Re-evaluation of the diversity and distribution of diazotrophs in the South China Sea by pyrosequencing the nifH gene
Peng Xiao A D , Yongguang Jiang B , Yang Liu A , Wenhua Tan C , Wenhua Li A D and Renhui Li A E
+ Author Affiliations
- Author Affiliations
A Key Laboratory of Algal Biology, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan, 430072, P. R. China.
B Shenzhen Key Laboratory for Marine Bio-resource and Eco-environment, College of Life Sciences, Shenzhen University, Shenzhen 518060, P. R. China.
C Department of Bioorganic Chemistry, Max Planck Institute for Chemical Ecology, Hans-Knöll-Straβe 8, D-07745 Jena, Germany.
D Present addres: University of Chinese Academy of Sciences, Beijing, 100049, P. R. China.
E Corresponding author. Email: reli@ihb.ac.cn
Marine and Freshwater Research 66(8) 681-691 https://doi.org/10.1071/MF14134
Submitted: 15 May 2014 Accepted: 29 July 2014 Published: 25 February 2015
Abstract
Previous studies on the diversity and composition of nifH genes in the South China Sea (SCS) were mainly based on quantitative PCR and DNA clone methods. The pyrosequencing results of partial nifH gene fragments were used to study the spatiotemporal heterogeneity in composition and diversity of diazotrophs in the SCS. Seawater samples were collected throughout the upper ocean (<200-m depth) in different sites, as follows: the Pearl River Estuary; Taiwan and Luzon Straits (which are affected by the Kuroshio Current); a Trichodesmium bloom site; and two open ocean sites. Sample collection was conducted in four surveys from 2007 to 2010. A large dataset containing 217 599 nifH reads from 27 samples was obtained. Putative diazotrophs in the SCS have reasonably low diversities, and the γ-proteobacteria and Trichodesmium were the two dominant nifH phylogenetic groups. No significant difference was observed among different regions and years. However, a significant difference existed among the samples obtained from different water depths. The results provide a broad and general view of the diversity and composition of the putative diazotrophs in the SCS.
Additional keywords: biodiversity, microorganism.
References
Acinas, S. G., Haverkamp, T. H., Huisman, J., and Stal, L. J. (2009). Phenotypic and genetic diversification of Pseudanabaena spp. (cyanobacteria). The ISME Journal 3, 31–46.| Phenotypic and genetic diversification of Pseudanabaena spp. (cyanobacteria).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXms12gsbc%3D&md5=861271997995f42bd3725eddd5f006a9CAS | 18769459PubMed |
Andersson, A. F., Lindberg, M., Jakobsson, H., Bäckhed, F., Nyrén, P., and Engstrand, L. (2008). Comparative analysis of human gut microbiota by barcoded pyrosequencing. PLoS ONE 3, e2836.
| Comparative analysis of human gut microbiota by barcoded pyrosequencing.Crossref | GoogleScholarGoogle Scholar | 18665274PubMed |
Bombar, D., Moisander, P. H., Dippner, J. W., Foster, R. A., Voss, M., Karfeld, B., and Zehr, J. P. (2011). Distribution of diazotrophic microorganisms and nifH gene expression in the Mekong River plume during intermonsoon. Marine Ecology Progress Series 424, 39–52.
| Distribution of diazotrophic microorganisms and nifH gene expression in the Mekong River plume during intermonsoon.Crossref | GoogleScholarGoogle Scholar |
Bombar, D., Turk-Kubo, K. A., Robidart, J., Carter, B. J., and Zehr, J. P. (2013). Non-cyanobacterial nifH phylotypes in the North Pacific Subtropical Gyre detected by flow-cytometry cell sorting. Environmental Microbiology Reports 5, 705–715.
| 1:CAS:528:DC%2BC3sXhsF2gsLvO&md5=103b8e31e3580b38cec6442f5528c225CAS | 24115621PubMed |
Boström, K. H., Riemann, L., Zweifel, U. L., and Hagström, Å. (2007). Nodularia sp. nifH gene transcripts in the Baltic Sea proper. Journal of Plankton Research 29, 391–399.
