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Phaeocystis

Phaeocystis is a genus of algae belonging to the Prymnesiophyte class and to the larger division of Haptophyta.[1] It is a widespread marine phytoplankton and can function at a wide range of temperatures (eurythermal) and salinities (euryhaline).[2] Members of this genus live in the open ocean, as well as in sea ice.[3] It has a polymorphic life cycle, ranging from free-living cells to large colonies.[2]

Phaeocystis
Phaeocystis globosa
Scientific classification
Domain:
(unranked):
Class:
Order:
Phaeocystales
Family:
Phaeocystaceae
Genus:
Phaeocystis

Lagerheim, 1893

The ability to form a floating colony is one of the unique attributes of Phaeocystis – hundreds of cells are embedded in a polysaccharide gel matrix, which can increase massively in size during blooms.[3] The largest Phaeocystis blooms form in the polar seas: P. pouchetii in the north and P. antarctica in the south.[1] This intense Phaeocystis productivity generally persists for about a three-month period, spanning most of the summer in the Southern Hemisphere. Phaeocystis-abundant ecosystems are generally associated with commercially important stocks of crustaceans, molluscs, fish and mammals. Phaeocystis may have negative effects on higher trophic levels in the marine ecosystem, and consequent impacts on human activities (such as fish farming and coastal tourism), by forming odorous foams on beaches during the wane of a bloom.[4]

The ability to form large blooms and its ubiquity make Phaeocystis an important contributor to the ocean carbon cycle.[5][6] In addition, Phaeocystis produces dimethyl sulfide (DMS), a key player in the sulfur cycle.[7][8]

Distribution and life cycle edit

 
Phaeocystis globosa colonies in culture. Scale bar is 500 μm.
 
Phaeocystis antarctica colonies, important phytoplankters of the Ross Sea that dominate early season blooms after the sea ice retreats and export significant carbon.[9]
 
Fluorescent microscopy of photosymbiotic acantharian hosting Phaeocystis symbionts. Red fluorescence is chlorophyll autofluorescence and allows observation of the altered morphology of Phaeocystis chloroplasts. Green fluorescence corresponds to LysoTracker dye, which stains digestive compartments. Symbionts are not being digested.

Free-living forms of Phaeocystis are globally distributed and occur in a variety of marine habitats, including coastal oceans, open oceans, polar seas and sea ice.[10] Seven species are currently assigned to the genus: P. antarctica, P. jahnii, P. globosa, P. pouchetti, P. scrobiculata (not in culture), P. cordata, and P. rex.[11] Three species (P. globosa, P. pouchetii, and P. antarctica) are associated with bloom formation in nutrient-rich areas,[12] which can occur either naturally (e.g. in the Ross Sea, Greenland Sea or the Barents Sea) or due to anthropogenic inputs (e.g. in the Southern Bight of the North Sea or the Persian Gulf). Generally, P. globosa blooms in temperate and tropical waters, whereas P. pouchetii and P. antarctica are better adjusted to the cold temperatures prevailing in Arctic and Antarctic waters, respectively. However, P. pouchetii also tolerates warmer temperatures[13] and has been seen in temperate waters.[14]

Genome comparison has shown that the RUBISCO spacer region (located in the plastid DNA, between two subunits of the enzyme 1,5 -bisphosphate carboxylase) is highly conserved among closely related colonial Phaeocystis species and identical in P. antarctica, P. pouchetii and two warm-temperate strains of P. globosa, with a single base substitution in two cold-temperate strains of P. globosa.[15]

Phaeocystis can exist as either free-living cells or colonies. Free-living cells can show a variety of morphologies, depending on the species. All species can exist as scaled flagellates, and this is the only form that has been observed for P. scrobiculata and P. cordata. Three species have been observed as colonies (P. globosa, P. pouchetii and P. antarctica) and these can also exist as a flagellate devoid of scales and filaments.[16] In colonies of Phaeocystis, the colony skin may provide protection against smaller zooplankton grazers and viruses.[17]

While suspected in other species (P. pouchetii and P. antarctica), a haploid-diploid life cycle has only been observed in P. globosa. In this cycle, sexual reproduction is dominant in colony bloom formation/termination, and two types of vegetative reproduction exist.[16]

