Spatial and seasonal variations of Cyanobacteria and their nitrogen fixation rates in Sanya Bay, South China Sea

Authors

  • Junde Dong South China Sea Institute of Oceanology, Chinese Academy of Sciences
  • Yanying Zhang South China Sea Institute of Oceanology, Chinese Academy of Sciences
  • Youshao Wang South China Sea Institute of Oceanology, Chinese Academy of Sciences
  • Si Zhang South China Sea Institute of Oceanology, Chinese Academy of Sciences
  • Hankui Wang South China Sea Institute of Oceanology, Chinese Academy of Sciences

DOI:

https://doi.org/10.3989/scimar.2008.72n2239

Keywords:

Trichodesmium, phytoplankton, nitrogen fixation, cyanobacteria, Sanya Bay

Abstract


The nitrogen fixation rates of planktonic and intertidal benthic cyanobacteria were investigated in Sanya Bay from 2003 to 2005. Trichodesmium thiebautii was the dominant species of planktonic cyanobacteria during our study. Significant seasonal and spatial variations in Trichodesmium spp. abundance were observed (P<0.01). The highest Trichodesmium concentrations occurred during intermonsoon periods and in the outer region of Sanya Bay (Outer Bay stations). At fixed station S03 the abundance of T. thiebautii ranged from 1.14×103 to 2060×103 trichomes m–2, with an annual mean of 273×103 trichomes m–2. The average nitrogen fixation rate per colony of T. thiebautii was 0.27 nmol N h-1 colony-1 and it did not show any obvious seasonal variations. Nitrogen fixation by planktonic cyanobacteria was highest in the Outer Bay stations, where the estimated amount of new nitrogen introduced by Trichodesmium contributed 0.03 to 1.63% of the total primary production and up to 11.64% of the new production. Statistical results showed that significant seasonal and spatial variations of nitrogen fixation rates were found among the intertidal communities. The main benthic nitrogen-fixing cyanobacteria were identified as members of the genera Anabaena, Calothrix, Lyngbya, Nostoc and Oscillatoria. The highest nitrogen fixation rate was found in microbial mats and the lowest in reefs and rocky sediments. All the benthic communities studied presented their highest nitrogen fixation activity in summer, with an average nitrogen fixation rate of 33.31 µmol N h-1 m-2, whereas the lowest nitrogen activity was detected in winter, with an average nitrogen fixation rate of 5.66 µmol N h-1 m-2. A Pearson correlation analysis indicated that the nitrogen fixation rate of three types of intertidal communities was significantly positively correlated to seawater temperature (P<0.05), whereas only the nitrogen fixation rate of the reefs and rock communities was significantly negatively correlated to seawater salinity (P<0.05).

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Author Biographies

Junde Dong, South China Sea Institute of Oceanology, Chinese Academy of Sciences

National Experiment Station of Tropical Marine Biology

Yanying Zhang, South China Sea Institute of Oceanology, Chinese Academy of Sciences

National Experiment Station of Tropical Marine Biology. Graduate school of Chinese Academy of Science, Beijing, China

Si Zhang, South China Sea Institute of Oceanology, Chinese Academy of Sciences

National Experiment Station of Tropical Marine Biology

Hankui Wang, South China Sea Institute of Oceanology, Chinese Academy of Sciences

National Experiment Station of Tropical Marine Biology

References

Arnaud, T., G. Stana, B. Evelyne, D.W. Rutger and W. Annick. – 2003. Cyanobacterial diversity in natural and artificial microbial mats of Lake Fryxell (McMurdo Dry Valleys, Antarctica): a morphological and molecular approach. Appl. Environ. Microbiol., 69: 5157-5169. doi:10.1128/AEM.69.9.5157-5169.2003

Bebout, B.M., H.W. Paerl, K.M. Crocker and L.E. Prufert. – 1987. Diel interactions of oxygenic photosynthesis and N2 fixation (acetylene reduction) in a marine microbial mat community. Appl. Environ. Microbiol., 53: 2353-2362.

