Biogeochemistry

, Volume 83, Issue 1–3, pp 293–309 | Cite as

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

  • Stuart J. Whipple
  • Bernard C. Patten
  • Peter G. Verity
  • Marc E. Frischer
  • Jeremy D. Long
  • Jens C. Nejstgaard
  • Jon T. Anderson
  • Anita  Jacobsen
  • Aud  Larsen
  • Joaquin  Martinez-Martinez
  • Stuart R. Borrett
RESEARCH ARTICLE

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.

Keywords

Conceptual model Life cycle Mesocosm Model-driven research Phaeocystis 

References

  1. Allen AE (2005) Defining the molecular basis for energy balance in marine diatoms under fluctuating environmental conditions. J Phycol 41:1073–1076CrossRefGoogle Scholar
  2. 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 39:247–255Google Scholar
  3. Ayers GP, Gillett RW (2000) DMS and its oxidation products in the remote marine atmosphere. J Sea Res 43:275–286CrossRefGoogle Scholar
  4. Baudoux A-C, Brussaard CPD (2005) Characterization of different viruses infecting the marine harmful algal bloom species Phaeocystis globosa. Virology 341:80–90CrossRefGoogle Scholar
  5. Boalch GT (1987) Recent blooms in the western English Channel. Rapp P-v Reun Cons int Explor Mer 187:94–97Google Scholar
  6. Bratbak G, Jacobsen A, Heldal M (1998a) Viral lysis of Phaeocystis pouchetii and bacterial secondary production. Aquat Microb Ecol 16:11–16Google Scholar
  7. 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 16:1–9Google Scholar
  8. 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 4:859–874CrossRefGoogle Scholar
  9. 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 70:3700–3705CrossRefGoogle Scholar
  10. Canziani GA, Hallam TG (1996) A mathematical model for Phaeocystis sp. dominated plankton community dynamics. I The basic model Nonlinear World 3:19–76Google Scholar
  11. Cariou V, Casotti R, Birrien JL, Vaulot D (1994) The initiation of Phaeocystis colonies. J Plankton Res 16:458–470CrossRefGoogle Scholar
  12. 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 1–45Google Scholar
  13. 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 188:131Google Scholar
  14. 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 487:33–44CrossRefGoogle Scholar
  15. 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 51:919–937CrossRefGoogle Scholar
  16. Guillard RRL, Hargraves PE (1993) Stichochrysis immobilis is a diatom, not a chrysophyte. Phycologia 32:234–236Google Scholar
  17. 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 187:101–111Google Scholar
  18. 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, NorwayGoogle Scholar
  19. Jacobsen A (2002) Morphology, relative DNA content and hypothetical life cycle of Phaeocystis pouchetii (Prymnesiophyceae); with special emphasis on the flagellated cell type. Sarsia 87:338–349CrossRefGoogle Scholar
  20. Jacobsen A, Bratbak G, Heldal M (1996) Isolation and characterization of a virus infecting Phaeocystis pouchetii (Prymnesiphyceae). J Phycol 32:923–927CrossRefGoogle Scholar
  21. 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, SpainGoogle Scholar
  22. Kauffman SA (1993) The origins of order. Self-organization and selection in evolution. Oxford University Press, New YorkGoogle Scholar
  23. Kauffman SA (1995) At home in the Universe. The search for laws of self-organization and complexity. Oxford University Press, New YorkGoogle Scholar
  24. Kayser H (1970) Experimental-ecological investigations on Phaeocystis poucheti (Haptophyceae). Helgol wiss Meeresunters 20:195–212CrossRefGoogle Scholar
  25. Kornmann PV (1955) Beobachtungen an Phaeocystis-Kulturen. Helgol wiss Meeresunters 5:218–233CrossRefGoogle Scholar
  26. 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 209–224Google Scholar
  27. 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 229–245Google Scholar
  28. 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 289:63–78Google Scholar
  29. Lancelot C, Wassmann P, Barth H (1994) Ecology of Phaeocystis-dominated ecosystems. J Mar Syst 5:1–4CrossRefGoogle Scholar
  30. 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 37:77–92CrossRefGoogle Scholar
  31. 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 32:868–872CrossRefGoogle Scholar
