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Comparative study of the composition and genetic diversity of the picoeukaryote community in a Chinese aquaculture area and an open sea area

Published online by Cambridge University Press:  01 March 2016

Xue Song
Affiliation:
College of Marine Life Science, Ocean University of China, Qingdao 266003, P.R. China
Zhimeng Xu
Affiliation:
College of Marine Life Science, Ocean University of China, Qingdao 266003, P.R. China
Qian Liu
Affiliation:
College of Marine Life Science, Ocean University of China, Qingdao 266003, P.R. China
Yan Li
Affiliation:
College of Marine Life Science, Ocean University of China, Qingdao 266003, P.R. China
Yu Ma
Affiliation:
College of Marine Life Science, Ocean University of China, Qingdao 266003, P.R. China
Jian Wang
Affiliation:
College of Marine Life Science, Ocean University of China, Qingdao 266003, P.R. China
Mengran Sun
Affiliation:
College of Marine Life Science, Ocean University of China, Qingdao 266003, P.R. China
Hongbing Shao
Affiliation:
College of Marine Life Science, Ocean University of China, Qingdao 266003, P.R. China
Hui Sun
Affiliation:
College of Marine Life Science, Ocean University of China, Qingdao 266003, P.R. China
Gill Malin
Affiliation:
School of Environmental Sciences, University of East Anglia, Norwich NR4 7TJ, UK
Yong Jiang*
Affiliation:
College of Marine Life Science, Ocean University of China, Qingdao 266003, P.R. China
Min Wang*
Affiliation:
College of Marine Life Science, Ocean University of China, Qingdao 266003, P.R. China
*
Correspondence should be addressed to:Y. Jiang and M. Wang, College of Marine Life Science, Ocean University of China, Qingdao 266003, P.R. China email: mingwang@ouc.edu.cnyongjiang@ouc.edu.cn
Correspondence should be addressed to:Y. Jiang and M. Wang, College of Marine Life Science, Ocean University of China, Qingdao 266003, P.R. China email: mingwang@ouc.edu.cnyongjiang@ouc.edu.cn

Abstract

Picoeukaryotes (<2–3 μm) perform key roles for the functioning of marine ecosystems, but little is known regarding the composition and diversity of picoeukaryotes in aquaculture areas. In this study, the Illumina MiSeq platform was used for sequencing the V4 variable region within the 18S rDNA gene to analyse genetic diversity and relative abundance of picoeukaryotic communities in the Qinhuangdao scallop cultivation area of the Bohai Sea. The community was dominated by three super groups, the alveolates (54%), stramenopiles (41%) and chlorophytes (3%), and three groups, dinoflagellates (54%), pelagomonadales (40%) and prasinophytes (3%). Furthermore, a contrasting station with open water away from the eutrophic aquaculture area was chosen. The communities collected from the two stations exhibited significant differences, with higher diversity in the aquaculture area. These results provide the first snapshot of the picoeukaryotic diversity in surface waters of the Qinhuangdao scallop cultivation area, and basic data for future studies on picoeukaryote community in an aquaculture region.

Type
Research Article
Copyright
Copyright © Marine Biological Association of the United Kingdom 2016 