Bell, P.R., I. Elmetri and P. Uwins. – 1999. Nitrogen fixation by Trichodesmium spp. in the Central and Northern Great Barrier Reef Lagoon: relative importance of the fixed-nitrogen load. Mar. Ecol. Prog. Ser., 186: 119-126. doi:10.3354/meps186119

Bissett, W. P., J.J. Walsh, D.A. Dieterle and K.L. Cardes. – 1999. Carbon cycling in the upper waters of the Sargasso Sea: I. Numerical simulation of differential carbon and nitrogen fluxes. Deep-Sea Res. I, 46: 205-269. doi:10.1016/S0967-0637(98)00062-4

Brad, M.B., W.F. Matthew and W.P. Hans. – 1993. Identification of the sources of energy for nitrogen fixation and physiological characterization of nitrogen-fixing members of a marine microbial mat community. Appl. Environ. Microbiol., 59: 1495-1503.

Bruns, J.A., J.P. Zehr and D.G. Capone. – 2002. Nitrogen-fixing phylotypes of Chesapeake Bay and Neuse River estuary sediments. Microb. Ecol., 44: 336-343. doi:10.1007/s00248-002-1000-9

Burris, R.H. – 1976. Nitrogen Fixation by Blue-green Algae of the Lizard Island Area of the Great Barrier Reef. Aust. J. Plant Physiol., 3: 41-51.

Capone, D.G. – 1982. Nitrogen fixation (acetylene reduction) by rhizosphere sediments of the eelgrass Zostera marina. Mar. Ecol. Prog. Ser., 10: 67-75. doi:10.3354/meps010067

Capone, D.G. – 1993. Determination of nitrogenase activity in aquatic samples using the acetylene reduction procedure. In: P.F. Kemp, B.F. Sherr, E.B. Sherr and J.J. Cole (eds.), Handbook of methods in aquatic microbial ecology, pp. 624-631. Lewis Press, Boca Raton, Fla.

Capone, D.G. and B.F. Taylor. – 1980. N2 fixation in the rhizosphere of Thalassia testudinum. Can. J. Microbiol., 26: 998-1005.

Capone, D.G. and E.J. Carpenter. – 1982. Nitrogen fixation in the marine environment. Science, 217: 1140-1142. doi:10.1126/science.217.4565.1140

Capone, D.G., J.P. Zehr, H.W. Pearl, B. Bergman and E.J. Carpenter. – 1997. Trichodesmium, a globally significant marine cyanobacterium. Science, 276: 1221-1229. doi:10.1126/science.276.5316.1221

Capone, D.G., P.A. Penhale, R.S. Oremland and B.F. Taylor. – 1979. Relationship between productivity and N2 (C2H2) fixation in the rhizosphere of Thalassia testudinium. Limnol. Oceanogr., 24: 117-125.

Carpenter, E.J., A. Subramaniam and D.G. Capone. – 2004. Biomass and primary productivity of the cyanobacterium Trichodesmium spp. in the tropical North Atlantic ocean, Deep-Sea Res. I, 51: 173-203. doi:10.1016/j.dsr.2003.10.006

Carpenter, E.J. and C.C. Price. – 1977. Nitrogen fixation, distribution, and production of Oscillatoria (Trichodesmium) spp. in the western Sargasso and Caribbean Seas. Limnol. Oceanogr., 22: 60-72.

Carpenter, E.J., J.M. O’Neil, R. Dawson, D.G. Capone, P.J.A. Siddiqui, T. Roenneberg and B. Bergman. – 1993. The tropical diazotrophic phytoplankter Trichodesmium: biological characteristics of two common species. Mar. Ecol. Prog. Ser., 95: 295-304.

Carpenter, E.J. and K. Romans. – 1991. Major role of the cyanobacterium Trichodesmium in nutrient cycling in the North Atlantic Ocean. Science, 254: 1356-1358. doi:10.1126/science.254.5036.1356

Charpy-Roubaud, C., L. Charpy and A.W.D. Larkum. – 1997. Contribution of N2 fixation to N primary productivity of the lagoon of Tikehau. Proc. 8th Int. Coral Reef Symp., 1: 803-808.

