The Shifts of Diazotrophic Communities in Spring and Summer Associated with Coral Galaxea astreata, Pavona decussata, and Porites lutea

Zhang, Yanying; Yang, Qingsong; Ling, Juan; Van Nostrand, Joy D.; Shi, Zhou; Zhou, Jizhong; Dong, Junde

doi:10.3389/fmicb.2016.01870

The Shifts of Diazotrophic Communities in Spring and Summer Associated with Coral Galaxea astreata, Pavona decussata, and Porites lutea

Journal Article · Tue Nov 22 00:00:00 EST 2016 · Frontiers in Microbiology

DOI:https://doi.org/10.3389/fmicb.2016.01870· OSTI ID:1506261

Zhang, Yanying ^[1]; Yang, Qingsong ^[2]; Ling, Juan ^[2]; Van Nostrand, Joy D. ^[3]; Shi, Zhou ^[3]; Zhou, Jizhong ^[3]; Dong, Junde ^[4]

Chinese Academy of Sciences, Guangzhou (China); Chinese Academy of Sciences, Sanya (China); Univ. of Oklahoma, Norman, OK (United States)
Chinese Academy of Sciences, Guangzhou (China)
Univ. of Oklahoma, Norman, OK (United States)
Chinese Academy of Sciences, Guangzhou (China); Chinese Academy of Sciences, Sanya (China)

The coral holobiont often resides in oligotrophic waters; both coral cells and their symbiotic dinoflagellates possess ammonium assimilation enzymes and potentially benefit from the nitrogen fixation of coral-associated diazotrophs. However, the seasonal dynamics of coral-associated diazotrophs are not well characterized. Here, the seasonal variations of diazotrophic communities associated with three corals, Galaxea astreata, Pavona decussata, and Porites lutea, were studied using nifH gene amplicon pyrosequencing techniques. Our results revealed a great diversity of coral-associated diazotrophs. nifH sequences related to Alphaproteobacteria, Deltaproteobacteria, and Gammaproteobacteria were ubiquitous and dominant in all corals in two seasons. In contrast with the coral P. decussata, both G. astreata and P. lutea showed significant seasonal changes in the diazotrophic communities and nifH gene abundance. Variable diazotroph groups accounted for a range from 11 to 49% within individual coral samples. Most of the variable diazotrophic groups from P. decussata were species-specific, however, the majority of overlapping variable groups in G. astreata and P. lutea showed the same seasonal variation characteristics. Rhodopseudomonas palustris- and Gluconacetobacter diazotrophicus-affiliated sequences were relatively abundant in the summer, whereas a nifH sequence related to Halorhodospira halophila was relatively abundant in spring G. astreata and P. lutea. The seasonal variations of all diazotrophic communities were significantly correlated with the seasonal shifts of ammonium and nitrate, suggesting that diazotrophs play an important role in the nitrogen cycle of the coral holobiont.

View Accepted Manuscript (DOE)

Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC)

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1506261

Journal Information:: Frontiers in Microbiology, Journal Name: Frontiers in Microbiology Journal Issue: NOV Vol. 7; ISSN 1664-302X

Publisher:: Frontiers Research FoundationCopyright Statement

Country of Publication:: United States

Language:: English

References (69)