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References

REFERENCES

Acosta, F., Ngugi, D.K. and Stingl, U. (2013) Diversity of picoeukaryotes at an oligotrophic site off the Northeastern Red Sea Coast. Aquatic Biosystems 1, 916.Google Scholar
Amato, K.R., Yeoman, C.J., Kent, A., Righini, N., Carbonero, F., Estrada, A., Gaskins, H.R., Stumpf, R.M., Yildirim, S., Torralba, M., Gillis, M., Wilson, B.A., Nelson, K.E., White, B.A. and Leigh, S.R. (2013) Habitat degradation impacts black howler monkey (Alouatta pigra) gastrointestinal microbiomes. ISME Journal 7, 13441353.CrossRefGoogle ScholarPubMed
Andersen, R.A., Bidigare, R.R., Keller, M.D. and 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 Research Part II: Topical Studies in Oceanography 43, 517537.CrossRefGoogle Scholar
Bai, X., Adolf, J.E., Bachvaroff, T., Place, A.R. and Coats, D.W. (2007) The interplay between host toxins and parasitism by Amoebophyra . Harmful Algae 6, 670678.CrossRefGoogle Scholar
Bricelj, V.M. and Lonsdale, D.J. (1997) Aureococcus anophagefferens: causes and ecological consequences of brown tides in US mid-Atlantic coastal waters. Limnology and Oceanography 42, 10231038.CrossRefGoogle Scholar
Bricelj, V., MacQuarrie, S. and Schaffner, R. (2001) Differential effects of Aureococcus anophagefferens isolates (“brown tide”) in unialgal and mixed suspensions on bivalve feeding. Marine Biology 139, 605616.Google Scholar
Boström, K.H., Simu, K., Hagström, Å. and Riemann, L. (2004) Optimization of DNA extraction for quantitative marinebacterioplankton community analysis. Limnology and Oceanography: Methods 2, 365373.Google Scholar
Cao, L., Wang, W., Yang, Y., Yang, C., Yuan, Z., Xiong, S. and Diana, J. (2007) Environmental impact of aquaculture and countermeasures to aquaculture pollution in China. Environmental Science and Pollution Research 14, 452462.Google ScholarPubMed
Caron, D.A., Countway, P.D., Jones, A.C., Kim, D.Y. and Schnetzer, A. (2012) Marine protistan diversity. Annual Review of Marine Science 4, 467493.CrossRefGoogle ScholarPubMed
Caron, D.A., Peele, E.R., Lim, E.L. and Dennett, M.R. (1999) Picoplankton and nanoplankton and their trophic coupling in surface waters of the Sargasso Sea south of Bermuda. Limnology and Oceanography 44, 259272.CrossRefGoogle Scholar
Chambouvet, A., Morin, P., Marie, D. and Guillou, L. (2008) Control of toxic marine dinoflagellate blooms by serial parasitic killers. Science 322, 12541257.CrossRefGoogle ScholarPubMed
Cheung, M.K., Au, C.H., Chu, K.H., Kwan, H.S. and Wong, C.K. (2010) Composition and genetic diversity of picoeukaryotes in subtropical coastal waters as revealed by 454 pyrosequencing. ISME Journal 4, 10531059.CrossRefGoogle Scholar
Cheung, M.K., Chu, K.H., Li, C.P., Kwan, H.S. and Wong, C.K. (2008) Genetic diversity of picoeukaryotes in a semi-enclosed harbour in the subtropical western Pacific Ocean. Aquatic Microbial Ecology 53, 295.CrossRefGoogle Scholar
Coats, D.W. (1999) Parasitic life styles of marine dinoflagellates. Journal of Eukaryotic Microbiology 46, 402409.CrossRefGoogle Scholar
Curds, C.R. (1992) Protozoa and the water industry. Cambridge: Cambridge University Press.Google Scholar
DeYoe, H.R., Chan, A.M. and Suttle, C.A. (1995) Phylogeny of Aureococcus anophagefferens and a morphologically similar bloom-forming alga from Texas as determined by 18S ribosomal RNA sequence analysis. Journal of Phycology 31, 413418.CrossRefGoogle Scholar
Díez, B., Pedrós-Alió, C. and Massana, R. (2001) Study of genetic diversity of eukaryotic picoplankton in different oceanic regions by small-subunit rRNA gene cloning and sequencing. Applied and Environmental Microbiology 67, 29322941.CrossRefGoogle ScholarPubMed
Drebes, G. (1984) Life-cycle and host specificity of marine parasitic dinophytes. Helgolander Meeresuntersuchungen 37, 603622.Google Scholar
Doherty, M., Costas, B.A., McManus, G.B. and Katz, L.A. (2007) Culture-independent assessment of planktonic ciliate diversity in coastal northwest Atlantic waters. Aquatic Microbial Ecology 48, 141.CrossRefGoogle Scholar