Chang, J., K.P. Chiang and G.C. Gong. – 2000. Seasonal variation and cross-shelf distribution of the nitrogen-fixing cyanobacterium, Trichodesmium, in southern East China Sea. Cont. Shelf. Res., 20: 479-492. doi:10.1016/S0278-4343(99)00082-5

Chen, Y.L., H.Y. Chen and Y.H. Lin. – 2003. Distribution and downward flux of Trichodesmium in the South China Sea as influenced by the transport from the Kuroshio Current. Mar. Ecol. Prog. Ser., 259: 47-57. doi:10.3354/meps259047

Dong, J.D., H.K. Wang, S. Zhang and L.M. Huang. – 2002a. Vertical distribution characteristics of seawater temperature and DIN in Sanya Bay. Tropic Oceanol., 21(1): 40-47.

Dong, J.D., H.K. Wang, S. Zhang, L.M. Huang and Z.D. Wang. – 2002b. Marine nitrogen-fixing organisms and their contribution to the N and C requirement for marine biological production. Acta Ecol. Sinica, 22: 1741-1749.

Dong, J.D., Y.Y. Zhang and Y.S. Wang. – 2006. Species and community development of marine cyanobacteria in Sanya Bay, South China Sea. Tropic Oceanol., 25(3): 40-46.

Doyle, R.D. and T.R. Fisher, 1994. Nitrogen fixation by periphyton and plankton on the Amazon floodplain at Lake Calado. Biogeochemistry 26: 41-66. doi:10.1007/BF02180403

Eisele, K.A., D.S. Schimel, L.A. Kapustka and W.J. Parton. – 1989. Effects of available P and N:P ratios of non-symbiotic dinitrogen fixation in tallgrass prairie soils. Oecologia, 79: 471-474. doi:10.1007/BF00378663

Eliska, R. and K. Jaroslava. – 2000. A function of cyanobacterial mats in phosphorus-limited tropical wetlands. Hydrobiologia, 431: 135-153. doi:10.1023/A:1004011318643

Fu, F.X. and P.R.F. Bell. – 2003. Effect of salinity on growth, pigmentation, N2 fixation and alkaline phosphatase activity of cultured Trichodesmium sp. Mar. Ecol. Prog. Ser., 257: 69-76. doi:10.3354/meps257069

Gotto, J.W., F.R. Tabita and C.V. Baalen. – 1981. Nitrogen fixation in intertidal environments of Texas Gulf coast. Estuar. Coast. Shelf Sci., 12: 231-235. doi:10.1016/S0302-3524(81)80099-0

Hoffmann, L. – 1999. Marine cyanobacteria in tropical regions: diversity and ecology. Eru. J. Phycol., 34: 371-379.

Huang, L.M., Y.H. Tan, and X.Y. Song. – 2003. The status of the ecological environment and a proposed protection strategy in Sanya Bay, Hainan Island, China. Mar. Pollut. Bull., 47: 180-186. doi:10.1016/S0025-326X(03)00070-5

Joye, S.B. and H.W. Paerl. -1994. Nitrogen cycling in microbial mats: rates and patterns of denitrification and nitrogen fixation. Mar. Biol., 119: 285-295. doi:10.1007/BF00349568

Karl, D., R. Letelier, L. Tupas, J. Dore, J. Christian and D. Hebel. – 1997. The role of nitrogen fixation in biogeochemical cycling in the subtropical North Pacific Ocean. Nature, 386: 533-538. doi:10.1038/41474

Karl, D., A. Michaels and B. Bergman. – 2002. Dinitrogen fixation in the world’s oceans. Biogeochemistry, 57: 47-98. doi:10.1023/A:1015798105851

Larkum, A. W.D., I.R. Kennedy and W.J. Muller. – 1988. Nitrogen fixation on a coral reef. Mar. Biol., 98: 143-155. doi:10.1007/BF00392669