| Nodularia sp. nifH gene transcripts in the Baltic Sea proper.Crossref | GoogleScholarGoogle Scholar |
Braun, S., Proctor, L., Zani, S., Mellon, M., and Zehr, J. (1999). Molecular evidence for zooplankton-associated nitrogen-fixing anaerobes based on amplification of the nifH gene. FEMS Microbiology Ecology 28, 273–279.
| Molecular evidence for zooplankton-associated nitrogen-fixing anaerobes based on amplification of the nifH gene.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXhvF2ntr4%3D&md5=2a7bb3537a77e4405bd81764169cb83bCAS |
Campbell, L., Carpenter, E., Montoya, J., Kustka, A., and Capone, D. (2005). Picoplankton community structure within and outside a Trichodesmium bloom in the southwestern Pacific Ocean. Vie et Milieu 55, 185–195.
Carpenter, E. J., Montoya, J. P., Burns, J., Mulholland, M. R., Subramaniam, A., and Capone, D. G. (1999). Extensive bloom of a N2-fixing diatom/cyanobacterial association in the tropical Atlantic Ocean. Marine Ecology Progress Series 185, 273–283.
| Extensive bloom of a N2-fixing diatom/cyanobacterial association in the tropical Atlantic Ocean.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXitF2ksw%3D%3D&md5=da854bf146b59978f555a087a8870b81CAS |
Chao, A. (1984). Nonparametric estimation of the number of classes in a population. Scandinavian Journal of Statistics 11, 265–270.
Chao, A., Chazdon, R. L., Colwell, R. K., and Shen, T. J. (2005). A new statistical approach for assessing similarity of species composition with incidence and abundance data. Ecology Letters 8, 148–159.
| A new statistical approach for assessing similarity of species composition with incidence and abundance data.Crossref | GoogleScholarGoogle Scholar |
Chen, Y. L. (2005). Spatial and seasonal variations of nitrate-based new production and primary production in the South China Sea. Deep-sea Research. Part I, Oceanographic Research Papers 52, 319–340.
| Spatial and seasonal variations of nitrate-based new production and primary production in the South China Sea.Crossref | GoogleScholarGoogle Scholar |
Chen, Y. L., Chen, H. Y., and Lin, Y. H. (2003). Distribution and downward flux of Trichodesmium in the South China Sea as influenced by the transport from the Kuroshio Current. Marine Ecology Progress Series 259, 47–57.
| Distribution and downward flux of Trichodesmium in the South China Sea as influenced by the transport from the Kuroshio Current.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXpvVCqur4%3D&md5=9f67e80487cee39f17007d893e00cbe2CAS |
Chen, Y. L., Chen, H. Y., Tuo, S., and Ohki, K. (2008). Seasonal dynamics of new production from Trichodesmium N2 fixation and nitrate uptake in the upstream Kuroshio and South China Sea basin. Limnology and Oceanography 53, 1705–1721.
| Seasonal dynamics of new production from Trichodesmium N2 fixation and nitrate uptake in the upstream Kuroshio and South China Sea basin.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtlWqsr%2FP&md5=de915895aed26e59612cbc28bd0e45f5CAS |
Chien, Y. T., and Zinder, S. H. (1994). Cloning, DNA sequencing, and characterization of a nifD-homologous gene from the archaeon Methanosarcina barkeri 227 which resembles nifD1 from the eubacterium Clostridium pasteurianum. Journal of Bacteriology 176, 6590–6598.
| 1:CAS:528:DyaK2MXhvV2nsbk%3D&md5=ba0c2422c0f5229efbad6baf01d03eccCAS | 7961410PubMed |
Church, M. J., Short, C. M., Jenkins, B. D., Karl, D. M., and Zehr, J. P. (2005). Temporal patterns of nitrogenase gene (nifH) expression in the oligotrophic North Pacific Ocean. Applied and Environmental Microbiology 71, 5362–5370.
