, Volume 24, Issue 7–8, pp 1450–1458 | Cite as

Spatial variation of phytoplankton community structure in Daya Bay, China

  • Zhao-Yu Jiang
  • You-Shao WangEmail author
  • Hao Cheng
  • Jian-Dong Zhang
  • Jiao Fei


Daya Bay is one of the largest and most important gulfs in the southern coast of China, in the northern part of the South China Sea. The phylogenetic diversity and spatial distribution of phytoplankton from the Daya Bay surface water and the relationship with the in situ water environment were investigated by the clone library of the large subunit of ribulose-1, 5-bisphosphate carboxylase (rbcL) gene. The dominant species of phytoplankton were diatoms and eustigmatophytes, which accounted for 81.9 % of all the clones of the rbcL genes. Prymnesiophytes were widely spread and wide varieties lived in Daya Bay, whereas the quantity was limited. The community structure of phytoplankton was shaped by pH and salinity and the concentration of silicate, phosphorus and nitrite. The phytoplankton biomass was significantly positively affected by phosphorus and nitrite but negatively by salinity and pH. Therefore, the phytoplankton distribution and biomass from Daya Bay were doubly affected by anthropic activities and natural factors.


Phytoplankton community Daya Bay Large subunit of ribulose-1, 5-bisphosphate carboxylase (rbcL) gene Redundancy analysis (RDA) Environmental variable 



This research was supported by, the National Natural Science Foundation of China (Nos. 41430966 and 41176101), the key projects in the National Science & Technology Pillar Program in the Eleventh Five-year Plan Period (No. 2012BAC07B0402), the Knowledge Innovation Programs of the Chinese Academy of Sciences (No. KSCX2-SW-132) and State Key Laboratory of Tropical Oceanography (No. LTOZZ1402).

Conflict of interest

The authors declare that they have no conflict of interest.