Benthic N ₂ fixation in coral reefs and the potential effects of human-induced environmental change Cardini, Ulisse; Bednarz, Vanessa N.; Foster, Rachel A. Ecology and Evolution, Vol. 4, Issue 9 https://doi.org/10.1002/ece3.1050	journal	March 2014
Nitrogen fixation (acetylene reduction) associated with the living coral Acropora variabilis Williams, W. M.; Viner, A. B.; Broughton, W. J. Marine Biology, Vol. 94, Issue 4 https://doi.org/10.1007/bf00431399	journal	January 1987
Availability of two forms of dissolved nitrogen to the coral Pocillopora damicornis and its symbiotic zooxanthellae Hoegh-Guldberg, O.; Williamson, J. Marine Biology, Vol. 133, Issue 3 https://doi.org/10.1007/s002270050496	journal	April 1999
Microbiota of the Major South Atlantic Reef Building Coral Mussismilia Fernando, Samodha C.; Wang, Jia; Sparling, Kimberly Microbial Ecology, Vol. 69, Issue 2 https://doi.org/10.1007/s00248-014-0474-6	journal	September 2014
Biological and chemical characteristics of the coral gastric cavity Agostini, S.; Suzuki, Y.; Higuchi, T. Coral Reefs, Vol. 31, Issue 1 https://doi.org/10.1007/s00338-011-0831-6	journal	October 2011
Nitrogenase proteins from Gluconacetobacter diazotrophicus, a sugarcane-colonizing bacterium Fisher, Karl; Newton, William E. Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics, Vol. 1750, Issue 2 https://doi.org/10.1016/j.bbapap.2005.04.010	journal	June 2005
Recent advances in nitrogen-fixing acetic acid bacteria Pedraza, Raúl O. International Journal of Food Microbiology, Vol. 125, Issue 1 https://doi.org/10.1016/j.ijfoodmicro.2007.11.079	journal	June 2008
Diazotrophic bacteria associated with Hawaiian Montipora corals: Diversity and abundance in correlation with symbiotic dinoflagellates Olson, N. D.; Ainsworth, T. D.; Gates, R. D. Journal of Experimental Marine Biology and Ecology, Vol. 371, Issue 2 https://doi.org/10.1016/j.jembe.2009.01.012	journal	April 2009
Vibrios dominate as culturable nitrogen-fixing bacteria of the Brazilian coral Mussismilia hispida Chimetto, Luciane A.; Brocchi, Marcelo; Thompson, Cristiane C. Systematic and Applied Microbiology, Vol. 31, Issue 4 https://doi.org/10.1016/j.syapm.2008.06.001	journal	September 2008
Nitrogen cycling in corals: the key to understanding holobiont functioning? Rädecker, Nils; Pogoreutz, Claudia; Voolstra, Christian R. Trends in Microbiology, Vol. 23, Issue 8 https://doi.org/10.1016/j.tim.2015.03.008	journal	August 2015
The future of coral reefs: a microbial perspective Ainsworth, Tracy D.; Thurber, Rebecca Vega; Gates, Ruth D. Trends in Ecology & Evolution, Vol. 25, Issue 4 https://doi.org/10.1016/j.tree.2009.11.001	journal	April 2010
Btrim: A fast, lightweight adapter and quality trimming program for next-generation sequencing technologies Kong, Yong Genomics, Vol. 98, Issue 2 https://doi.org/10.1016/j.ygeno.2011.05.009	journal	August 2011
Improvement in the RFLP procedure for studying the diversity of nifH genes in communities of nitrogen fixers in soil Poly, Franck; Monrozier, Lucile Jocteur; Bally, René Research in Microbiology, Vol. 152, Issue 1 https://doi.org/10.1016/s0923-2508(00)01172-4	journal	January 2001
Bacterial diversity and White Plague Disease-associated community changes in the Caribbean coral Montastraea faveolata Sunagawa, Shinichi; DeSantis, Todd Z.; Piceno, Yvette M. The ISME Journal, Vol. 3, Issue 5 https://doi.org/10.1038/ismej.2008.131	journal	January 2009
The dynamics of microbial partnerships in the coral Isopora palifera Chen, Chung-Pin; Tseng, Ching-Hung; Chen, Chaolun A. The ISME Journal, Vol. 5, Issue 4 https://doi.org/10.1038/ismej.2010.151	journal	October 2010
A single-cell view of ammonium assimilation in coral–dinoflagellate symbiosis Pernice, Mathieu; Meibom, Anders; Van Den Heuvel, Annamieke The ISME Journal, Vol. 6, Issue 7 https://doi.org/10.1038/ismej.2011.196	journal	January 2012
Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms Caporaso, J. Gregory; Lauber, Christian L.; Walters, William A. The ISME Journal, Vol. 6, Issue 8 https://doi.org/10.1038/ismej.2012.8	journal	March 2012
Climate change affects key nitrogen-fixing bacterial populations on coral reefs Santos, Henrique F.; Carmo, Flávia L.; Duarte, Gustavo The ISME Journal, Vol. 8, Issue 11 https://doi.org/10.1038/ismej.2014.70	journal	May 2014