| Temporal patterns of nitrogenase gene (nifH) expression in the oligotrophic North Pacific Ocean.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtVahtr%2FE&md5=a6e26db6593dd733361f700e250cb597CAS | 16151126PubMed |
Dowd, S. E., Callaway, T. R., Wolcott, R. D., Sun, Y., McKeehan, T., Hagevoort, R. G., and Edrington, T. S. (2008). Evaluation of the bacterial diversity in the feces of cattle using 16S rDNA bacterial tag-encoded FLX amplicon pyrosequencing (bTEFAP). BMC Microbiology 8, 125.
| Evaluation of the bacterial diversity in the feces of cattle using 16S rDNA bacterial tag-encoded FLX amplicon pyrosequencing (bTEFAP).Crossref | GoogleScholarGoogle Scholar | 18652685PubMed |
Eddy, S. R. (1998). Profile hidden Markov models. Bioinformatics 14, 755–763.
| Profile hidden Markov models.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXktlCmtQ%3D%3D&md5=e8b382b036cdc9c0c9781e7da65754dcCAS | 9918945PubMed |
Farnelid, H., Andersson, A. F., Bertilsson, S., Al-Soud, W. A., Hansen, L. H., Sørensen, S., Steward, G. F., Hagström, Å., and Riemann, L. (2011). Nitrogenase gene amplicons from global marine surface waters are dominated by genes of non-cyanobacteria. PLoS ONE 6, e19223.
| Nitrogenase gene amplicons from global marine surface waters are dominated by genes of non-cyanobacteria.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXlslGmt7o%3D&md5=3f9a0b0be5aa03eca05d2257dc6df836CAS | 21559425PubMed |
Farnelid, H., Bentzon-Tilia, M., Andersson, A. F., Bertilsson, S., Jost, G., Labrenz, M., Jurgens, K., and Riemann, L. (2013a). Active nitrogen-fixing heterotrophic bacteria at and below the chemocline of the central Baltic Sea. The ISME Journal 7, 1413–1423.
| Active nitrogen-fixing heterotrophic bacteria at and below the chemocline of the central Baltic Sea.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhtValt7zL&md5=098a4f516f2a11a6e7cbe8e48f7aaa3aCAS | 23446833PubMed |
Farnelid, H., Harder, J., Bentzon-Tilia, M., and Riemann, L. (2013b). Isolation of heterotrophic diazotrophic bacteria from estuarine surface waters. Environmental Microbiology , .
| Isolation of heterotrophic diazotrophic bacteria from estuarine surface waters.Crossref | GoogleScholarGoogle Scholar | 24330580PubMed |
Foster, R. A., Paytan, A., and Zehr, J. P. (2009). Seasonality of N2 fixation and nifH gene diversity in the Gulf of Aqaba (Red Sea). Limnology and Oceanography 54, 219–233.
| Seasonality of N2 fixation and nifH gene diversity in the Gulf of Aqaba (Red Sea).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhsVCrsbfE&md5=fd6a98f4908c528896b5b73419e0d39fCAS |
Gaby, J. C., and Buckley, D. H. (2012). A comprehensive evaluation of PCR primers to amplify the nifH gene of nitrogenase. PLoS ONE 7, e42149.
| A comprehensive evaluation of PCR primers to amplify the nifH gene of nitrogenase.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtFWlsbnP&md5=386d2fd7d8ea0d9d437c5b49de60788dCAS | 22848735PubMed |
Goto, M., Ando, S., Hachisuka, Y., and Yoneyama, T. (2005). Contamination of diverse nifH and nifH-like DNA into commercial PCR primers. FEMS Microbiology Letters 246, 33–38.
| Contamination of diverse nifH and nifH-like DNA into commercial PCR primers.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXjslKgtr4%3D&md5=f6968dd185af6c8994ed7a1cbac3e2c4CAS | 15869959PubMed |
Hall, T. A. (1999). BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41, 95–98.
