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Gaining integrated understanding of Phaeocystis spp. (Prymnesiophyceae) through model-driven laboratory and mesocosm studies

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Abstract

Knowledge of the complex life cycle of Phaeocystis is a key to understanding its role in marine ecosystems and global biogeochemistry. An existing life cycle model was modified and used to integrate understanding of the Phaeocystis life cycle. In model-driven research, models expose gaps in our understanding, empirical studies ensue, and feedback improves understanding. Following this scheme, three facets of the life cycle model were examined here. With four exceptions, the empirical studies described have been presented in other literature citations. The first facet involved testing for the existence of a process or producing its description. These studies included: demonstration of in vitro colony division in Phaeocystis pouchetii, description of in vitro change in colony shape for P. pouchetii associated with senescence, determining which P. pouchetii life stage is vulnerable to viral infection and lysis, and an experiment designed to determine whether the sediment could be a source of new Phaeocystis colonies to overlying waters; results suggested that more-detailed investigation of benthic particles as a physical substrate for colony formation is warranted. The second facet involved investigation of process rate quantification or process control parameters. Process rate quantification included measurements of colony division rate and growth rate using mesocosm-derived colonies. Process control experiments included testing diatom frustule enhancement of P. pouchetii colony formation from solitary cells, and investigation of mesozooplanktonic suppression and microzooplanktonic enhancement of Phaeocystis globosa colony formation by planktonic grazer infochemicals. The third facet pertained to the molecular identification of genetic differences between single cells and colonies of P. globosa. These studies were designed to provide insight to the question of control factors involved in the transition between single cell and colonial life stages. The life cycle model provided a ready place to incorporate new insights and understanding from empirical studies into an existing model, and can be used to improve simulation models of the direct and indirect effects of Phaeocystis on global biogeochemistry.

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References

  • Allen AE (2005) Defining the molecular basis for energy balance in marine diatoms under fluctuating environmental conditions. J Phycol 41:1073–1076

    Article  Google Scholar 

  • Allen AE, Booth MG, Verity PG, Frischer ME (2005) Influence of nitrate availability on the distribution and abundance of heterotrophic bacterial nitrate assimilation genes in the Barents Sea during summer. Aquat Microb Ecol 39:247–255

    Google Scholar 

  • Ayers GP, Gillett RW (2000) DMS and its oxidation products in the remote marine atmosphere. J Sea Res 43:275–286

    Article  Google Scholar 

  • Baudoux A-C, Brussaard CPD (2005) Characterization of different viruses infecting the marine harmful algal bloom species Phaeocystis globosa. Virology 341:80–90

    Article  Google Scholar 

  • Boalch GT (1987) Recent blooms in the western English Channel. Rapp P-v Reun Cons int Explor Mer 187:94–97

    Google Scholar 

  • Bratbak G, Jacobsen A, Heldal M (1998a) Viral lysis of Phaeocystis pouchetii and bacterial secondary production. Aquat Microb Ecol 16:11–16

    Google Scholar 

  • Bratbak G, Jacobsen A, Heldal M, Nagasaki K, Thingstad F (1998b) Viral production in Phaeocystis pouchetii and its relation to host cell growth and nutrition. Aquat Microb Ecol 16:1–9

    Google Scholar 

  • Brussaard CPD, Kuipers B, Veldhuis MJW (2005) A mesocosm study of Phaeocystis globosa population dynamics I. Regulatory role of viruses in bloom control. Harmful Algae 4:859–874

    Article  Google Scholar 

  • Brussaard CPD, Short SM, Frederickson CM, Suttle CA (2004) Isolation and phylogenetic analysis of novel viruses infecting the phytoplankton Phaeocystis globosa (Prymnesiophyseae). Appl Environ Microbiol 70:3700–3705

    Article  Google Scholar 

  • Canziani GA, Hallam TG (1996) A mathematical model for Phaeocystis sp. dominated plankton community dynamics. I The basic model Nonlinear World 3:19–76

    Google Scholar 

  • Cariou V, Casotti R, Birrien JL, Vaulot D (1994) The initiation of Phaeocystis colonies. J Plankton Res 16:458–470