The coral core microbiome identifies rare bacterial taxa as ubiquitous endosymbionts D. Ainsworth, Tracy; Krause, Lutz; Bridge, Thomas The ISME Journal, Vol. 9, Issue 10 https://doi.org/10.1038/ismej.2015.39	journal	April 2015
Complete genome sequence of the metabolically versatile photosynthetic bacterium Rhodopseudomonas palustris Larimer, Frank W; Chain, Patrick; Hauser, Loren Nature Biotechnology, Vol. 22, Issue 1, p. 55-61 https://doi.org/10.1038/nbt923	journal	December 2003
Global microbialization of coral reefs Haas, Andreas F.; Fairoz, Mohamed F. M.; Kelly, Linda W. Nature Microbiology, Vol. 1, Issue 6 https://doi.org/10.1038/nmicrobiol.2016.42	journal	April 2016
Horizontal gene transfer enables programmable gene stability in synthetic microbiota Wang, Teng; Weiss, Andrea; Aqeel, Ammara Nature Chemical Biology, Vol. 18, Issue 11 https://doi.org/10.1038/s41589-022-01114-3	journal	September 2022
The functional gene composition and metabolic potential of coral-associated microbial communities Zhang, Yanying; Ling, Juan; Yang, Qingsong Scientific Reports, Vol. 5, Issue 1 https://doi.org/10.1038/srep16191	journal	November 2015
Nitrogenase gene diversity and microbial community structure: a cross-system comparison Zehr, Jonathan P.; Jenkins, Bethany D.; Short, Steven M. Environmental Microbiology, Vol. 5, Issue 7 https://doi.org/10.1046/j.1462-2920.2003.00451.x	journal	July 2003
Local genomic adaptation of coral reef-associated microbiomes to gradients of natural variability and anthropogenic stressors Kelly, L. W.; Williams, G. J.; Barott, K. L. Proceedings of the National Academy of Sciences, Vol. 111, Issue 28 https://doi.org/10.1073/pnas.1403319111	journal	June 2014
Coral-Associated Bacterial Assemblages: Current Knowledge and the Potential for Climate-Driven Impacts Mouchka, Morgan E.; Hewson, Ian; Harvell, C. Drew Integrative and Comparative Biology, Vol. 50, Issue 4 https://doi.org/10.1093/icb/icq061	journal	June 2010
Longitudinal variability of diazotroph abundances in the subtropical North Atlantic Ocean Benavides, Mar; Moisander, Pia H.; Daley, Meaghan C. Journal of Plankton Research, Vol. 38, Issue 3 https://doi.org/10.1093/plankt/fbv121	journal	January 2016
Amplicon pyrosequencing reveals spatial and temporal consistency in diazotroph assemblages of the A cropora millepora microbiome : Diazotroph communities associated with the coral Lema, Kimberley A.; Willis, Bette L.; Bourne, David G. Environmental Microbiology, Vol. 16, Issue 10 https://doi.org/10.1111/1462-2920.12366	journal	January 2014
Physiology and dinitrogen fixation of Acetobacter diazotrophicus Stephan, M. P.; Oliveira, M.; Teixeira, K. R. S. FEMS Microbiology Letters, Vol. 77, Issue 1 https://doi.org/10.1111/j.1574-6968.1991.tb04323.x	journal	January 1991
Onset and establishment of diazotrophs and other bacterial associates in the early life history stages of the coral Acropora millepora Lema, Kimberley A.; Bourne, David G.; Willis, Bette L. Molecular Ecology, Vol. 23, Issue 19 https://doi.org/10.1111/mec.12899	journal	September 2014
Nitrogen Fixation in a Coral Reef Community Wiebe, W. J.; Johannes, R. E.; Webb, K. L. Science, Vol. 188, Issue 4185 https://doi.org/10.1126/science.188.4185.257	journal	April 1975
Molecular Detection and Ecological Significance of the Cyanobacterial Genera Geitlerinema and Leptolyngbya in Black Band Disease of Corals Myers, J. L.; Sekar, R.; Richardson, L. L. Applied and Environmental Microbiology, Vol. 73, Issue 16 https://doi.org/10.1128/aem.00900-07	journal	June 2007
Elevated Carbon Dioxide Alters the Structure of Soil Microbial Communities Deng, Ye; He, Zhili; Xu, Meiying Applied and Environmental Microbiology, Vol. 78, Issue 8 https://doi.org/10.1128/aem.06924-11	journal	February 2012
Characterization of Geographically Distinct Bacterial Communities Associated with Coral Mucus Produced by Acropora spp. and Porites spp. McKew, B. A.; Dumbrell, A. J.; Daud, S. D. Applied and Environmental Microbiology, Vol. 78, Issue 15 https://doi.org/10.1128/aem.07764-11	journal	May 2012
Cyanobacteria Associated with Coral Black Band Disease in Caribbean and Indo-Pacific Reefs Frias-Lopez, J.; Bonheyo, G. T.; Jin, Q. Applied and Environmental Microbiology, Vol. 69, Issue 4 https://doi.org/10.1128/aem.69.4.2409-2413.2003	journal	April 2003