| 1:CAS:528:DC%2BD3cXhtVyjs7Y%3D&md5=9cb2157f64a65889a72f8b3c73c686caCAS |
Halm, H., Lam, P., Ferdelman, T. G., Lavik, G., Dittmar, T., LaRoche, J., D’Hondt, S., and Kuypers, M. M. (2012). Heterotrophic organisms dominate nitrogen fixation in the South Pacific Gyre. The ISME Journal 6, 1238–1249.
| Heterotrophic organisms dominate nitrogen fixation in the South Pacific Gyre.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xnt1eltbg%3D&md5=2e7e482de452b6e90c3d73d2ba808e02CAS | 22170429PubMed |
Hamers, L., Hemeryck, Y., Herweyers, G., Janssen, M., Keters, H., Rousseau, R., and Vanhoutte, A. (1989). Similarity measures in scientometric research: the Jaccard index versus Salton’s cosine formula. Information Processing & Management 25, 315–318.
| Similarity measures in scientometric research: the Jaccard index versus Salton’s cosine formula.Crossref | GoogleScholarGoogle Scholar |
Haverkamp, T., Acinas, S. G., Doeleman, M., Stomp, M., Huisman, J., and Stal, L. J. (2008). Diversity and phylogeny of Baltic Sea picocyanobacteria inferred from their ITS and phycobiliprotein operons. Environmental Microbiology 10, 174–188.
| 1:CAS:528:DC%2BD1cXisFCgu7s%3D&md5=b5c4a7a0127d659d55e6eff0a387428cCAS | 17903216PubMed |
Huber, J. A., Welch, D. B. M., Morrison, H. G., Huse, S. M., Neal, P. R., Butterfield, D. A., and Sogin, M. L. (2007). Microbial population structures in the deep marine biosphere. science 318, 97–100.
| Microbial population structures in the deep marine biosphere.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtFWitbrP&md5=eb3a09e830f5cc1e2141c4f7b7c94d53CAS | 17916733PubMed |
Huse, S. M., Huber, J. A., Morrison, H. G., Sogin, M. L., and Mark Welch, D. (2007). Accuracy and quality of massively parallel DNA pyrosequencing. Genome Biology 8, R143.
| Accuracy and quality of massively parallel DNA pyrosequencing.Crossref | GoogleScholarGoogle Scholar | 17659080PubMed |
Huse, S. M., Welch, D. M., Morrison, H. G., and Sogin, M. L. (2010). Ironing out the wrinkles in the rare biosphere through improved OTU clustering. Environmental Microbiology 12, 1889–1898.
| Ironing out the wrinkles in the rare biosphere through improved OTU clustering.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtVegsLnO&md5=2835ec42c3d4c52e988430cd4b862e82CAS | 20236171PubMed |
Karl, D., Letelier, R., Tupas, L., Dore, J., Christian, J., and Hebel, D. (1997). The role of nitrogen fixation in biogeochemical cycling in the subtropical North Pacific Ocean. Nature 388, 533–538.
| The role of nitrogen fixation in biogeochemical cycling in the subtropical North Pacific Ocean.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXlt1art70%3D&md5=45cb80c87553ff5ae8ae011e796cb4d5CAS |
Kong, L. L., Jing, H. M., Kataoka, T., Sun, J., and Liu, H. B. (2011). Phylogenetic diversity and spatio-temporal distribution of nitrogenase genes (nifH) in the northern South China Sea. Aquatic Microbial Ecology 65, 15–27.
| Phylogenetic diversity and spatio-temporal distribution of nitrogenase genes (nifH) in the northern South China Sea.Crossref | GoogleScholarGoogle Scholar |
Kunin, V., Engelbrektson, A., Ochman, H., and Hugenholtz, P. (2010). Wrinkles in the rare biosphere: pyrosequencing errors can lead to artificial inflation of diversity estimates. Environmental Microbiology 12, 118–123.