Impacts on global ocean edit

The genus Phaeocystis is a major producer of 3-dimethylsulphoniopropionate (DMSP), the precursor of dimethyl sulfide (DMS). Biogenic DMS contributes approximately 1.5×1013 g sulfur to the atmosphere annually and plays a major part in the global sulfur cycle, which can affect cloud formation and, potentially, climate regulation.[1]

Symbiosis edit

Phaeocystis species are endosymbionts to acantharian radiolarians.[18][19] Acantharians collected in different ocean basins host different species of Phaeocystis as their dominant symbionts: P. antarctica is found as the primary symbiont to acantharians in the Southern Ocean and P. cordata and P. jahnii are among the dominant symbionts found in acantharians collected in warm oligotrophic regions of the Indian and Pacific oceans.[18] In addition to the described Phaeocystis species, sequences belonging to the molecular clade Phaeo02 often make up a majority of symbiotic sequences recovered from acantharians in warm-water regions.[18][19] Whether or not this symbiosis represents a true mutualism with both partners benefiting, is debated. [20] Extreme cellular remodeling is observed in symbiotic Phaeocystis, including a drastic increase in chloroplast number and an enlarged central vacuole.[18] [19] This phenotypic change is probably induced by the host to increase photosynthetic output by symbionts, but if it renders symbiotic cells incapable of future cell-division, the symbiosis is a dead end for Phaeocystis.[20] The symbiosis is ecologically relevant because it creates primary production hot spots in low-nutrient regions,[21] but it remains to be determined how the symbiosis has affected Phaeocystis evolution.