Letelier, R.M. and D.M. Karl. – 1996. Role of Trichodesmium spp. In the productivity of the subtropical North Pacific Ocean. Mar. Ecol. Prog. Ser., 133: 263-273. doi:10.3354/meps133263

Letelier, R.M. and D.M. Karl. – 1998. Trichodesmium spp. Physiology and nutrient fluxes in the North Pacific subtropical gyre. Aquat. Micro. Ecol., 15: 265-276. doi:10.3354/ame015265

Letelier, R.M., J.E. Dore, C.D. Winn and D.M. Karl. – 1996. Seasonal and interannual variations in photosynthetic carbon assimilation at station ALOHA. Deep-Sea Res. II, 43: 467-490. doi:10.1016/0967-0645(96)00006-9

Lugomela, C., T.J. Lyimo, I. Bryceson, A.K. Semisi and B. Bergman. – 2002. Trichodesmium in costal waters of Tanzania: diversity, seasonality, nitrogen and carbon fixation. Hydrobiologia, 477: 1-13. doi:10.1023/A:1021017125376

Mcroy, C.P., J.J. Goering and B. Chaney. – 1973. Nitrogen fixation associated with seagrasses. Limnol. Oceanogr., 18: 998-1002.

Mills, M.M., C. Ridame, M. Davey, J. Laroche and R. J. Geider. – 2004. Iron and phosphorus co-limit nitrogen fixation in the eastern tropical North Atlantic. Nature, 429: 292-294. doi:10.1038/nature02550

Montoya, J.P., M. Voss, P. Kähler, and D.G. Capone. – 1996. A simple, high-precission, high-sensitivity tracer assay for N2 fixation. Appl. Environ. Microbiol., 62: 986-993.

Mulholland, M.R., S. Floge, E.J. Carpenter and D.G. Capone. – 2002. Phosphorus dynamics in cultures and natural populations of Trichodesmium spp. Mar. Ecol. Prog. Ser., 239:45-55 doi:10.3354/meps239045

Mulholland, M.R. and P.W. Bernhardt. – 2005. The effect of growth rate, phosphorus concentration, and temperature on N2 fixation, carbon fixation, and nitrogen release in continuous cultures of Trichodesmium IMS101. Limnol. Oceanogr., 50: 839-849.

O’Donohue, M.J., D.J.W. Moriarty and I.C. McRae. – 1991. Nitrogen fixation in sediments and the rhizosphere of the seagrass Zostera capricornia. Microbial. Ecol., 22: 53-64. doi:10.1007/BF02540212

Omoregie, E.O., L.L. Crumbliss, B.M. Bebout and J.P. Zehr. – 2004. Determination of nitrogen-fixing phylotypes in Lyngbya sp. And Microcoleus chthonoplastes cyanobacterial mats from Guerrero Negro, Baja California, Mexico. Appl. Environ. Microbiol., 70: 2119-2128. doi:10.1128/AEM.70.4.2119-2128.2004

Parsons, T.R., M. Takahashi and B. Hargrave. – 1984. Biological Oceanographic Processed (3rd edition). Oxford, Pergamon Press. Patriquin, D.G. – 1972. The origin of nitrogen and phosphorus for the growth of the marine angiosperm Thalassia testudinium. Mar. Biol., 16: 25-46.

Patriquin, D.G. and R. Knowles. – 1972. Nitrogen fixation in the rhizosphere of marine angiosperms. Mar. Biol., 16: 49-58. doi:10.1007/BF00347847

Pereg-Gerk, L., S. Nehemia and L. Yaakov. – 2002. In Situ nitrogen fixation associated with seagrasses in the Gulf of Elat (Red Sea). Aquat. Ecol., 36: 387-394. doi:10.1023/A:1016566019208

Postgate, J.R. – 1982. The fundamentals of nitrogen fixation. Cambridge University Press, London.