| Wrinkles in the rare biosphere: pyrosequencing errors can lead to artificial inflation of diversity estimates.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhvFaisb4%3D&md5=90255980c23c2bac34f541034ffef6e4CAS | 19725865PubMed |
Langlois, R. J., Hümmer, D., and LaRoche, J. (2008). Abundances and distributions of the dominant nifH phylotypes in the Northern Atlantic Ocean. Applied and Environmental Microbiology 74, 1922–1931.
| Abundances and distributions of the dominant nifH phylotypes in the Northern Atlantic Ocean.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXjs1ags7k%3D&md5=ba2c86fb4a3755a45bfca1d972d84b2aCAS | 18245263PubMed |
Letunic, I., and Bork, P. (2007). Interactive Tree Of Life (iTOL): an online tool for phylogenetic tree display and annotation. Bioinformatics 23, 127–128.
| Interactive Tree Of Life (iTOL): an online tool for phylogenetic tree display and annotation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtlGktLzN&md5=d1187e616561f3ebbbe8c5956ac1c0b9CAS | 17050570PubMed |
Li, W., and Godzik, A. (2006). Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics 22, 1658–1659.
| Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XmsVent7s%3D&md5=8fcf96455910bcd59ffb5e4d3b4c2bb4CAS | 16731699PubMed |
Liu, K. K., Chao, S. Y., Shaw, P. T., Gong, G. C., Chen, C. C., and Tang, T. (2002). Monsoon-forced chlorophyll distribution and primary production in the South China Sea: observations and a numerical study. Deep-sea Research. Part I, Oceanographic Research Papers 49, 1387–1412.
| Monsoon-forced chlorophyll distribution and primary production in the South China Sea: observations and a numerical study.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XmtlWgtbs%3D&md5=dece7c18270b024abd628febe31ecc7bCAS |
Martin, A. P. (2002). Phylogenetic approaches for describing and comparing the diversity of microbial communities. Applied and Environmental Microbiology 68, 3673–3682.
| Phylogenetic approaches for describing and comparing the diversity of microbial communities.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XmtVaqtLY%3D&md5=b6fd93f12d5c1565e733b8e874a91916CAS | 12147459PubMed |
Mazard, S. L., Fuller, N. J., Orcutt, K. M., Bridle, O., and Scanlan, D. J. (2004). PCR analysis of the distribution of unicellular cyanobacterial diazotrophs in the Arabian Sea. Applied and Environmental Microbiology 70, 7355–7364.
| PCR analysis of the distribution of unicellular cyanobacterial diazotrophs in the Arabian Sea.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhtFaitrvK&md5=81f321e7f48b04dd88787e320748d1deCAS | 15574936PubMed |
Mehta, M. P., Butterfield, D. A., and Baross, J. A. (2003). Phylogenetic diversity of nitrogenase (nifH) genes in deep-sea and hydrothermal vent environments of the Juan de Fuca Ridge. Applied and Environmental Microbiology 69, 960–970.
| Phylogenetic diversity of nitrogenase (nifH) genes in deep-sea and hydrothermal vent environments of the Juan de Fuca Ridge.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXhtF2isbw%3D&md5=f8a0ebcd22e0f1cd6dbef0d1036090b1CAS | 12571018PubMed |
Metzger, E. J., and Hurlburt, H. E. (2001). The nondeterministic nature of Kuroshio penetration and Eddy shedding in the South China Sea. Journal of Physical Oceanography 31, 1712–1732.
| The nondeterministic nature of Kuroshio penetration and Eddy shedding in the South China Sea.Crossref | GoogleScholarGoogle Scholar |
Moisander, P. H., Beinart, R. A., Voss, M., and Zehr, J. P. (2008). Diversity and abundance of diazotrophic microorganisms in the South China Sea during intermonsoon. The ISME Journal 2, 954–967.