References edit

  1. ^ a b c "phaeocystis research". www.phaeocystis.org.
  2. ^ a b Schoemann, Véronique; Becquevort, Sylvie; Stefels, Jacqueline; Rousseau, Véronique; Lancelot, Christiane (2005-01-01). "Phaeocystis blooms in the global ocean and their controlling mechanisms: a review". Journal of Sea Research. Iron Resources and Oceanic Nutrients - Advancement of Global Environmental Simulations. 53 (1–2): 43–66. Bibcode:2005JSR....53...43S. CiteSeerX 10.1.1.319.9563. doi:10.1016/j.seares.2004.01.008.
  3. ^ a b "Welcome to the Phaeocystis antarctica genome sequencing project homepage". www.phaeocystis.org.
  4. ^ Lancelot, C; Mathot, S (1987). "Dynamics of a Phaeocystis-dominated spring bloom in Belgian coastal waters. I. Phytoplanktonic activities and related parameters". Marine Ecology Progress Series. 37: 239–248. Bibcode:1987MEPS...37..239L. doi:10.3354/meps037239.
  5. ^ Smith, Walker O.; Codispoti, Louis A.; Nelson, David M.; Manley, Thomas; Buskey, Edward J.; Niebauer, H. Joseph; Cota, Glenn F. (1991-08-08). "Importance of Phaeocystis blooms in the high-latitude ocean carbon cycle". Nature. 352 (6335): 514–516. Bibcode:1991Natur.352..514S. doi:10.1038/352514a0. S2CID 4369806.
  6. ^ DiTullio, G. R.; Grebmeier, J. M.; Arrigo, K. R.; Lizotte, M. P.; Robinson, D. H.; Leventer, A.; Barry, J. P.; VanWoert, M. L.; Dunbar, R. B. (2000). "Rapid and early export of Phaeocystis antarctica blooms in the Ross Sea, Antarctica". Nature. 404 (6778): 595–598. Bibcode:2000Natur.404..595D. doi:10.1038/35007061. PMID 10766240. S2CID 4409009.
  7. ^ Stefels, J., Van Boekel, W.H.M., 1993. Production of DMS from dissolved DMSP in axenic cultures of the marine phytoplankton species Phaeocystis sp., Mar. Ecol. Prog. Ser. 97, 11 –18.
  8. ^ J, Stefels; L, Dijkhuizen; WWC, Gieskes (1995-07-20). "DMSP-lyase activity in a spring phytoplankton bloom off the Dutch coast, related to Phaeocystis sp. abundance" (PDF). Marine Ecology Progress Series. 123: 235–243. Bibcode:1995MEPS..123..235S. doi:10.3354/meps123235.
  9. ^ Bender, S.J., Moran, D.M., McIlvin, M.R., Zheng, H., McCrow, J.P., Badger, J., DiTullio, G.R., Allen, A.E. and Saito, M.A. (2018) "Colony formation in Phaeocystis antarctica: connecting molecular mechanisms with iron biogeochemistry". Biogeosciences, 15(16): 4923–4942. doi:10.5194/bg-15-4923-2018.
  10. ^ Thomsen, H.A., Buck, K.R., Chavez, F.P., 1994. Haptophytes as components of marine phytoplankton., In: Green, J.C., Leadbeater, B.S.C. (Eds.), The Haptophyte Algae. Clarendon Press, Oxford, UK, pp. 187– 208.
  11. ^ Andersen, Robert A.; Bailey, J. Craig; Decelle, Johan; Probert, Ian (2015-04-03). "Phaeocystis rex sp. nov. (Phaeocystales, Prymnesiophyceae): a new solitary species that produces a multilayered scale cell covering". European Journal of Phycology. 50 (2): 207–222. doi:10.1080/09670262.2015.1024287. ISSN 0967-0262.
  12. ^ Lancelot, C., Keller, M.D., Rousseau, V., Smith Jr., W.O., Mathot, S., 1998. Autecology of the marine haptophyte Phaeocystis sp., In: Anderson, D.M., Cembella, A.D., Hallagraeff, G.M. (Eds.), Physiological Ecology of Harmful Algal blooms, vol. 41. Springer-Verlag, Berlin, pp. 209–224.
  13. ^ Baumann, M.E.M.; Lancelot, C.; Brandini, F.P.; Sakshaug, E.; John, D.M. (1994). "The taxonomic identity of the cosmopolitan prymnesiophyte Phaeocystis: a morphological and ecophysiological approach". Journal of Marine Systems. 5 (1): 5–22. Bibcode:1994JMS.....5....5B. doi:10.1016/0924-7963(94)90013-2.
  14. ^ Philippart, Catharina J. M.; Cadée, Gerhard C.; van Raaphorst, Wim; Riegman, Roel (2000-01-01). "Long-term phytoplankton-nutrient interactions in a shallow coastal sea: Algal community structure, nutrient budgets, and denitrification potential". Limnology and Oceanography. 45 (1): 131–144. Bibcode:2000LimOc..45..131P. doi:10.4319/lo.2000.45.1.0131. ISSN 1939-5590. S2CID 86169774.
  15. ^ Lange, Martin; Chen, Yue-Qin; Medlin, Linda K. (2002-02-01). "Molecular genetic delineation of Phaeocystis species (Prymnesiophyceae) using coding and non-coding regions of nuclear and plastid genomes" (PDF). European Journal of Phycology. 37 (1): 77–92. doi:10.1017/S0967026201003481. ISSN 1469-4433. S2CID 55951287.
  16. ^ a b Rousseau, Véronique; Chrétiennot-Dinet, Marie-Josèphe; Jacobsen, Anita; Verity, Peter; Whipple, Stuart (2007-04-13). "The life cycle of Phaeocystis: state of knowledge and presumptive role in ecology". Biogeochemistry. 83 (1–3): 29–47. doi:10.1007/s10533-007-9085-3. ISSN 0168-2563. S2CID 54973619.
  17. ^ Verity, Peter G.; Brussaard, Corina P.; Nejstgaard, Jens C.; Leeuwe, Maria A. van; Lancelot, Christiane; Medlin, Linda K. (2007-03-16). "Current understanding of Phaeocystis ecology and biogeochemistry, and perspectives for future research" (PDF). Biogeochemistry. 83 (1–3): 311–330. doi:10.1007/s10533-007-9090-6. ISSN 0168-2563. S2CID 55210194.
  18. ^ a b c d Decelle, Johan; Simó, Rafel; Galí, Martí; Vargas, Colomban de; Colin, Sébastien; Desdevises, Yves; Bittner, Lucie; Probert, Ian; Not, Fabrice (2012-10-30). "An original mode of symbiosis in open ocean plankton". Proceedings of the National Academy of Sciences. 109 (44): 18000–18005. Bibcode:2012PNAS..10918000D. doi:10.1073/pnas.1212303109. ISSN 0027-8424. PMC 3497740. PMID 23071304.
  19. ^ a b c Mars Brisbin, Margaret; Grossmann, Mary M.; Mesrop, Lisa Y.; Mitarai, Satoshi (2018). "Intra-host Symbiont Diversity and Extended Symbiont Maintenance in Photosymbiotic Acantharea (Clade F)". Frontiers in Microbiology. 9: 1998. doi:10.3389/fmicb.2018.01998. ISSN 1664-302X. PMC 6120437. PMID 30210473.
  20. ^ a b Decelle, Johan (2013-07-30). "New perspectives on the functioning and evolution of photosymbiosis in plankton". Communicative & Integrative Biology. 6 (4): e24560. doi:10.4161/cib.24560. PMC 3742057. PMID 23986805.
  21. ^ Caron, David A.; Swanberg, Neil R.; Michaels, Anthony F.; Howse, Frances A. (1995-01-01). "Primary productivity by symbiont-bearing planktonic sarcodines (Acantharia, Radiolaria, Foraminifera) in surface waters near Bermuda". Journal of Plankton Research. 17 (1): 103–129. doi:10.1093/plankt/17.1.103. ISSN 0142-7873.