Gobler, C.J. and Sunda, W.G. (2012) Ecosystem disruptive algal blooms of the brown tide species, Aureococcus anophagefferens and Aureoumbra lagunensis . Harmful Algae 14, 3645.CrossRefGoogle Scholar
Guillou, L., Viprey, M., Chambouvet, A., Welsh, R.M., Kirkham, A.R., Massana, R., Scanlan, D.J. and Worden, A.Z. (2008) Widespread occurrence and genetic diversity of marine parasitoids belonging to Syndiniales (Alveolata). Environmental Microbiology 10, 33493365.CrossRefGoogle ScholarPubMed
Hammer, Ø., Harper, D.A.T. and Ryan, P.D. (2001) PAST: Paleontological Statistics Software Package for education and data analysis. Palaeontolia Electronica 4, 9.Google Scholar
Herfort, L., Peterson, T.D., Prahl, F.G., McCue, L.A., Needoba, J.A., Crump, B.C., Roegner, G.C., Campbell, V. and Zuber, P. (2012) Red waters of Myrionecta rubra are biogeochemical hotspots for the Columbia River estuary with impacts on primary/secondary productions and nutrient cycles. Estuaries and Coasts 35, 878891.CrossRefGoogle Scholar
Jardillier, L., Zubkov, M.V., Pearman, J. and Scanlan, D.J. (2010) Significant CO2 fixation by small prymnesiophytes in the subtropical and tropical northeast Atlantic Ocean. ISME Journal 4, 11801192.CrossRefGoogle ScholarPubMed
Johansson, M. and Coats, D.W. (2002) Ciliate grazing on the parasite Amoebophrya sp. decreases infection of the red-tide dinoflagellate Akashiwo sanguinea . Aquatic Microbial Ecology 28, 6978.CrossRefGoogle Scholar
Kyewalyanga, M., Sathyendranath, S. and Platt, T. (2002) Effect of Mesodinium rubrum (= Myrionecta rubra) on the action and absorption spectra of phytoplankton in a coastal marine inlet. Journal of Plankton Research 24, 687702.CrossRefGoogle Scholar
López-García, P., Rodriguez-Valera, F., Pedrós-Alió, C. and Moreira, D. (2001) Unexpected diversity of small eukaryotes in deep-sea Antarctic plankton. Nature 409, 603607.CrossRefGoogle ScholarPubMed
Lovejoy, C., Vincent, W.F., Bonilla, S., Roy, S., Martineau, M.J., Terrado, R., Potvin, M., Massana, R. and Pedrós-Alió, C. (2007) Distribution, phylogeny, and growth of cold-adapted picoprasinophyte in arctic seas. Journal of Phycology 43, 7889.CrossRefGoogle Scholar
Lu, D., Qi, Y., Gu, H., Dai, X., Wang, H., Gao, Y., Shen, P., Zhang, Q., Yu, R. and Lu, S. (2014) Causative species of harmful algal blooms in Chinese coastal waters. Algological Studies 145, 145168.CrossRefGoogle Scholar
Massana, R. (2011) Eukaryotic picoplankton in surface oceans. Annual Review of Microbiology 65, 91110.CrossRefGoogle ScholarPubMed
Muller-Feuga, A. (2000) The role of microalgae in aquaculture: situation and trends. Journal of Applied Phycology 12, 527534.CrossRefGoogle Scholar
Moon-van der Staay, S.Y., De Wachter, R. and Vaulot, D. (2001) Oceanic 18S rDNA sequences from picoplankton reveal unsuspected eukaryotic diversity. Nature 409, 607610.CrossRefGoogle ScholarPubMed
Not, F., Massana, R., Latasa, M., Marie, D., Colson, C., Eikrem, W., Pedrós-Alió, C., Vaulot, D. and Simon, N. (2005) Late summer community composition and abundance of photosynthetic picoeukaryotes in Norwegian and Barents Seas. Limnology and Oceanography 50, 16771686.CrossRefGoogle Scholar
Not, F., Valentin, K., Romari, K., Lovejoy, C., Massana, R., Töbe, K., Vaulot, D. and Medlin, L.K. (2007) Picobiliphytes: a marine picoplanktonic algal group with unknown affinities to other eukaryotes. Science 315, 253255.CrossRefGoogle ScholarPubMed
Naylor, R.L., Goldburg, R.J., Primavera, J.H., Kautsky, N., Beveridge, M.C., Clay, J., Folke, C., Lubchenco, J., Mooney, H. and Troell, M. (2000) Effect of aquaculture on world fish supplies. Nature 405, 10171024.CrossRefGoogle ScholarPubMed
Partensky, F., Guillou, L., Simon, N. and Vaulot, D. (1997) Recent advances in the use of molecular techniques to assess the genetic diversity of marine photosynthetic microorganisms. Vie et Milieu 47, 367374.Google Scholar