Biology of Pseudomonas stutzeri Lalucat, J.; Bennasar, A.; Bosch, R. Microbiology and Molecular Biology Reviews, Vol. 70, Issue 2 https://doi.org/10.1128/mmbr.00047-05	journal	June 2006
Research Progress and Perspectives of Nitrogen Fixing Bacterium, Gluconacetobacter diazotrophicus , in Monocot Plants Eskin, N.; Vessey, K.; Tian, L. International Journal of Agronomy, Vol. 2014 https://doi.org/10.1155/2014/208383	journal	January 2014
Nitrogen fixation in the mucus of Red Sea corals Grover, R.; Ferrier-Pages, C.; Maguer, J. -F. Journal of Experimental Biology, Vol. 217, Issue 22 https://doi.org/10.1242/jeb.111591	journal	October 2014
Threatened Corals Provide Underexplored Microbial Habitats Sunagawa, Shinichi; Woodley, Cheryl M.; Medina, Mónica PLoS ONE, Vol. 5, Issue 3 https://doi.org/10.1371/journal.pone.0009554	journal	March 2010
A Comprehensive Evaluation of PCR Primers to Amplify the nifH Gene of Nitrogenase Gaby, John Christian; Buckley, Daniel H. PLoS ONE, Vol. 7, Issue 7 https://doi.org/10.1371/journal.pone.0042149	journal	July 2012
Assessing Coral Reefs on a Pacific-Wide Scale Using the Microbialization Score McDole, Tracey; Nulton, James; Barott, Katie L. PLoS ONE, Vol. 7, Issue 9 https://doi.org/10.1371/journal.pone.0043233	journal	September 2012
Released coral mucus does not enhance planktonic N2 fixation rates Camps, M.; Benavides, M.; Lema, Ka Aquatic Microbial Ecology, Vol. 77, Issue 1 https://doi.org/10.3354/ame01787	journal	July 2016
Nitrogen fixation by symbiotic cyanobacteria provides a source of nitrogen for the scleractinian coral Montastraea cavernosa Lesser, Mp; Falcón, Li; Rodríguez-Román, A. Marine Ecology Progress Series, Vol. 346 https://doi.org/10.3354/meps07008	journal	September 2007
Ocean acidification rapidly reduces dinitrogen fixation associated with the hermatypic coral Seriatopora hystrix Rädecker, N.; Meyer, Fw; Bednarz, Vn Marine Ecology Progress Series, Vol. 511 https://doi.org/10.3354/meps10912	journal	September 2014
Nitrogen fixation (acetylene reduction) in stony corals: evidence for coral-bacteria interactions Shashar, N.; Cohen, Y.; Loya, Y. Marine Ecology Progress Series, Vol. 111 https://doi.org/10.3354/meps111259	journal	January 1994
Microenvironment and photosynthesis of zooxanthellae in scleractinian corals studied with microsensors for O2, pH and light Kühl, M.; Cohen, Y.; Dalsgaard, T. Marine Ecology Progress Series, Vol. 117 https://doi.org/10.3354/meps117159	journal	January 1995
Diversity and distribution of coral-associated bacteria Rohwer, F.; Seguritan, V.; Azam, F. Marine Ecology Progress Series, Vol. 243 https://doi.org/10.3354/meps243001	journal	January 2002
Microbes in the coral holobiont: partners through evolution, development, and ecological interactions Thompson, Janelle R.; Rivera, Hanny E.; Closek, Collin J. Frontiers in Cellular and Infection Microbiology, Vol. 4 https://doi.org/10.3389/fcimb.2014.00176	journal	January 2015
Nitrogen fixation (acetylene reduction) on a coral reef Shashar, N.; Feldstein, T.; Cohen, Y. Coral Reefs, Vol. 13, Issue 3 https://doi.org/10.1007/BF00301195	journal	July 1994
Nitrogen fixation (acetylene reduction) associated with macroalgae in a coral-reef community in the Bahamas Capone, D. G.; Taylor, D. L.; Taylor, B. F. Marine Biology, Vol. 40, Issue 1 https://doi.org/10.1007/BF00390624	journal	January 1977
Nitrogen fixation (acetylene reduction) associated with the living coral Acropora variabilis Williams, W. M.; Viner, A. B.; Broughton, W. J. Marine Biology, Vol. 94, Issue 4 https://doi.org/10.1007/BF00431399	journal	January 1987
The status of the ecological environment and a proposed protection strategy in Sanya Bay, Hainan Island, China Huang, Liangmin; Tan, Yehui; Song, Xingyu Marine Pollution Bulletin, Vol. 47, Issue 1-6 https://doi.org/10.1016/S0025-326X(03)00070-5	journal	January 2003
Ecological physiology of the black band disease cyanobacterium Phormidium corallyticum Richardson, Laurie L.; Kuta, Kevin G. FEMS Microbiology Ecology, Vol. 43, Issue 3 https://doi.org/10.1016/S0168-6496(03)00025-4	journal	April 2003