phaeocystis, genus, algae, belonging, prymnesiophyte, class, larger, division, haptophyta, widespread, marine, phytoplankton, function, wide, range, temperatures, eurythermal, salinities, euryhaline, members, this, genus, live, open, ocean, well, polymorphic, . Phaeocystis is a genus of algae belonging to the Prymnesiophyte class and to the larger division of Haptophyta 1 It is a widespread marine phytoplankton and can function at a wide range of temperatures eurythermal and salinities euryhaline 2 Members of this genus live in the open ocean as well as in sea ice 3 It has a polymorphic life cycle ranging from free living cells to large colonies 2 Phaeocystis Phaeocystis globosa Scientific classification Domain Eukaryota unranked Haptophyta Class Prymnesiophyceae Order Phaeocystales Family Phaeocystaceae Genus PhaeocystisLagerheim 1893 The ability to form a floating colony is one of the unique attributes of Phaeocystis hundreds of cells are embedded in a polysaccharide gel matrix which can increase massively in size during blooms 3 The largest Phaeocystis blooms form in the polar seas P pouchetii in the north and P antarctica in the south 1 This intense Phaeocystis productivity generally persists for about a three month period spanning most of the summer in the Southern Hemisphere Phaeocystis abundant ecosystems are generally associated with commercially important stocks of crustaceans molluscs fish and mammals Phaeocystis may have negative effects on higher trophic levels in the marine ecosystem and consequent impacts on human activities such as fish farming and coastal tourism by forming odorous foams on beaches during the wane of a bloom 4 The ability to form large blooms and its ubiquity make Phaeocystis an important contributor to the ocean carbon cycle 5 6 In addition Phaeocystis produces dimethyl sulfide DMS a key player in the sulfur cycle 7 8 Contents 1 Distribution and life cycle 2 Impacts on global ocean 3 Symbiosis 4 ReferencesDistribution and life cycle edit nbsp Phaeocystis globosa colonies in culture Scale bar is 500 mm nbsp Phaeocystis antarctica colonies important phytoplankters of the Ross Sea that dominate early season blooms after the sea ice retreats and export significant carbon 9 nbsp Fluorescent microscopy of photosymbiotic acantharian hosting Phaeocystis symbionts Red fluorescence is chlorophyll autofluorescence and allows observation of the altered morphology of Phaeocystis chloroplasts Green fluorescence corresponds to LysoTracker dye which stains digestive compartments Symbionts are not being digested Free living forms of Phaeocystis are globally distributed and occur in a variety of marine habitats including coastal oceans open oceans polar seas and sea ice 10 Seven species are currently assigned to the genus P antarctica P jahnii P globosa P pouchetti P scrobiculata not in culture P cordata and P rex 11 Three species P globosa P pouchetii and P antarctica are associated with bloom formation in nutrient rich areas 12 which can occur either naturally e g in the Ross Sea Greenland Sea or the Barents Sea or due to anthropogenic inputs e g in the Southern Bight of the North Sea or the Persian Gulf Generally P globosa blooms in temperate and tropical waters whereas P pouchetii and P antarctica are better adjusted to the cold temperatures prevailing in Arctic and Antarctic waters respectively However P pouchetii also tolerates warmer temperatures 13 and has been seen in temperate waters 14 Genome comparison has shown that the RUBISCO spacer region located in the plastid DNA between two subunits of the enzyme 1 5 bisphosphate carboxylase is highly conserved among closely related colonial Phaeocystis species and identical in P antarctica P pouchetii and two warm temperate strains of P globosa with a single base substitution in two cold temperate strains of P globosa 15 Phaeocystis can exist as either free living cells or colonies Free living cells can show a variety of morphologies