Philippot, L., Spor, A., Hénault, C., Bru, D., Bizouard, F., Jones, C.M., Sarr, A. and Maron, P.A. (2013) Loss in microbial diversity affects nitrogen cycling in soil. ISME Journal 7, 16091619.CrossRefGoogle ScholarPubMed
Rocke, E., Jing, H. and Liu, H. (2013) Phylogenetic composition and distribution of picoeukaryotes in the hypoxic northwestern coast of the Gulf of Mexico. Microbiologyopen 2, 130143.CrossRefGoogle ScholarPubMed
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., Robinson, C.J., Sahl, J.W., Stres, B., Thallinger, G.G., Van Horn, D.J. and Weber, C.F. (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Applied and Environmental Microbiology 75, 75377541.CrossRefGoogle ScholarPubMed
Sherr, E. and Sherr, B. (2008) Understanding roles of microbes in marine pelagic food webs: a brief history. In Kirchman, D.L. (ed.) Microbial Ecology of the Oceans 2nd edition. Hoboken, NJ: John Wiley & Sons, 2744.CrossRefGoogle Scholar
Siano, R., Alves-de-Souza, C., Foulon, E., Bendif, E.M., Simon, N., Guillou, L. and Not, F. (2011) Distribution and host diversity of Amoebophryidae parasites across oligotrophic waters of the Mediterranean Sea. Biogeosciences 8, 267278.CrossRefGoogle Scholar
Simon, N., Barlow, R.G., Marie, D., Partensky, F. and Vaulot, D. (1994) Characterization of oceanic photosynthetic picoeukaryotes by flow cytometry. Journal of Phycology 30, 922935.CrossRefGoogle Scholar
Smayda, T.J. and Reynolds, C.S. (2003) Strategies of marine dinoflagellate survival and some rules of assembly. Journal of Sea Research 49, 95106.CrossRefGoogle Scholar
Sun, H., Wang, M., Wang, J., Song, X., Shao, H. and Zhen, Y. (2014) Effect of aquaculture activities on distribution of ultraplankton. Oceanologia et Limnologia Sinica 6, 12721278. [In Chinese with English abstract.]Google Scholar
Stoeck, T., Bass, D., Nebel, M., Christen, R., Jones, M.D., Breiner, H.W. and Richards, T.A. (2010) Multiple marker parallel tag environmental DNA sequencing reveals a highly complex eukaryotic community in marine anoxic water. Molecular Ecology 19, 2131.CrossRefGoogle ScholarPubMed
Taylor, F.J.R. (1984) Toxic dinoflagellates: taxonomic and biogeographic aspects with emphasis on Protogonyaulax. In ACS Symposium series 262, 7797.Google Scholar
Thomsen, H.A. (1986) A survey of the smallest eukaryotic organisms of the marine phytoplankton. Canadian Bulletin of Fisheries and Aquatic Sciences 214, 121158.Google Scholar
Viprey, M., Guillou, L., Ferréol, M. and Vaulot, D. (2008) Wide genetic diversity of picoplanktonic green algae (Chloroplastida) in the Mediterranean Sea uncovered by a phylum-biased PCR approach. Environmental Microbiology 10, 18041822.CrossRefGoogle ScholarPubMed
Wang, D., He, E., Liu, G. and Liu, Q. (2013) Relationship between red tide organisms and environmental factors in the Beidaihe waters of the Qinhuangdao. Marine Forecasts 5, 17. [In Chinese with English abstract.]Google Scholar
Wu, W., Huang, B., Liao, Y. and Sun, P. (2014) Picoeukaryotic diversity and distribution in the subtropical–tropical South China Sea. FEMS Microbiology Ecology 89, 563579.CrossRefGoogle ScholarPubMed
Yih, W. and Coats, D.W. (2000) Infection of Gymnodinium sanguineum by the Dinoflagellate Amoebophrya sp.: effect of nutrient environment on parasite generation time, reproduction, and infectivity. Journal of Eukaryotic Microbiology 47, 504510.CrossRefGoogle ScholarPubMed
Zingone, A. and Enevoldsen, H.O. (2000) The diversity of harmful algal blooms: a challenge for science and management. Ocean and Coastal Management 43, 725748.CrossRefGoogle Scholar
Zöllner, E., Hoppe, H.G., Sommer, U. and Jürgens, K. (2009) Effect of zooplankton-mediated trophic cascades on marine microbial food web components (bacteria, nanoflagellates, ciliates). Limnology and Oceanography 54, 262275.CrossRefGoogle Scholar
Zhang, Q.C., Qiu, L.M., Yu, R.C., Kong, F.Z., Wang, Y.F., Yan, T., Gobler, C.J. and Zhou, M.J. (2012) Emergence of brown tides caused by Aureococcus anophagefferens Hargraves et Sieburth in China. Harmful Algae 19, 117124.CrossRefGoogle Scholar
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