  32. 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
  33. 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 ScienceGoogle Scholar
  34. Medlin LK, Zingone A (in press) A review: the genus Phaeocystis and its species. BiogeochemistryGoogle Scholar
  35. Montsant A, Jabbari K, Maheswari U, Bowler C (2005) Comparative genomics of the pennate diatom Phaeodactylum tricornutum. Plant Physiol 137:500–513CrossRefGoogle Scholar
  36. 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 321:99–121Google Scholar
  37. 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 22:2181–2203CrossRefGoogle Scholar
  38. Peperzak L, Gieskes WWC, Duin R, Colijn F (2000b) The vitamin B requirement of Phaeocystis globosa (Prymnesiophyceae). J Plankton Res 22:1529–1537CrossRefGoogle Scholar
  39. Rousseau V, Jacobsen A, Verity P, Whipple S (in press) The life cycle of Phaeocystis: state of knowledge and presumptive role in ecology. Biogeochemistry Google Scholar
  40. Rousseau V, Mathot S, Lancelot C (1990) Calculating carbon biomass of Phaeocystis sp. from microscopic observations Mar Biol 107:305–314CrossRefGoogle Scholar
  41. 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 5:23–39CrossRefGoogle Scholar
  42. Ruardij P, Veldhuis MJW, Brussaard CPD (2005) Modeling the bloom dynamics of the polymorphic phytoplankter Phaeocystis globosa: impact of grazers and viruses. Harmful Algae 4:941–963CrossRefGoogle Scholar
  43. 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 352:514–516CrossRefGoogle Scholar
  44. Stefansson U, Olafsson J (1991) Nutrients and fertility of Icelandic waters. Rit Fiskideildar 12:1–56Google Scholar
  45. Tang KW (2003) Grazing and colony size development in Phaeocystis globosa (Prymnesiophyceae): the role of a chemical signal. J Plankton Res 25:831–842CrossRefGoogle Scholar
  46. Veldhuis MJW, Brussaard CPD, Noordeloos AAM (2005) Living in a Phaeocystis colony: a way to be a successful algal species. J Sea Res 53:841–858Google Scholar
  47. Veldhuis MJW, Colijn F, Venekamp LAH (1986) The spring bloom of Phaeocystis pouchetii (Haptophyceae) in Dutch coastal waters. Neth J Sea Res 20:37–48CrossRefGoogle Scholar
  48. Verity PG (2000) Grazing experiments and model simulations of the role of zooplankton in Phaeocystis food webs. J Sea Res 43:317–343CrossRefGoogle Scholar
  49. Verity PG, Smetacek V (1996) Organism life cycles, predation, and the structure of marine pelagic ecosystems. Mar Ecol Prog Ser 130:277–293Google Scholar
  50. 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 10:749–766CrossRefGoogle Scholar
  51. 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 ResGoogle Scholar
  52. Waldrop MM (1992) Complexity. The emerging science at the edge of order and chaos. Simon and Schuster, New YorkGoogle Scholar
  53. Walker TL, Collet C, Purton S (2005) Algal transgenics in the genomic era. J Phycol 41:1077–1093CrossRefGoogle Scholar
  54. 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 4:823–840CrossRefGoogle Scholar
  55. 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 23:171–182CrossRefGoogle Scholar
  56. 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 57:83–110CrossRefGoogle Scholar
  57. 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 27:495–501CrossRefGoogle Scholar
  58. 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 35:1322–1337CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, Inc. 2007

Authors and Affiliations

  • Stuart J. Whipple
    • 1
    • 2
  • Bernard C. Patten
    • 2
  • Peter G. Verity
    • 1
  • Marc E. Frischer
    • 1
  • Jeremy D. Long
    • 3
  • Jens C. Nejstgaard
    • 4
  • Jon T. Anderson
    • 5
  • Anita  Jacobsen
    • 4
  • Aud  Larsen
    • 4
  • Joaquin  Martinez-Martinez
    • 6
  • Stuart R. Borrett
    • 7
  1. 1.Skidaway Institute of OceanographySavannahUSA
  2. 2.Institute of EcologyUniversity of GeorgiaAthensUSA
  3. 3.Marine Science CenterNortheastern UniversityNahantUSA
  4. 4.Department of BiologyUniversity of BergenBergenNorway
  5. 5.Estuarine Research CenterMorgan State UniversitySt. LeonardUSA
  6. 6.Plymouth Marine LaboratoryPlymouthUK
  7. 7.Computational Learning LaboratoryStanford UniversityStanfordUSA

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