical pollution on the community composition, diversity and abundance of anammox bacteria in the Jiaojiang Estuary (China).PLoS ONE, 7, 33826-33826.
38	Huang S, Chen C, Yang X, Wu Q, Zhang R (2011) Distribution of typical denitrifying functional genes and diversity of the nirS-encoding bacterial community related to environmental characteristics of river sediments.Biogeosciences, 8, 3041-3051.
39	Humbert S, Tarnawski S, Fromin N, Mallet MP, Aragno M, Zopfi J (2009) Molecular detection of anammox bacteria in terrestrial ecosystems: distribution and diversity.The ISME Journal, 4, 450-454.
40	Jørgensen BB (1996) Material flux in the sediment. In: Eutrophication in Coastal Marine Ecosystems, Coastal Estuarine Studies (eds Jørgensen BB, Richardson K), Vol. 52, pp. 115-135. AGU, Washington,DC.
41	Jones CM, Hallin S (2010) Ecological and evolutionary factors underlying global and local assembly of denitrifier communities.The ISME Journal, 4, 633-641.
42	Jones K (1982) Nitrogen fixation in the temperate estuarine intertidal sediments of the River Lune.Limnology and Oceanography, 27, 455-460.
43	Karl D, Michaels A, Bergman B, Capone D, Carpenter E, Leetelier R, Lipschultz F, Paerl H, Sigman D, Stal L (2002) Dinitrogen fixation in the world’s oceans.Biogeochemistry, 57, 47-98.
44	Kartal B, Kupers MMM, Lavik G, Schalk J, Op den Camp HJM, Jetten MSM, Strous M (2007) Anammox bacteria disguised as denitrifiers: nitrate reduction to dinitrogen gas via nitrite and ammonium.Environmental Microbiology, 9, 635-642.
45	Kim SW, Fushinobu S, Zhou S, Wakagi T, Shoun H (2009) Eukaryotic nirK genes encoding copper-containing nitrite reductase: originating from the protomitochondrion? Applied and Environmental Microbiology, 75, 2652-2658.
46	Kirshtein JD, Paerl HW, Zehr J (1991) Amplification, cloning and sequencing of a nifH segment from aquatic microorganisms and natural communities.Applied and Environmental Microbiology, 57, 2645.
47	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.
48	Kuenen JG (2008) Anammox bacteria: from discovery to application.Nature Reviews Microbiology, 6, 320-326.
49	Lage MD, Reed HE, Weihe C, Crain CM, Martiny JBH (2010) Nitrogen and phosphorus enrichment alter the composition of ammonia-oxidizing bacteria in salt marsh sediments.The ISME Journal, 4, 933-944.
50	Laverock B, Smith CJ, Tait K, Osborn AM, Widdicombe S, Gilbert JA (2010) Bioturbating shrimp alter the structure and diversity of bacterial communities in coastal marine sediments.The ISME Journal, 4, 1531-1544.
51	Li M, Cao H, Hong YG, Gu JD (2011a) 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 and Environments, 26, 15-22.
52	Li M, Cao H, Hong Y, Gu JD (2011b) Spatial distribution and abundances of ammonia-oxidizing archaea (AOA) and ammonia-oxidizing bacteria (AOB) in mangrove sediments.Applied Microbiology and Biotechnology, 89, 1243-1254.
53	Li M, Ford T, Li XY, Gu JD (2011c) Cytochrome cd1-containing nitrite reductase encoding gene nirS as a new functional biomarker for detection of anaerobic ammonium oxidizing (Anammox) bacteria. Environmental Science and Technology, 45, 3547-3553.
54	Li M, Hong YG, Cao HL, Gu JD (2011d) Mangrove trees affect the community structure and distribution of anammox bacteria at an anthropogenic-polluted mangrove in the Pearl River Delta reflected by 16S rRNA and hydrazine oxidoreductase (HZO) encoding gene analyses.Ecotoxicology, 20, 1780-1790.
55	Li M, Hong Y, 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.Applied Microbiology and Biotechnology, 86, 781-790.
56	Liu XD, Tiquia SM, Holguin G, Wu LY, Nold SC, Devol AH, Luo K, Palumbo AV, Tiedje JM, Zhou JZ (2003) Molecular diversity of denitrifying genes in continental margin sediments within the oxygen-deficient zone off the Pacific coast of Mexico.Applied and Environmental Microbiology, 69, 3549-3560.
57	Lopes VR, Vasconcelos VM (2011) Planktonic and benthic cyanobacteria of European brackish waters: a perspective on estuaries and brackish seas.European Journal of Phycology, 46, 292-304.