Improvement in the RFLP procedure for studying the diversity of nifH genes in communities of nitrogen fixers in soil Poly, Franck; Monrozier, Lucile Jocteur; Bally, René Research in Microbiology, Vol. 152, Issue 1 https://doi.org/10.1016/S0923-2508(00)01172-4	journal	January 2001
Influence of human activity and monsoon dynamics on spatial and temporal hydrochemistry in tropical coastal waters (Sanya Bay, South China Sea) Wu, Mei-Lin; Ling, Juan; Long, Li-Juan Chemistry and Ecology, Vol. 28, Issue 4 https://doi.org/10.1080/02757540.2011.650167	journal	August 2012
FLASH: fast length adjustment of short reads to improve genome assemblies Magoc, T.; Salzberg, S. L. Bioinformatics, Vol. 27, Issue 21 https://doi.org/10.1093/bioinformatics/btr507	journal	September 2011
Thiorhodospira sibirica gen. nov., sp. nov., a new alkaliphilic purple sulfur bacterium from a Siberian soda lake Bryantseva, I.; Gorlenko, V. M.; Kompantseva, E. I. International Journal of Systematic Bacteriology, Vol. 49, Issue 2 https://doi.org/10.1099/00207713-49-2-697	journal	April 1999
Coral-associated bacterial communities on Ningaloo Reef, Western Australia: Coral bacterial communities, Ningaloo Reef Ceh, Janja; Van Keulen, Mike; Bourne, David G. FEMS Microbiology Ecology, Vol. 75, Issue 1 https://doi.org/10.1111/j.1574-6941.2010.00986.x	journal	November 2010
Molecular Detection and Ecological Significance of the Cyanobacterial Genera Geitlerinema and Leptolyngbya in Black Band Disease of Corals Myers, J. L.; Sekar, R.; Richardson, L. L. Applied and Environmental Microbiology, Vol. 73, Issue 16 https://doi.org/10.1128/AEM.00900-07	journal	June 2007
Spatial and Species Variations in Bacterial Communities Associated with Corals from the Red Sea as Revealed by Pyrosequencing Lee, On On; Yang, Jiangke; Bougouffa, Salim Applied and Environmental Microbiology, Vol. 78, Issue 20 https://doi.org/10.1128/AEM.01111-12	journal	August 2012
Elevated Carbon Dioxide Alters the Structure of Soil Microbial Communities Deng, Ye; He, Zhili; Xu, Meiying Applied and Environmental Microbiology, Vol. 78, Issue 8 https://doi.org/10.1128/AEM.06924-11	journal	February 2012
Characterization of Geographically Distinct Bacterial Communities Associated with Coral Mucus Produced by Acropora spp. and Porites spp. McKew, B. A.; Dumbrell, A. J.; Daud, S. D. Applied and Environmental Microbiology, Vol. 78, Issue 15 https://doi.org/10.1128/AEM.07764-11	journal	May 2012
Corals Form Characteristic Associations with Symbiotic Nitrogen-Fixing Bacteria Lema, Kimberley A.; Willis, Bette L.; Bourne, David G. Applied and Environmental Microbiology, Vol. 78, Issue 9 https://doi.org/10.1128/AEM.07800-11	journal	February 2012
Cyanobacteria Associated with Coral Black Band Disease in Caribbean and Indo-Pacific Reefs Frias-Lopez, J.; Bonheyo, G. T.; Jin, Q. Applied and Environmental Microbiology, Vol. 69, Issue 4 https://doi.org/10.1128/AEM.69.4.2409-2413.2003	journal	April 2003
Biology of Pseudomonas stutzeri Lalucat, J.; Bennasar, A.; Bosch, R. Microbiology and Molecular Biology Reviews, Vol. 70, Issue 2 https://doi.org/10.1128/MMBR.00047-05	journal	June 2006
Ecological Patterns of nifH Genes in Four Terrestrial Climatic Zones Explored with Targeted Metagenomics Using FrameBot, a New Informatics Tool Wang, Qiong; Quensen, John F.; Fish, Jordan A. mBio, Vol. 4, Issue 5 https://doi.org/10.1128/mBio.00592-13	journal	September 2013
Cloning and characterization of nif structural and regulatory genes in the purple sulfur bacterium, Halorhodospira halophila Tsuihiji, Hisayoshi; Yamazaki, Yoichi; Kamikubo, Hironari Journal of Bioscience and Bioengineering, Vol. 101, Issue 3 https://doi.org/10.1263/jbb.101.263	journal	March 2006
Ocean acidification rapidly reduces dinitrogen fixation associated with the hermatypic coral Seriatopora hystrix Rädecker, Nils; Meyer, Friedrich Wilhelm; Bednarz, Vanessa N. PANGAEA https://doi.org/10.1594/pangaea.843730	dataset	January 2014
Phytoplankton distribution and their relationship to environmental variables in Sanya Bay, South China Sea [Phytoplankton distribution and their relationship to environmental variables in Sanya Bay, South China Sea] Zhang, Yanying; Dong, Junde; Ling, Juan Scientia Marina, Vol. 74, Issue 4 https://doi.org/10.3989/scimar.2010.74n4783	journal	July 2010