    Article  Google Scholar 

  • Davidson AT, Marchant HJ (1992) The biology and ecology of Phaeocystis (Prymnesiophyceae). In: Round FE, Chapman DJ (eds) Progress in Phycological Research. Biopress Ltd, Bristol, UK pp 1–45

    Google Scholar 

  • Eilertsen HC (1989) Phaeocystis pouchetii (Hariot) Lagerheim, a key species in Arctic marine ecosystems: Life history and physiology. Rapp P-v Reun Cons int Explor Mer 188:131

    Google Scholar 

  • Frischer ME, Hansen AS, Wyllie JA, Wimbush J, Murray J, Nierzwicki-Bauer SA (2002) Specific amplification of the 18S rRNA gene as a method to detect zebra mussel (Dreissena polymorpha) larvae in plankton samples. Hydrobiologia 487:33–44

    Article  Google Scholar 

  • Gabric AJ, Matrai PA, Vernet M (1999) Modelling the production of dimethylsulfide during the vernal blooms in the Barents Sea. Tellus Ser B Chem Phys Meteorol 51:919–937

    Article  Google Scholar 

  • Guillard RRL, Hargraves PE (1993) Stichochrysis immobilis is a diatom, not a chrysophyte. Phycologia 32:234–236

    Google Scholar 

  • Hamm CE, Simson DA, Merkel R, Smetacek V (1999) Colonies of Phaeocystis globosa are protected by a thin but tough skin. Mar Ecol Prog Ser 187:101–111

    Google Scholar 

  • Jacobsen A (2000) New aspects of bloom dynamics of Phaeocystis pouchetii (Haptophyta) in Norwegian waters. PhD Dissertation. Department of Fisheries and Marine Biology (45pp). University of Bergen, Bergen, Norway

  • Jacobsen A (2002) Morphology, relative DNA content and hypothetical life cycle of Phaeocystis pouchetii (Prymnesiophyceae); with special emphasis on the flagellated cell type. Sarsia 87:338–349

    Article  Google Scholar 

  • Jacobsen A, Bratbak G, Heldal M (1996) Isolation and characterization of a virus infecting Phaeocystis pouchetii (Prymnesiphyceae). J Phycol 32:923–927

    Article  Google Scholar 

  • Jacobsen A, Martínez-Martínez J, Verity P, Frischer ME, Sandaa RA, Larsen A (2005) Are colonies or colonial cell of Phaoecystis pouchetii (Prymnesiophyceae) suseptible to virus infection? American society of limnology and oceanography, summer meeting. ASLO, Santiago de Compostela, Spain

    Google Scholar 

  • Kauffman SA (1993) The origins of order. Self-organization and selection in evolution. Oxford University Press, New York

    Google Scholar 

  • Kauffman SA (1995) At home in the Universe. The search for laws of self-organization and complexity. Oxford University Press, New York

    Google Scholar 

  • Kayser H (1970) Experimental-ecological investigations on Phaeocystis poucheti (Haptophyceae). Helgol wiss Meeresunters 20:195–212

    Article  Google Scholar 

  • Kornmann PV (1955) Beobachtungen an Phaeocystis-Kulturen. Helgol wiss Meeresunters 5:218–233

    Article  Google Scholar 

  • Lancelot C, Keller MD, Rousseau V, Smith WO, Mathot S (1998) Autecology of the marine Haptophyte Phaeocystis sp. In: Anderson DM, Cembella AD, Hallegraeff GM (eds) Physiological ecology of harmful algal blooms. Springer-Verlag, Berlin pp 209–224

    Google Scholar 

  • Lancelot C, Rousseau V (1994) Ecology of Phaeocystis: the key role of colony forms. In: Green JC, Leadbeater BSC (eds) The haptophyte algae. Clarendon Press, Oxford pp 229–245

    Google Scholar 

  • Lancelot C, Spitz Y, Gypens N, Ruddick K, Becquevort S, Rousseau V, Lacroix G, Billen G (2005) Modelling diatom and Phaeocystis blooms and nutrient cycles in the Southern Bight of the North Sea: the MIRO model. Mar Ecol Prog Ser 289:63–78