| Diversity and abundance of diazotrophic microorganisms in the South China Sea during intermonsoon.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtF2qsrnL&md5=045005c8da580d42a3a1a7114700bf98CAS | 18528417PubMed |
Moisander, P. H., Beinart, R. A., Hewson, I., White, A. E., Johnson, K. S., Carlson, C. A., Montoya, J. P., and Zehr, J. P. (2010). Unicellular cyanobacterial distributions broaden the oceanic N2 fixation domain. Science 327, 1512–1514.
| Unicellular cyanobacterial distributions broaden the oceanic N2 fixation domain.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXjt1Gnu7w%3D&md5=d4766159e308e90eea074e73569a416cCAS | 20185682PubMed |
Montoya, J. P., Holl, C. M., Zehr, J. P., Hansen, A., Villareal, T. A., and Capone, D. G. (2004). High rates of N2 fixation by unicellular diazotrophs in the oligotrophic Pacific Ocean. Nature 430, 1027–1032.
| High rates of N2 fixation by unicellular diazotrophs in the oligotrophic Pacific Ocean.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXmvFCisLc%3D&md5=d407aaff61d0375436714ff2e3f48b39CAS | 15329721PubMed |
Orcutt, K. M., Lipschultz, F., Gundersen, K., Arimoto, R., Michaels, A. F., Knap, A. H., and Gallon, J. R. (2001). A seasonal study of the significance of N2 fixation by Trichodesmium spp. at the Bermuda Atlantic Time-series Study (BATS) site. Deep-sea Research. Part II, Topical Studies in Oceanography 48, 1583–1608.
| A seasonal study of the significance of N2 fixation by Trichodesmium spp. at the Bermuda Atlantic Time-series Study (BATS) site.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXkt1Cru7w%3D&md5=f6637b2f61c42a59346298e7e8e33127CAS |
Paerl, H. W. (2012). Marine plankton. In ‘Ecology of Cyanobacteria II’ (Ed. B. A. Whitton.). pp. 127–153. (Springer: New York.)
Porebski, S., Bailey, L. G., and Baum, B. R. (1997). Modification of a CTAB DNA extraction protocol for plants containing high polysaccharide and polyphenol components. Plant Molecular Biology Reporter 15, 8–15.
| Modification of a CTAB DNA extraction protocol for plants containing high polysaccharide and polyphenol components.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXivVejsbs%3D&md5=a7f419393fcc914a04d7f6e314d6a638CAS |
Raymond, J., Siefert, J. L., Staples, C. R., and Blankenship, R. E. (2004). The natural history of nitrogen fixation. Molecular Biology and Evolution 21, 541–554.
| The natural history of nitrogen fixation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXis1entLk%3D&md5=c341bd5b6851b0ff906cb885342eec5eCAS | 14694078PubMed |
Riemann, L., Farnelid, H., and Steward, G. F. (2010). Nitrogenase genes in non-cyanobacterial plankton: prevalence, diversity and regulation in marine waters. Aquatic Microbial Ecology 61, 235–247.
| Nitrogenase genes in non-cyanobacterial plankton: prevalence, diversity and regulation in marine waters.Crossref | GoogleScholarGoogle Scholar |
Santhanam, R., Srinivasan, A., Ramadhas, V., and Devaraj, M. (1994). Impact of Trichodesmium bloom on the plankton and productivity in the Tuticorin Bay, southeast coast of India. Indian Journal of Marine Sciences 23, 27–30.
| 1:CAS:528:DyaK2cXkvFSqur0%3D&md5=c397970f3baeb8427ad0f2d2ec7eb3dfCAS |
Schloss, P. D. (2008). Evaluating different approaches that test whether microbial communities have the same structure. The ISME Journal 2, 265–275.
| Evaluating different approaches that test whether microbial communities have the same structure.Crossref | GoogleScholarGoogle Scholar | 18239608PubMed |
Schloss, P. D., Westcott, S. L., Ryabin, T., Hall, J. R., Hartmann, M., Hollister, E. B., Lesniewski, R. A., Oakley, B. B., Parks, D. H., and Robinson, C. J. (2009). Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Applied and Environmental Microbiology 75, 7537–7541.
| Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXis1yltw%3D%3D&md5=dc8a4123aa8e237b0f4b1241f513e276CAS | 19801464PubMed |
Shaw, P. T., Chao, S. Y., Liu, K. K., Pai, S. C., and Liu, C. T. (1996). Winter upwelling off Luzon in the northeastern South China Sea. Journal of Geophysical Research – Oceans 101, 16 435–16 448.
| Winter upwelling off Luzon in the northeastern South China Sea.Crossref | GoogleScholarGoogle Scholar |
Sogin, M. L., Morrison, H. G., Huber, J. A., Welch, D. M., Huse, S. M., Neal, P. R., Arrieta, J. M., and Herndl, G. J. (2006). Microbial diversity in the deep sea and the underexplored “rare biosphere”. Proceedings of the National Academy of Sciences of the United States of America 103, 12 115–12 120.
| Microbial diversity in the deep sea and the underexplored “rare biosphere”.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xotlyisb4%3D&md5=34f163c2b3fc9651161de56ae6a6845dCAS |
Stal, L. J., Albertano, P., Bergman, B., Bröckel, K. v., Gallon, J. R., Hayes, P. K., Sivonen, K., and Walsby, A. E. (2003). BASIC: Baltic Sea cyanobacteria. An investigation of the structure and dynamics of water blooms of cyanobacteria in the Baltic Sea – responses to a changing environment. Continental Shelf Research 23, 1695–1714.
| BASIC: Baltic Sea cyanobacteria. An investigation of the structure and dynamics of water blooms of cyanobacteria in the Baltic Sea – responses to a changing environment.Crossref | GoogleScholarGoogle Scholar |
Stomp, M., Huisman, J., Voros, L., Pick, F. R., Laamanen, M., Haverkamp, T., and Stal, L. J. (2007). Colourful coexistence of red and green picocyanobacteria in lakes and seas. Ecology Letters 10, 290–298.
| Colourful coexistence of red and green picocyanobacteria in lakes and seas.Crossref | GoogleScholarGoogle Scholar | 17355568PubMed |
Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M., and Kumar, S. (2011). MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution 28, 2731–2739.
| MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXht1eiu73K&md5=887c0fd611631fa5076e3aa6bcbb4e32CAS | 21546353PubMed |
Turk, K. A., Rees, A. P., Zehr, J. P., Pereira, N., Swift, P., Shelley, R., Lohan, M., Woodward, E. M. S., and Gilbert, J. (2011). Nitrogen fixation and nitrogenase (nifH) expression in tropical waters of the eastern North Atlantic. The ISME Journal 5, 1201–1212.
| Nitrogen fixation and nitrogenase (nifH) expression in tropical waters of the eastern North Atlantic.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXnvVaqsb8%3D&md5=ec35d0c4ce0b25f168df06e4a71f657aCAS | 21228888PubMed |
Turk-Kubo, K. A., Karamchandani, M., Capone, D. G., and Zehr, J. P. (2013). The paradox of marine heterotrophic nitrogen fixation: abundances of heterotrophic diazotrophs do not account for nitrogen fixation rates in the eastern tropical South Pacific. Environmental Microbiology , .
| The paradox of marine heterotrophic nitrogen fixation: abundances of heterotrophic diazotrophs do not account for nitrogen fixation rates in the eastern tropical South Pacific.Crossref | GoogleScholarGoogle Scholar |
Wu, J., Chung, S. W., Wen, L. S., Liu, K. K., Chen, Y. L. L., Chen, H. Y., and Karl, D. M. (2003). Dissolved inorganic phosphorus, dissolved iron, and Trichodesmium in the oligotrophic South China Sea. Global Biogeochemical Cycles 17, 8-1–8-10.
| Dissolved inorganic phosphorus, dissolved iron, and Trichodesmium in the oligotrophic South China Sea.Crossref | GoogleScholarGoogle Scholar |
Young, J. (2005). The phylogeny and evolution of nitrogenases. In ‘Genomes and Genomics of Nitrogen-fixing Organisms’ (Eds R. Palacios and W. E. Newton.). pp. 221–241. (Springer: Dordrecht.)