Rippka, R., J. Deruelles, J. Waterbury, M. Herdman and R. Stanier. – 1979. Generic assignments, strain histories and properties of pure cultures of cyanobacteria. J. Gen. Microbiol., 111:1-61

Roubaud, C.C., L. Charpy and AW.D. Larkum. – 2001. Atmospheric dinitrogen fixation by benthic communities of Tikehau Lagoon (Tuamotu Archipelago, French Polynesia) and its contribution to benthic primary production. Mar. Biol., 139: 991-997. doi:10.1007/s002270100636

Saino, T. and A. Hattori. – 1982. Aerobic nitrogen fixation by the marine non-heterocystous cyanobacterium Trichodesmium (Oscillatoria) spp.: Its protective mechanism against oxygen. Mar. Biol., 70: 251-254. doi:10.1007/BF00396843

Sañudo-Wilhelmy, S.A., A.B. Kustka, C.J. Gobler, D.A. Hutchins, M. Yang, K. Lwiza, J. Burns, D.G. Capone, J.A. Raven and E.J. Carpenter. – 2001. Phosphorus limitation of nitrogen fixation by Trichodesmium in the central Atlantic Ocean. Nature, 411: 66-69. doi:10.1038/35075041

Shashar, N., T. Feldstein, Y. Cohen and Y. Loya. – 1994. Nitrogen fixation (acetylene reduction) on a coral reef. Coral Reefs, 13: 171-174. doi:10.1007/BF00301195

Smith, G.W. and S.S. Hayasaka. – 1982. Nitrogenase activity associated with Halodule wrightii roots. Appl. Environ. Microbiol., 43:1244-1248.

Stal, L.J. – 1995. Physiological ecology of Cyanobacteria in microbial mats and other communities. New Phytol., 131: 1- 32. doi:10.1111/j.1469-8137.1995.tb03051.x

Stal, L.J., S. Grossberger and W.E. Krumbein. – 1984. Nitrogen fixation associated with the cyanobacterial mat of a marine laminated microbial ecosystem. Mar. Biol., 82: 217-224. doi:10.1007/BF00392402

Tan, Y.H., L.M. Huang, Q.C. Chen and X.P. Huang. – 2004. Seasonal variation in zooplankton composition and grazing impact on phytoplankton standing stock in the Pearl River Estuary, China. Cont. Shelf Res., 24: 1949-1968. doi:10.1016/j.csr.2004.06.018

Umezaki, I. – 1974. On the taxonomy of the genus Trichodesmium. Bull. Plankton Soc. Jpn., 20, 93-100.

Welsh, D.T., S. Bourgués, R. de Wit and R.A. Herbert. – 1996. Seasonal variations in nitrogen-fixation (acetylene reduction) and sulphate-reduction rates in the rhizosphere of Zostera noltii: nitrogen fixation by sulphate-reducing bacteria. Mar. Biol., 125: 619-628. doi:10.1007/BF00349243

Wilkinson, C.R., D.M. Williams, P.W. Sammarco, R.W. Hogg and L.A. Trott. – 1984. Rates of nitrogen fixation on coral reefs across the continental shelf of the central Great Barrier Reef. Mar. Biol., 80: 255-262. doi:10.1007/BF00392820

Zehr, J.P., M. Mellon, S. Braun, W. Litaker, T. Steppe and H.W. Pearl. – 1995. Diversity of heterotrophic nitrogen fixation genes in a marine cyanobacterial mat. Appl. Environ. Microbiol., 61: 2527-2532.

Zhang Y.Y., J.D. Dong and S. Zhang. – 2006. Study on nitrogen fixation physiology of marine cyanobacteria Calothrix sp. Strain MCT1 and Lyngbya sp. strain MCT6. Tropic Oceanol., 25(4): 17-21.

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2008-06-30

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Dong J, Zhang Y, Wang Y, Zhang S, Wang H. Spatial and seasonal variations of Cyanobacteria and their nitrogen fixation rates in Sanya Bay, South China Sea. Sci. mar. [Internet]. 2008Jun.30 [cited 2024Mar.29];72(2):239-51. Available from: https://scientiamarina.revistas.csic.es/index.php/scientiamarina/article/view/821

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