Cited By (3)

Analysis of nifH DNA and RNA reveals a disproportionate contribution to nitrogenase activities by rare plankton-associated diazotrophs Yang, Qingsong; Dong, Junde; Ahmad, Manzoor BMC Microbiology https://doi.org/10.21203/rs.2.9602/v1	journal	August 2019
Diversity and Activity of Diazotrophs in Great Barrier Reef Surface Waters Messer, Lauren F.; Brown, Mark V.; Furnas, Miles J. Frontiers in Microbiology, Vol. 8 https://doi.org/10.3389/fmicb.2017.00967	journal	June 2017
Season structures prokaryotic partners but not algal symbionts in subtropical hard corals Cai, Lin; Zhou, Guowei; Tong, Haoya Applied Microbiology and Biotechnology, Vol. 102, Issue 11 https://doi.org/10.1007/s00253-018-8909-5	journal	April 2018

Similar Records

Diversity and Structure of Diazotrophic Communities in Mangrove Rhizosphere, Revealed by High-Throughput Sequencing

Journal Article · Tue Oct 17 20:00:00 EDT 2017 · Frontiers in Microbiology · OSTI ID:1479338

Response of Biological Soil Crust Diazotrophs to Season, Altered Summer Precipitation, and Year-Round Increased Temperature in an Arid Grassland of the Colorado Plateau, USA

Journal Article · Sat Dec 31 19:00:00 EST 2011 · Frontiers in Microbiology · OSTI ID:1396109

Metagenomic insights into diazotrophic communities across Arctic glacier forefields

Journal Article · Mon Jun 11 20:00:00 EDT 2018 · FEMS Microbiology Ecology (Online) · OSTI ID:1461009

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
coral reef
diazotrophs
diversity
nifH
pyrosequencing

The Shifts of Diazotrophic Communities in Spring and Summer Associated with Coral Galaxea astreata, Pavona decussata, and Porites lutea

Citation Formats

References (69)

Cited By (3)

Similar Records

Related Subjects