Yue, J. C., Clayton, M. K., and Lin, F. C. (2001). A nonparametric estimator of species overlap. Biometrics 57, 743–749.
| A nonparametric estimator of species overlap.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3MrgtFOiuw%3D%3D&md5=6f0235e9a4ac1cd112ec15539c8bab7eCAS | 11550923PubMed |
Zani, S., Mellon, M. T., Collier, J. L., and Zehr, J. P. (2000). Expression of nifH genes in natural microbial assemblages in Lake George, New York, detected by reverse transcriptase PCR. Applied and Environmental Microbiology 66, 3119–3124.
| Expression of nifH genes in natural microbial assemblages in Lake George, New York, detected by reverse transcriptase PCR.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXkslKltb8%3D&md5=cf9648437da538a25ca3433efec210f8CAS | 10877818PubMed |
Zehr, J. P. (2011). Nitrogen fixation by marine cyanobacteria. Trends in Microbiology 19, 162–173.
| Nitrogen fixation by marine cyanobacteria.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXkt1KhtLw%3D&md5=71a416713d0607fd6819d5e67cf7ef2aCAS | 21227699PubMed |
Zehr, J. P., and McReynolds, L. A. (1989). Use of degenerate oligonucleotides for amplification of the nifH gene from the marine cyanobacterium Trichodesmium thiebautii. Applied and Environmental Microbiology 55, 2522–2526.
| 1:CAS:528:DyaL1MXlvVymsrk%3D&md5=88a078052aae2c830e653cdf015e8dc5CAS | 2513774PubMed |
Zehr, J., and Turner, P. (2001). Nitrogen fixation: nitrogenase genes and gene expression. In ‘Methods in Microbiology, Vol. 30’ (Eds C. Harwood and A. Wipat.). pp. 271–286. (Academic Press: New York.)
Zehr, J. P., Crumbliss, L. L., Church, M. J., Omoregie, E. O., and Jenkins, B. D. (2003a). Nitrogenase genes in PCR and RT-PCR reagents: implications for studies of diversity of functional genes. BioTechniques 35, 996–1013.
| 1:CAS:528:DC%2BD3sXovFWlsbo%3D&md5=e27cf1e07a9e2d7cbe65e79dc911d6b8CAS | 14628674PubMed |
Zehr, J. P., Jenkins, B. D., Short, S. M., and Steward, G. F. (2003b). Nitrogenase gene diversity and microbial community structure: a cross-system comparison. Environmental Microbiology 5, 539–554.
| Nitrogenase gene diversity and microbial community structure: a cross-system comparison.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXlvFChs7s%3D&md5=1b8665a50bdc6e4f366809f4917f5f3eCAS | 12823187PubMed |
Zehr, J. P., Bench, S. R., Mondragon, E. A., McCarren, J., and DeLong, E. F. (2007). Low genomic diversity in tropical oceanic N2-fixing cyanobacteria. Proceedings of the National Academy of Sciences of the United States of America 104, 17 807–17 812.
| Low genomic diversity in tropical oceanic N2-fixing cyanobacteria.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXht12lur%2FP&md5=0cb8987292d67a33087c32b8a88bc7e4CAS |
Zhang, Y., Zhao, Z., Sun, J., and Jiao, N. (2011). Diversity and distribution of diazotrophic communities in the South China Sea deep basin with mesoscale cyclonic eddy perturbations. FEMS Microbiology Ecology 78, 417–427.
| Diversity and distribution of diazotrophic communities in the South China Sea deep basin with mesoscale cyclonic eddy perturbations.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhs1SqtLnI&md5=5c1268a9d64232f69baa85fcf05f6465CAS | 22066702PubMed |