58	Lovell CR, Friez MJ, Longshore JW, Bagwell CE (2001) Recovery and phylogenetic analysis of nifH sequences from diazotrophic bacteria associated with dead aboveground biomass of Spartina alterniflora.Applied and Environmental Microbiology, 67, 5308-5314.
59	Lund MB, Smith JM, Francis CA (2012) Diversity, abundance and expression of nitrite reductase (nirK)-like genes in marine Thaumarchaea.The ISME Journal, 6, 1966-1977.
60	Magalhães CM, Machado A, Matos P, Bordalo AA (2011) Impact of copper on the diversity, abundance and transcription of nitrite and nitrous oxide reductase genes in an urban European estuary.FEMS Microbiology Ecology, 77, 274-284.
61	Midgley GF (2012) Biodiversity and ecosystem function.Science, 335, 174-175.
62	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.Applied and Environmental Microbiology, 75, 7153-7162.
63	Mohan SB, Schmid M, Jetten M, Cole JA (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 Microbiology Ecology, 49, 433-443.
64	Mohr W, Großkopf T, Wallace DWR, LaRoche J (2010) Methodological underestimation of oceanic nitrogen fixation rates.PLoS ONE, 5, e12583.
65	Moin NS, Nelson KA, Bush A, Bernhard AE (2009) Distribution and diversity of archaeal and bacterial ammonia oxidizers in salt marsh sediments.Applied and Environmental Microbiology, 75, 7461-7468.
66	Moisander PH, Morrison AE, Ward BB, Jenkins BD, Zehr JP (2007) Spatial-temporal variability in diazotroph assemblages in Chesapeake Bay using an oligonucleotide nifH microarray.Environmental Microbiology, 9, 1823-1835.
67	Moseman SM, Zhang R, Qian PY, Levin LA (2008) Diversity and functional responses of nitrogen-fixing microbes to three wetland invasions.Biological Invasions, 11, 225-239.
68	Mosier AC, Francis CA (2008) Relative abundance and diversity of ammonia-oxidizing archaea and bacteria in the San Francisco Bay estuary.Environmental Microbiology, 10, 3002-3016.
69	Mosier AC, Francis CA (2010) Denitrifier abundance and activity across the San Francisco Bay estuary.Environmental Microbiology Reports, 2, 667-676.
70	Musat F, Harder J, Widdel F (2006) Study of nitrogen fixation in microbial communities of oil-contaminated marine sediment microcosms.Environmental Microbiology, 10, 1834-1843.
71	Nogales B, Timmis KN, Nedwell DB, Osborn AM (2002) Detection and diversity of expressed denitrification genes in estuarine sediments after reverse transcription-PCR amplification from mRNA.Applied and Environmental Microbiology, 68, 5017-5025.
72	Olson, ND, Ainsworth TD, Gates RD, Takabayashi M (2009) Diazotrophic bacteria associated with Hawaiian Montipora corals: diversity and abundance in correlation with symbiotic dinoflagellates.Journal of Experimental Marine Biology and Ecology, 371, 140-146.
73	Penton CR, Devol AH, Tiedje JM (2006) Molecular evidence for the broad distribution of anaerobic ammonium-oxidizing bacteria in freshwater and marine sediments.Applied and Environmental Microbiology, 72, 6829-6832.
74	Philippot L (2002) Denitrifying genes in bacterial and archaeal genomes.Biochimica et Biophysica Acta, 1557, 355-376.
75	Prieme A, Braker G, Tiedje JM (2002) Diversity of nitrite reductase (nirK and nirS) gene fragments in forested upland and wetland soils.Applied and Environmental Microbiology, 68, 1893-1924.
76	Prosser JI, Nicol GW (2008) Relative contributions of archaea and bacteria to aerobic ammonia oxidation in the environment.Environmental Microbiology, 10, 2931-2941.
77	Ravikumar S, Kathiresan K, Ignatiammal STM, Selvam MB, Shanthy S (2004) Nitrogen-fixing azotobacters from mangrove habitat and their utility as marine biofertilizers.Journal of Experimental Marine Biology and Ecology, 312, 5-17.
78	Raymond J, Siefert JL, Staples CR, Blankenship RE (2004) The natural history of nitrogen fixation.Molecular Biology and Evolution, 21, 541-554.
113	Zumft WG (1997) Cell biology and molecular basis of denitrification.Microbiology and Molecular Biology Reviews, 61, 533-616.