  1. Andersen RA, Bidigare RR, Latasa M (1996) A comparison of HPLC pigment signatures and electron microscopic observations for oligotrophic waters of the North Atlantic and Pacific Oceans. Deep-Sea Res II 43:517–537CrossRefGoogle Scholar
  2. Antia AN, Koeve W, Fischer G, Blanz T, Schulz-Bull D, Schölten J, Neuer S, Kremling K, Kuss J, Peinert R, Hebbeln D, Bathmann U, Conte M, Fehner U, Zeitzschel B (2001) Basin-wide particulate carbon flux in the Atlantic Ocean: regional export patterns and potential for atmospheric CO2 sequestration. Global Biogeochem Cycle 15:845–862CrossRefGoogle Scholar
  3. Ashida H, Saito Y, Kojima C, Kobayashi K, Ogasawara N, Yokota A (2003) A functional link between RuBisCO-like protein of Bacillus and photosynthetic RuBisCO. Science 302:286–290CrossRefGoogle Scholar
  4. Bernardi Aubry F, Acri F, Bianchi F, Pugnetti A (2013) Looking for patterns in the phytoplankton community of the Mediterranean microtidal Venice Lagoon: evidence from ten years of observations. Sci Mar 77:47–60CrossRefGoogle Scholar
  5. Bowler C, Karl DM, Colwell RR (2009) Microbial oceanography in a sea of opportunity. Nature 459:180–184CrossRefGoogle Scholar
  6. Cao H, Hong Y, Li M, Gu JD (2012) Community shift of ammonia-oxidizing bacteria along an anthropogenic pollution gradient from the Pearl River Delta to the South China Sea. Appl Microbiol Biotechnol 94:247–259CrossRefGoogle Scholar
  7. Corredor JE, Wawrik B, Paul JH, Tran H, Kerkhof L, Lopez JM, Dieppa A, Cardenas O (2004) Geochemical rate-RNA integration study: ribulose-1,5-bisphosphate carboxylase/oxygenase gene transcription and photosynthetic capacity of planktonic photoautotrophs. Appl Environ Microb 70:5459–5468CrossRefGoogle Scholar
  8. Eisen JA, Nelson KE, Paulsen IT, Heidelberg JF, Wu M, Dodson RJ, Deboy R, Gwinn ML, Nelson WC, Haft DH, Hickey EK, Peterson JD, Durkin AS, Kolonay JL, Yang F, Holt I, Umayam LA, Mason T, Brenner M, Shea TP, Parksey D, Nierman WC, Feldblyum TV, Hansen CL, Craven MB, Radune D, Vamathevan J, Khouri H, White O, Gruber TM, Ketchum KA, Venter JC, Tettelin H, Bryant DA, Fraser CM (2002) The complete genome sequence of Chlorobium tepidum TLS, a photosynthetic, anaerobic, green-sulfur bacterium. Proc Natl Acad Sci USA 99:9509–9514CrossRefGoogle Scholar
  9. Falkowski PG, Katz ME, Knoll AH, Quigg A, Raven JA, Schofield O, Taylor FJR (2004) The evolution of modern eukaryotic phytoplankton. Science 305:354–360CrossRefGoogle Scholar
  10. Field CB, Behrenfeld MJ, Randerson JT, Falkowski P (1998) Primary production of the biosphere: integrating terrestrial and oceanic components. Science 281:237–240CrossRefGoogle Scholar
  11. Gasiūnaitė ZR, Cardoso AC, Heiskanen AS, Henriksen P, Kauppila P, Olenina I, Pilkaitytė R, Purina I, Razinkovas A, Sagert S, Schubert H, Wasmund N (2005) Seasonality of coastal phytoplankton in the Baltic Sea: influence of salinity and eutrophication. Estuar Coast Shelf S 65:239–252CrossRefGoogle Scholar
  12. Gregorio V, Büchi L, Anneville O, Rimet F, Bouchez A, Chèvre N (2012) Risk of herbicide mixtures as a key parameter to explain phytoplankton fluctuation in a great lake: the case of Lake Geneva, Switzerland. Ecotoxicology 21:2306–2318CrossRefGoogle Scholar
  13. Hanson TE, Tabita FR (2001) A ribulose-1,5-bisphosphate carboxylase/oxygenase (RubisCO)-like protein from Chlorobium tepidum that is involved with sulfur metabolism and the response to oxidative stress. Proc Natl Acad Sci USA 98:4397–4402CrossRefGoogle Scholar
  14. Howarth R, Sharpley A, Walker D (2002) Sources of nutrient pollution to coastal waters in the United States: implications for achieving coastal water quality goals. Estuar Coast 25:656–676CrossRefGoogle Scholar
  15. Jiang ZY, Wang YS, Sun FL (2014) Spatial structure of eukaryotic ultra plankton community in the northern South China Sea. Biologia 69:557–565CrossRefGoogle Scholar