depending on the species All species can exist as scaled flagellates and this is the only form that has been observed for P scrobiculata and P cordata Three species have been observed as colonies P globosa P pouchetii and P antarctica and these can also exist as a flagellate devoid of scales and filaments 16 In colonies of Phaeocystis the colony skin may provide protection against smaller zooplankton grazers and viruses 17 While suspected in other species P pouchetii and P antarctica a haploid diploid life cycle has only been observed in P globosa In this cycle sexual reproduction is dominant in colony bloom formation termination and two types of vegetative reproduction exist 16 Impacts on global ocean editThe genus Phaeocystis is a major producer of 3 dimethylsulphoniopropionate DMSP the precursor of dimethyl sulfide DMS Biogenic DMS contributes approximately 1 5 1013 g sulfur to the atmosphere annually and plays a major part in the global sulfur cycle which can affect cloud formation and potentially climate regulation 1 Symbiosis editPhaeocystis species are endosymbionts to acantharian radiolarians 18 19 Acantharians collected in different ocean basins host different species of Phaeocystis as their dominant symbionts P antarctica is found as the primary symbiont to acantharians in the Southern Ocean and P cordata and P jahnii are among the dominant symbionts found in acantharians collected in warm oligotrophic regions of the Indian and Pacific oceans 18 In addition to the described Phaeocystis species sequences belonging to the molecular clade Phaeo02 often make up a majority of symbiotic sequences recovered from acantharians in warm water regions 18 19 Whether or not this symbiosis represents a true mutualism with both partners benefiting is debated 20 Extreme cellular remodeling is observed in symbiotic Phaeocystis including a drastic increase in chloroplast number and an enlarged central vacuole 18 19 This phenotypic change is probably induced by the host to increase photosynthetic output by symbionts but if it renders symbiotic cells incapable of future cell division the symbiosis is a dead end for Phaeocystis 20 The symbiosis is ecologically relevant because it creates primary production hot spots in low nutrient regions 21 but it remains to be determined how the symbiosis has affected Phaeocystis evolution References edit a b c phaeocystis research www phaeocystis org a b Schoemann Veronique Becquevort Sylvie Stefels Jacqueline Rousseau Veronique Lancelot Christiane 2005 01 01 Phaeocystis blooms in the global ocean and their controlling mechanisms a review Journal of Sea Research Iron Resources and Oceanic Nutrients Advancement of Global Environmental Simulations 53 1 2 43 66 Bibcode 2005JSR 53 43S CiteSeerX 10 1 1 319 9563 doi 10 1016 j seares 2004 01 008 a b Welcome to the Phaeocystis antarctica genome sequencing project homepage www phaeocystis org Lancelot C Mathot S 1987 Dynamics of a Phaeocystis dominated spring bloom in Belgian coastal waters I Phytoplanktonic activities and related parameters Marine Ecology Progress Series 37 239 248 Bibcode 1987MEPS 37 239L doi 10 3354 meps037239 Smith Walker O Codispoti Louis A Nelson David M Manley Thomas Buskey Edward J Niebauer H Joseph Cota Glenn F 1991 08 08 Importance of Phaeocystis blooms in the high latitude ocean carbon cycle Nature 352 6335 514 516 Bibcode 1991Natur 352 514S doi 10 1038 352514a0 S2CID 4369806 DiTullio G R Grebmeier J M Arrigo K R Lizotte M P Robinson D H Leventer A Barry J P VanWoert M L Dunbar R B 2000 Rapid and early export of Phaeocystis antarctica blooms in the Ross Sea Antarctica Nature 404 6778 595 598 Bibcode 2000Natur 404 595D doi 10 1038 35007061 PMID 10766240 S2CID 4409009 Stefels J Van Boekel W H M 1993 Production of DMS from dissolved DMSP in axenic cultures of the marine phytoplankton species Phaeocystis sp Mar Ecol Prog Ser 97 11 18 J Stefels L Dijkhuizen WWC Gieskes 1995 07 20 DMSP lyase activity in a spring