生境 Habitat	nifH分类(子类) nifH-based cluster (subcluster)	16S rRNA系统地位 Classification based on 16S rRNA gene	代表属 Representative genus	参考文献 Reference
潮间带微生物席/蓝细菌席Intertidal microbial/cyanobacterial mats	I (E) I (E) I (J) III (E) III (E)	Cyanobacteria γ-Proteobacteria α-Proteobacteria δ-Proteobacteria Fimicutes	Lyngbya Azotobacter Rhizobium Desulfovibrio Clostridium	Zehr et al., 1995 Steppe & Paerl, 2005
河口沉积物 Estuarine sediment	I (E) I (I) III (E) III (A)	γ-Proteobacteria γ-Proteobacteria δ-Proteobacteria Firmicutes	Azotobacter Klebsiella Desulfovibrio Clostridium	Burns et al., 2002 Herbert, 1999 Jones, 1982
盐沼植物根际 Rhizosphere in salt marsh	I (I) I (H) I (J) I (E) I (H) I (J) I (U)	γ-Proteobacteria γ-Proteobacteria α-Proteobacteria γ-Proteobacteria γ-Proteobacteria α-Proteobacteria γ-Proteobacteria	Enterobacter Spirilla Rhizobium Azotobacter Vibrio Azospirillum Psuedomonas	Bergholz et al., 2001 Lovell et al., 2001
海草(藻)根际 Rhizosphere of seagrass and seaweed	I (I) I (E) III (A) III (E)	γ-Proteobacteria γ-Proteobacteria Firmicutes δ-Proteobacteria	Rhizobium Azotobacter Clostridium Desulfomicrobium Desulfovibrio	Kirshtein et al., 1991 Smith et al., 2004 Achá et al., 2005
红树林根际 Rhizosphere of mangrove plants	I (I) I (E) III (A) I (J) I (I)	γ-Proteobacteria γ-Proteobacteria Firmicutes α-Proteobacteria γ-Proteobacteria	Rhizobium Azotobacter Clostridium Azospirillum Klebsiella	Thatoi et al., 2013
珊瑚礁区沉积物/珊瑚虫体 Sediment in coral reef environments/coral endosymbiot	I I (H) I (J) III (A)	Cyanobacteria γ-Proteobacteria α-Proteobacteria Firmicutes	Coccoid Vibrio Rhodobacter Clostridium	Olson et al., 2009 Rohwer et al., 2002

生境 Habitat	nifH分类(子类) nifH-based cluster (subcluster)	16S rRNA系统地位 Classification based on 16S rRNA gene	代表属 Representative genus	参考文献 Reference
潮间带微生物席/蓝细菌席Intertidal microbial/cyanobacterial mats	I (E) I (E) I (J) III (E) III (E)	Cyanobacteria γ-Proteobacteria α-Proteobacteria δ-Proteobacteria Fimicutes	Lyngbya Azotobacter Rhizobium Desulfovibrio Clostridium	Zehr et al., 1995 Steppe & Paerl, 2005
河口沉积物 Estuarine sediment	I (E) I (I) III (E) III (A)	γ-Proteobacteria γ-Proteobacteria δ-Proteobacteria Firmicutes	Azotobacter Klebsiella Desulfovibrio Clostridium	Burns et al., 2002 Herbert, 1999 Jones, 1982
盐沼植物根际 Rhizosphere in salt marsh	I (I) I (H) I (J) I (E) I (H) I (J) I (U)	γ-Proteobacteria γ-Proteobacteria α-Proteobacteria γ-Proteobacteria γ-Proteobacteria α-Proteobacteria γ-Proteobacteria	Enterobacter Spirilla Rhizobium Azotobacter Vibrio Azospirillum Psuedomonas	Bergholz et al., 2001 Lovell et al., 2001
海草(藻)根际 Rhizosphere of seagrass and seaweed	I (I) I (E) III (A) III (E)	γ-Proteobacteria γ-Proteobacteria Firmicutes δ-Proteobacteria	Rhizobium Azotobacter Clostridium Desulfomicrobium Desulfovibrio	Kirshtein et al., 1991 Smith et al., 2004 Achá et al., 2005
红树林根际 Rhizosphere of mangrove plants	I (I) I (E) III (A) I (J) I (I)	γ-Proteobacteria γ-Proteobacteria Firmicutes α-Proteobacteria γ-Proteobacteria	Rhizobium Azotobacter Clostridium Azospirillum Klebsiella	Thatoi et al., 2013
珊瑚礁区沉积物/珊瑚虫体 Sediment in coral reef environments/coral endosymbiot	I I (H) I (J) III (A)	Cyanobacteria γ-Proteobacteria α-Proteobacteria Firmicutes	Coccoid Vibrio Rhodobacter Clostridium	Olson et al., 2009 Rohwer et al., 2002

[1]	Kexin Cao, Jingwen Wang, Guo Zheng, Pengfeng Wu, Yingbin Li, Shuyan Cui. Effects of precipitation regime change and nitrogen deposition on soil nematode diversity in the grassland of northern China [J]. Biodiv Sci, 2024, 32(3): 23491-.