  16. Kunst F, Ogasawara N, Moszer I, Albertini AM, Alloni GO, Azevedo V, Haga K (1997) The complete genome sequence of the gram-positive bacterium Bacillus subtilis. Nature 390:249–256CrossRefGoogle Scholar
  17. La Du J, Erdner D, Dyhrman S, Anderson D (2002) Molecular approaches to understanding population dynamics of the toxic dinoflagellate Alexandrium fundyense. Biol Bull 203:244–245CrossRefGoogle Scholar
  18. Lapointe BE, Clark MW (1992) Nutrient inputs from the watershed and coastal eutrophication in the Florida Keys. Estuaries 15:465–476CrossRefGoogle Scholar
  19. Li M, Hong Y, Cao H, Gu JD (2013) Community structures and distribution of anaerobic ammonium oxidizing and nirS-encoding nitrite-reducing bacteria in surface sediments of the South China Sea. Microbial Ecol 66:281–296CrossRefGoogle Scholar
  20. Lin R, Buijse L, Dimitrov MR, Dohmen P, Kosol S, Maltby L, Roessink I, Sinkeldam JA, Smidt H, Van Wijngaarden KPA, Brock TC (2012) Effects of the fungicide metiram in outdoor freshwater microcosms: responses of invertebrates, primary producers and microbes. Ecotoxicology 21:1550–1569CrossRefGoogle Scholar
  21. López-Flores R, Boix D, Badosa A, Brucet S, Quintana XD (2009) Environmental factors affecting bacterioplankton and phytoplankton dynamics in confined Mediterranean salt marshes (NE Spain). J Exp Mar Biol Ecol 369:118–126CrossRefGoogle Scholar
  22. Lozupone C, Hamady M, Knight R (2006) UniFrac-an online tool for comparing microbial community diversity in a phylogenetic context. BMC Bioinform 7:371CrossRefGoogle Scholar
  23. McCarthy JJ, Taylor WR, Taft JL (1977) Nitrogenous nutrition of the plankton in the Chesapeake Bay. 1. Nutrient availability and phytoplankton preferences. Limnol Oceanogr 22:996–1011CrossRefGoogle Scholar
  24. Möllmann C, Diekmann R, Müller-Karulis B, Kornilovs G, Plikshs M, Axe P (2009) Reorganization of a large marine ecosystem due to atmospheric and anthropogenic pressure: a discontinuous regime shift in the Central Baltic Sea. Glob Change Biol 15:1377–1393CrossRefGoogle Scholar
  25. Murtugudde I, Beauchamp RJ, McClain CR, Lewis MR, Busalacchi A (2002) Effects of penetrative radiation on the upper tropical ocean circulation. J Clim 15:470–486CrossRefGoogle Scholar
  26. Pomati F, Nizzetto L (2013) Assessing triclosan-induced ecological and trans-generational effects in natural phytoplankton communities: a trait-based field method. Ecotoxicology 22:779–794CrossRefGoogle Scholar
  27. Rabosky DL, Sorhannus U (2009) Diversity dynamics of marine planktonic diatoms across the Cenozoic. Nature 457:183–186CrossRefGoogle Scholar
  28. Riebesell U (2004) Effects of CO2 enrichment on marine phytoplankton. J Oceanogr 60:719–729CrossRefGoogle Scholar
  29. Roemmich D, McGowan J (1995) Climatic warming and the decline of zooplankton in the California current. Science 267:1324–1326CrossRefGoogle Scholar
  30. Sabine CL, Feely RA, Gruber N, Key RM, Lee K, Bullister JL, Wanninkhof R, Wong CSI, Wallace DWR, Tilbrook B, Millero FJ, Peng T-H, Kozyr A, Ono T, Rios AF (2004) The oceanic sink for anthropogenic CO2. Science 305:367–371CrossRefGoogle Scholar
  31. Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425Google Scholar
  32. Schloss PD, Handelsman J (2006) Introducing SONS, a tool for operational taxonomic unit-based comparisons of microbial community memberships and structures. Appl Environ Microbiol 72:6773–6779CrossRefGoogle Scholar
  33. Smetacek V (1999) Diatoms and the carbon ocean cycle. Protist 150:25–32CrossRefGoogle Scholar
  34. Song X, Huang L, Zhang J, Huang X, Zhang J, Yin J, Tan Y, Liu S (2004) Variation of phytoplankton biomass and primary production in Daya Bay during spring and summer. Mar Pollut Bull 49:1036–1044CrossRefGoogle Scholar
  35. Suikkanen S, Laamanen M, Huttunen M (2007) Long-term changes in summer phytoplankton communities of the open northern Baltic Sea. Estuar Coast Shelf S 71:580–592CrossRefGoogle Scholar