    Google Scholar 

  • Lancelot C, Wassmann P, Barth H (1994) Ecology of Phaeocystis-dominated ecosystems. J Mar Syst 5:1–4

    Article  Google Scholar 

  • Lange M, Chen Y-Q, Medlin LK (2002) Molecular genetic delineation of Phaeocystis species (Prymnesiophyceae) using coding and non-coding regions of nuclear and plastid genomes. Eur J Phycol 37:77–92

    Article  Google Scholar 

  • Lange M, Laure G, Vaulot D, Simon N, Amann RI, Ludwig W (1996) Identification of the class Prymnesiophyceae and the genus Phaeocystis with ribosomal RNA-targeted nucleic acid probes detected by flow cytometry. J Phycol 32:868–872

    Article  Google Scholar 

  • Long JD (2004) Plasticity of consumer-prey interactions in the sea: chemical signaling, learned aversion, and ecological consequences. PhD Dissertation. Department of Biology (119pp). Georgia Institute of Technology, Atlanta, GA, USA. URL link: http://www.etd.gatech.edu/theses/available/etd-11182004–164652/unrestricted/long_jeremy_d_200412_phd.pdf

  • Long JD, Smalley GW, Barsby T, Anderson JT, and Hay ME (submitted) Chemical cues induce consumer-specific defences in a bloom-forming marine phytoplankton. Proceedings of the National Academy of Science

  • Medlin LK, Zingone A (in press) A review: the genus Phaeocystis and its species. Biogeochemistry

  • Montsant A, Jabbari K, Maheswari U, Bowler C (2005) Comparative genomics of the pennate diatom Phaeodactylum tricornutum. Plant Physiol 137:500–513

    Article  Google Scholar 

  • Nejstgaard JC, Frischer ME, Verity PG, Anderson JT, Jacobsen A, Zirbel MJ, Larsen A, Martínez-Martínez J, Sazhin AF, Walters T, Bronk DA, Whipple SJ, Borrett SR, Patten BC, Long JD (2006) Plankton development and trophic transfer in sea water enclosures added nutrients and Phaeocystis pouchetii. Mar Ecol Prog Ser 321:99–121

    Google Scholar 

  • Peperzak L, Colijn F, Vrieling EG, Gieskes WWC, Peeters JCH (2000a) Observations of flagellates in colonies of Phaeocystis globosa (Prymnesiophyceae); a hypothesis for their position in the life cycle. J Plankton Res 22:2181–2203

    Article  Google Scholar 

  • Peperzak L, Gieskes WWC, Duin R, Colijn F (2000b) The vitamin B requirement of Phaeocystis globosa (Prymnesiophyceae). J Plankton Res 22:1529–1537

    Article  Google Scholar 

  • Rousseau V, Jacobsen A, Verity P, Whipple S (in press) The life cycle of Phaeocystis: state of knowledge and presumptive role in ecology. Biogeochemistry

  • Rousseau V, Mathot S, Lancelot C (1990) Calculating carbon biomass of Phaeocystis sp. from microscopic observations Mar Biol 107:305–314

    Article  Google Scholar 

  • Rousseau V, Vaulot D, Casotti R, Cariou V, Lenz J, Gunkel J, Baumann M (1994) The life cycle of Phaeocystis (Prymnesiophyceae): evidence and hypotheses. J Mar Syst 5:23–39

    Article  Google Scholar 

  • Ruardij P, Veldhuis MJW, Brussaard CPD (2005) Modeling the bloom dynamics of the polymorphic phytoplankter Phaeocystis globosa: impact of grazers and viruses. Harmful Algae 4:941–963

    Article  Google Scholar 

  • Smith Jr WO, Codispoti LA, Nelson DM, Manley T, Buskey EJ, Niebauer HJ, Cota GF (1991) Importance of Phaeocystis blooms in the high-latitude ocean carbon cycle. Nature 352:514–516

    Article  Google Scholar 

  • Stefansson U, Olafsson J (1991) Nutrients and fertility of Icelandic waters. Rit Fiskideildar 12:1–56