[2]	Yasu Cao, Min Fan, Yu Peng, Jiaxun Xin, Nanyi Peng. Effects of landscape pattern dynamics on plant species and functional diversity in Hunshandak Sandland [J]. Biodiv Sci, 2023, 31(8): 23048-.
[3]	Fayang Li, Yingyu Li, Wenni Jiang, Shuguang Liu, Chao Huo, Qiaoqi Sun, Hongfei Zou. How forest fires affect bird diversity over time in boreal forest interiors and edges in the Greater Khingan Mountains [J]. Biodiv Sci, 2023, 31(7): 22665-.
[4]	Xiaocheng Chen, Pengzhan Zhang, Bin Kang, Linshan Liu, Liang Zhao. Species and functional diversity of the passerine birds in the Tibetan Plateau based on specimens from the collection of Northwest Institute of Plateau Biology, Chinese Academy of Sciences [J]. Biodiv Sci, 2023, 31(5): 22638-.
[5]	Yuanyuan Xiao, Wei Feng, Yangui Qiao, Yuqing Zhang, Shugao Qin. Effects of soil microbial community characteristics on soil multifunctionality in sand-fixation shrublands [J]. Biodiv Sci, 2023, 31(4): 22585-.
[6]	Xinyang Zhou, Yutao Wang, Jianping Li. Response of plant community composition to precipitation changes in typical grasslands in the Loess Plateau [J]. Biodiv Sci, 2023, 31(3): 22118-.
[7]	Wei Zhang, Dongdong Zhai, Fei Xiong, Hongyan Liu, Yuanyuan Chen, Ying Wang, Chuansong Liao, Xinbin Duan, Huiwu Tian, Huatang Deng, Daqing Chen. Community structure and functional diversity of fishes in the Three Gorges Reservoir [J]. Biodiv Sci, 2023, 31(2): 22136-.
[8]	Wang Chaoya, Li Jintao, Liu Chang, Wang Bo, Miao Baige, Peng Yanqiong. Interannual stability in butterfly diversity and the larvae-plant interaction network structure at Xishuangbanna Tropical Botanical Garden [J]. Biodiv Sci, 2023, 31(12): 23305-.
[9]	Jinhua Liu, Feng Li, Tao Tian, Haifeng Xiao. Response of soil bacteria and nematodes to litter identity and diversity of dominant plants in a tropical rainforest [J]. Biodiv Sci, 2023, 31(11): 23276-.
[10]	Caifang Luo, Tao Yang, Qiuyu Zhang, Xinpei Wang, Zehao Shen. Plant functional traits, community functional diversity and their environmental determinants of the semi-humid evergreen broad-leaved forest in the Central Yunnan Plateau [J]. Biodiv Sci, 2023, 31(11): 23215-.
[11]	Chao Zhang, Juan Li, Haiyun Cheng, Jiachong Duan, Zhao Pan. Patterns and environmental drivers of the butterfly diversity in the western region of Qinling Mountains [J]. Biodiv Sci, 2023, 31(1): 22272-.
[12]	Xiaoyan Jiang, Shengjie Gao, Yan Jiang, Yun Tian, Xin Jia, Tianshan Zha. Species diversity, functional diversity, and phylogenetic diversity in plant communities at different phases of vegetation restoration in the Mu Us sandy grassland [J]. Biodiv Sci, 2022, 30(5): 21387-.
[13]	Xiaotong Liu, Yijia Tian, Hanwen Liu, Cuiying Liang, Siwei Jiang, Wenju Liang, Xiaoke Zhang. Seasonal variation in cropland soil nematode community composition in the lower reaches of Liaohe Plain [J]. Biodiv Sci, 2022, 30(12): 22222-.
[14]	Qiuju Chen, Zhixian Sun, Xuejian Li, Rui Zhang, Rui Xi, Chen Tian, Xin Wang, Yingchun Xing, Yahui Zhao. Fish diversity of Wuyishan National Park and its adjacent areas [J]. Biodiv Sci, 2022, 30(11): 22260-.
[15]	Yu Ren, Shengli Tao, Tianyu Hu, Haitao Yang, Hongcan Guan, Yanjun Su, Kai Cheng, Mengxi Chen, Huawei Wan, Qinghua Guo. The outlook and system construction for monitoring Essential Biodiversity Variables based on remote sensing: The case of China [J]. Biodiv Sci, 2022, 30(10): 22530-.