  36. Sun CC, Wang YS, Sun SL, Zhang FQ (2006) Dynamic analysis of phytoplankton community characteristics in Daya Bay, China. Acta Ecol Sin 26(12):3948–3958CrossRefGoogle Scholar
  37. Sun CC, Wang YS, Wu ML, Dong JD, Wang YT, Sun FL, Zhang YY (2011) Seasonal variation of water quality and phytoplankton response patterns in Daya Bay, China. Int J Enviro Res Public Health 8:2951–2966CrossRefGoogle Scholar
  38. Suzuki K, Handa N, Kiyosawa H, Ishizaka J (1997) Temporal and spatial distribution of phytoplankton pigments in the central Pacific Ocean along 175°E during the boreal summers of 1992 and 1993. J Oceanogr 53:383–396CrossRefGoogle Scholar
  39. Tabita FR (1999) Microbial ribulose 1, 5-bisphosphate carboxylase/oxygenase: a different perspective. Photosynth Res 60:1–28CrossRefGoogle Scholar
  40. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739CrossRefGoogle Scholar
  41. ter Braak CJF, Smilauer P (2002) CANOCO reference manual and CanoDraw for Windows user’s guide: software for canonical community ordination (version 4.5), NYGoogle Scholar
  42. Vera MS, Di Fiori E, Lagomarsino L, Sinistro R, Escaray R, Iummato MM, Juárez A, de Molina Ríos, Mdel C, Tell C, Pizarro H (2012) Direct and indirect effects of the glyphosate formulation Glifosato Atanor® on freshwater microbial communities. Ecotoxicology 21:1805–1816CrossRefGoogle Scholar
  43. Volkman JK, Barrett SM, Blackburn SI (1999) Fatty acids and hydroxy fatty acids in three species of freshwater eustigmatophytes. J Phycol 35:1005–1012CrossRefGoogle Scholar
  44. Wang YS, Lou ZP, Sun CS, Wu ML, Han SH (2006) Multivariate statistical analysis of water quality and phytoplankton characteristics in Daya Bay, China, from 1999 to 2002. Oceanologia 48:193–211Google Scholar
  45. Wang YS, Lou ZP, Sun CC, Sun S (2008) Ecological environment changes in Daya Bay, China, from 1982 to 2004. Mar Pollut Bull 56:1871–1879CrossRefGoogle Scholar
  46. Wang YS, Sun CC, Lou ZP, Wang H, Mitchell BG, Wu ML, Sun ZX (2011) Identification of water quality and benthos characteristics in Daya Bay, China, from 2001 to 2004. Oceanol Hydrobiol St 40:82–95CrossRefGoogle Scholar
  47. Watson GM, Tabita FR (1997) Microbial ribulose 1, 5-bisphosphate carboxylase/oxygenase: a molecule for phylogenetic and enzymological investigation. FEMS Microbiol Lett 146:13–22CrossRefGoogle Scholar
  48. Watson GM, Yu JP, Tabita FR (1999) Unusual ribulose 1, 5-bisphosphate carboxylase/oxygenase of anoxic Archaea. J Bacteriol 181:1569–1575Google Scholar
  49. Wawrik B, Paul JH (2004) Phytoplankton community structure and productivity along the axis of the Mississippi River plume in oligotrophic Gulf of Mexico waters. Aquat Microb Ecol 35:185–196CrossRefGoogle Scholar
  50. Wawrik B, Paul JH, Campbell L, Griffin D, Houchin L, Fuentes-Ortega A, Muller-Karger FE (2003) Vertical structure of the phytoplankton community associated with a coastal plume in the Gulf of Mexico. Mar Ecol Prog Ser 251:87–101CrossRefGoogle Scholar
  51. Yang YH, Jiao NZ (2004) Dynamics of picoplankton in the Nansha Islands area of the South China Sea. Acta Ecol Sin 23:493–504Google Scholar
  52. Zimmermann J, Jahn R, Gemeinholzer B (2011) Barcoding diatoms: evaluation of the V4 subregion on the 18S rRNA gene, including new primers and protocols. Org Divers Evol 11:173–192CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2015

Authors and Affiliations

  • Zhao-Yu Jiang
    • 1
    • 2
  • You-Shao Wang
    • 1
    • 2
    Email author
  • Hao Cheng
    • 1
  • Jian-Dong Zhang
    • 1
  • Jiao Fei
    • 1
  1. 1.State Key Laboratory of Tropical Oceanography, South China Sea Institute of OceanologyChinese Academy of SciencesGuangzhouChina
  2. 2.Daya Bay Marine Biology Research StationChinese Academy of SciencesShenzhenChina

Personalised recommendations