    Google Scholar 

  • Tang KW (2003) Grazing and colony size development in Phaeocystis globosa (Prymnesiophyceae): the role of a chemical signal. J Plankton Res 25:831–842

    Article  Google Scholar 

  • Veldhuis MJW, Brussaard CPD, Noordeloos AAM (2005) Living in a Phaeocystis colony: a way to be a successful algal species. J Sea Res 53:841–858

    Google Scholar 

  • Veldhuis MJW, Colijn F, Venekamp LAH (1986) The spring bloom of Phaeocystis pouchetii (Haptophyceae) in Dutch coastal waters. Neth J Sea Res 20:37–48

    Article  Google Scholar 

  • Verity PG (2000) Grazing experiments and model simulations of the role of zooplankton in Phaeocystis food webs. J Sea Res 43:317–343

    Article  Google Scholar 

  • Verity PG, Smetacek V (1996) Organism life cycles, predation, and the structure of marine pelagic ecosystems. Mar Ecol Prog Ser 130:277–293

    Google Scholar 

  • Verity PG, Villareal TA, Smayda TJ (1988) Ecological investigations of blooms of colonial Phaeocystis pouchetii. II. The role of life-cycle phenomena in bloom termination. J Plankton Res 10:749–766

    Article  Google Scholar 

  • Verity PG, Whipple SJ, Nejstgaard JC, and Alderkamp A-C (in press) Colony size, cell density, carbon and nitrogen contents of Phaeocystis pouchetii from western Norway. J Plankton Res

  • Waldrop MM (1992) Complexity. The emerging science at the edge of order and chaos. Simon and Schuster, New York

    Google Scholar 

  • Walker TL, Collet C, Purton S (2005) Algal transgenics in the genomic era. J Phycol 41:1077–1093

    Article  Google Scholar 

  • Wassmann P, Ratkova T, Reigstad M (2005) The contribution of single and colonial cells of Phaecystis pouchetii to spring and summer blooms in the north-eastern North Atlantic. Harmful Algae 4:823–840

    Article  Google Scholar 

  • Weisse T, Grimm N, Hickel W, Martens P (1986) Dynamics of Phaeocystis pouchetii blooms in the Wadden Sea of Sylt (German Bight, North Sea). Estuar Coast Shelf Sci 23:171–182

    Article  Google Scholar 

  • Whipple SJ, Patten BC, Verity PG (2005a) Life cycle of the marine alga Phaeocystis: a conceptual model to summarize literature and guide research. J Mar Syst 57:83–110

    Article  Google Scholar 

  • Whipple SJ, Patten BC, Verity PG (2005b) Colony growth and evidence for colony multiplication in Phaeocystis pouchetii (Prymnesiophyceae) isolated from mesocosm blooms. J Plankton Res 27:495–501

    Article  Google Scholar 

  • Zingone A, Chretiennot-Dinet M-J, Lange M, Medlin L (1999) Morphological and genetic characterization of Phaeocystis cordata and P. jahnii (Prymnesiophyceae), two new species from the Mediterranean Sea. J Phycol 35:1322–1337

    Article  Google Scholar 

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Acknowledgements

The authors would like to thank T. Sorlie, A. Aadnesen, and H. Gjertsen of the University of Bergen Marine Biological Station for assistance during mesocosm experiments. We thank current and former Skidaway Institute of Oceanography staff: M. Zirbel, T. Walters, J. Danforth, K. Kohlberg, G. Smalley, D. Heaton, J. Brofft, and R. Hristov. We also thank current and former Georgia Institute of Technology student and faculty members: T. Barsby and M. Hay. Funding was provided by US National Science Foundation grant OPP-00-83381. This paper is a contribution to the SCOR WG 120 “Phaeocystis, major link in the biochemical cycling of climate-relevant elements”.

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Whipple, S., Patten, B., Verity, P. et al. Gaining integrated understanding of Phaeocystis spp. (Prymnesiophyceae) through model-driven laboratory and mesocosm studies. Biogeochemistry 83, 293–309 (2007). https://doi.org/10.1007/s10533-007-9089-z

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  • DOI: https://doi.org/10.1007/s10533-007-9089-z

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