phytoplankton bloom off the Dutch coast related to Phaeocystis sp abundance PDF Marine Ecology Progress Series 123 235 243 Bibcode 1995MEPS 123 235S doi 10 3354 meps123235 Bender S J Moran D M McIlvin M R Zheng H McCrow J P Badger J DiTullio G R Allen A E and Saito M A 2018 Colony formation in Phaeocystis antarctica connecting molecular mechanisms with iron biogeochemistry Biogeosciences 15 16 4923 4942 doi 10 5194 bg 15 4923 2018 Thomsen H A Buck K R Chavez F P 1994 Haptophytes as components of marine phytoplankton In Green J C Leadbeater B S C Eds The Haptophyte Algae Clarendon Press Oxford UK pp 187 208 Andersen Robert A Bailey J Craig Decelle Johan Probert Ian 2015 04 03 Phaeocystis rex sp nov Phaeocystales Prymnesiophyceae a new solitary species that produces a multilayered scale cell covering European Journal of Phycology 50 2 207 222 doi 10 1080 09670262 2015 1024287 ISSN 0967 0262 Lancelot C Keller M D Rousseau V Smith Jr W O Mathot S 1998 Autecology of the marine haptophyte Phaeocystis sp In Anderson D M Cembella A D Hallagraeff G M Eds Physiological Ecology of Harmful Algal blooms vol 41 Springer Verlag Berlin pp 209 224 Baumann M E M Lancelot C Brandini F P Sakshaug E John D M 1994 The taxonomic identity of the cosmopolitan prymnesiophyte Phaeocystis a morphological and ecophysiological approach Journal of Marine Systems 5 1 5 22 Bibcode 1994JMS 5 5B doi 10 1016 0924 7963 94 90013 2 Philippart Catharina J M Cadee Gerhard C van Raaphorst Wim Riegman Roel 2000 01 01 Long term phytoplankton nutrient interactions in a shallow coastal sea Algal community structure nutrient budgets and denitrification potential Limnology and Oceanography 45 1 131 144 Bibcode 2000LimOc 45 131P doi 10 4319 lo 2000 45 1 0131 ISSN 1939 5590 S2CID 86169774 Lange Martin Chen Yue Qin Medlin Linda K 2002 02 01 Molecular genetic delineation of Phaeocystis species Prymnesiophyceae using coding and non coding regions of nuclear and plastid genomes PDF European Journal of Phycology 37 1 77 92 doi 10 1017 S0967026201003481 ISSN 1469 4433 S2CID 55951287 a b Rousseau Veronique Chretiennot Dinet Marie Josephe Jacobsen Anita Verity Peter Whipple Stuart 2007 04 13 The life cycle of Phaeocystis state of knowledge and presumptive role in ecology Biogeochemistry 83 1 3 29 47 doi 10 1007 s10533 007 9085 3 ISSN 0168 2563 S2CID 54973619 Verity Peter G Brussaard Corina P Nejstgaard Jens C Leeuwe Maria A van Lancelot Christiane Medlin Linda K 2007 03 16 Current understanding of Phaeocystis ecology and biogeochemistry and perspectives for future research PDF Biogeochemistry 83 1 3 311 330 doi 10 1007 s10533 007 9090 6 ISSN 0168 2563 S2CID 55210194 a b c d Decelle Johan Simo Rafel Gali Marti Vargas Colomban de Colin Sebastien Desdevises Yves Bittner Lucie Probert Ian Not Fabrice 2012 10 30 An original mode of symbiosis in open ocean plankton Proceedings of the National Academy of Sciences 109 44 18000 18005 Bibcode 2012PNAS 10918000D doi 10 1073 pnas 1212303109 ISSN 0027 8424 PMC 3497740 PMID 23071304 a b c Mars Brisbin Margaret Grossmann Mary M Mesrop Lisa Y Mitarai Satoshi 2018 Intra host Symbiont Diversity and Extended Symbiont Maintenance in Photosymbiotic Acantharea Clade F Frontiers in Microbiology 9 1998 doi 10 3389 fmicb 2018 01998 ISSN 1664 302X PMC 6120437 PMID 30210473 a b Decelle Johan 2013 07 30 New perspectives on the functioning and evolution of photosymbiosis in plankton Communicative amp Integrative Biology 6 4 e24560 doi 10 4161 cib 24560 PMC 3742057 PMID 23986805 Caron David A Swanberg Neil R Michaels Anthony F Howse Frances A 1995 01 01 Primary productivity by symbiont bearing planktonic sarcodines Acantharia Radiolaria Foraminifera in surface waters near Bermuda Journal of Plankton Research 17 1 103 129 doi 10 1093 plankt 17 1 103 ISSN 0142 7873 Retrieved from https en wikipedia org w index php title Phaeocystis amp oldid 1217740754, wikipedia, wiki, book, books, library,

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