The Acquisition of Plastids/Phototrophy in Heterotrophic Dinoflagellates
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RIS BIB ENDNOTEThe Acquisition of Plastids/Phototrophy in Heterotrophic Dinoflagellates
Publication date: 2014
Acta Protozoologica, 2014, Volume 53, Issue 1, pp. 39 - 50
https://doi.org/10.4467/16890027AP.14.005.1442Authors
The Acquisition of Plastids/Phototrophy in Heterotrophic Dinoflagellates
Several dinoflagellates are known to practice acquired phototrophy by either hosting intact algal endosymbionts or retaining plastids. The acquisition of phototrophy in dinoflagellates appears to occur independently over a variety of orders, rather than being restricted to any specific order(s). While dinoflagellates with intact algal cells host endosymbionts of cyanobacteria, pelagophyte, prasinophyte or dictyochophyte, most organelle-retaining dinoflagellates acquire plastids from cryptophytes. In dinoflagellates with acquired phototrophy, the mechanism by which symbionts or plastids are obtained has not been well studied at sub-cellular or ultrastructural level, and thus little is known regarding their mechanism to sequester and maintain photosynthetic structures, except for three cases, Amphidinium poecilochroum, Gymnodinium aeruginosum, and Dinophysis caudata with peduncle feeding. Dinoflagellates with acquired phototrophy display different degrees of reduction of the retained endosymbiont and organelles, ranging from those which contain intact whole algal cells (e.g. green Noctiluca scintillans), to those which have retained almost a full complement of organelles (e.g., Amphidinium poecilochroum and Podolampas bipes), to those in which only the plastids remain (e.g., Amphidinium wigrense and Dinophysis spp.). A series of events leading to acquisition and subsequent degeneration of a whole-cell endosymbiont have been widely recognized as evolutionary pathway of the acquisition of plastids. However, recent work on D. caudata suggests that acquisition of phototrophy by predation (i.e. kleptoplastidy) may be a mechanism and evolutionary pathway through which plastids originated in dinoflagellates with ‘foreign’ plastids other than the ‘typical’ peridinin-type plastids. Most organelle-retaining dinoflagellates are facultative mixotrophs, with Dinophysis species and an undescribed Antarctic dinoflagellate being the only obligate mixotrophs known so far. The establishment of dinoflagellates with acquired phototrophy in cultures and careful research using the cultures would help improve our knowledge of the evolution of the dinoflagellate plastids and their ecophysiology.
Buskey E. J., Coulter C. J., Brown S. L. (1994) Feeding, growth and bioluminescence of the heterotrophic dinoflagellate Protoperidinium huberi. Mar. Biol. 121: 373–380
Daugbjerg N., Jensen M. H., Hansen P. J. (2013) Using nuclearencoded LSU and SSU rDNA sequences to identify the eukaryotic endosymbiont in Amphisolenia bidentata (Dinophyceae). Protist 164: 411–422
Deane J. A., Strachan I. M., Saunders G. W., Hill D. R. A., McFadden G. I. (2002) Cryptomonad evolution: nuclear 18S rDNA phylogeny versus cell morphology and pigmentation. J. Phycol. 38: 1236–1244
Elbrächter M., Schnepf E. (1996) Gymnodinium chlorophorum, a new green, bloom-forming dinoflagellate (Gymnodiniales, Dinophyceae) with a vestigial prasinophyte endosymbiont. Phycologia 35: 381–393
Eriksen N. T., Hayes K. C., Lewitus A. J. (2002) Growth responses of the mixotrophic dinoflagellates, Cryptoperidiniopsis sp. And Pfiesteria piscicida, to light under prey-saturated conditions. Harmful Algae 1: 191–203
Escalera L., Reguera B., Takishita K., Yoshimatsu S., Koike K., Koike K. (2011) Cyanobacterial endosymbionts in the benthic dinoflagellate Sinophysis canaliculata (Dinophysiales, Dinophyceae). Protist 162: 304–314
Farmer M. A., Roberts K. R. (1990) Organelle loss in the endosymbiont of Gymnodinium acidotum (Dinophyceae). Protoplasma 153: 178–185
Feinstein T. N., Traslavina R., Sun M.-Y., Lin S. (2002) Effects of light on photosynthesis, grazing, and population dynamics of the heterotrophic dinoflagellate Pfiesteria piscicida (Dinophyceae). J. Phycol. 38: 659–669
Fields S. D., Rhodes R. G. (1991) Ingestion and retention of Chroomonas spp. (Cryptophyceae) by Gymnodinium acidotum (Dinophyceae). J. Phycol. 27: 525–529
Foster R. A., Collier J. L., Carpenter E. J. (2006) Reverse transcription PCR amplification of cyanobacterial symbiont 16S rRNA sequences from single non-photosynthetic eukaryotic marine planktonic host cells. J. Phycol. 42: 243–250
Furuya K., Saito H., Sriwoon R., Omura T., Furio E. E., Borja V. M, Lirdwitayaprasit T. (2006) Vegetative growth of Noctiluca scintillans containing the endosymbiont Pedinomonas noctilucae. Afr. J. Mar. Sci. 28: 305–308
Garcia-Cuetos L., Moestrup Ø., Hansen P. J., Daugbjerg N. (2010) The toxic dinoflagellate Dinophysis acuminata harbors permanent chloroplasts of cryptomonad origin, not kleptochloroplasts. Harmful Algae 9: 25–38
Gast R. J., Moran D. M., Dennett M. R., Caron D. A. (2007) Kleptoplasty in an Antarctic dinoflagellate: caught in evolutionary transition? Environ. Microbiol. 9: 39–45
Gómez F., Furuya K. (2007) Kofoidinium, Spatulodinium and other kofoidiniaceans (Noctilucales, Dinophyceae) in the Pacific Ocean. Eur. J. Protistol. 43: 115–124
Hallegraeff G. M., Jeffrey S. W. (1984) Tropical phytoplankton species and pigments of continental shelf waters of North and North-West Australia. Mar. Ecol. Prog. Ser. 20: 59–74
Hallegraeff G. M., Lucas I. A. N. (1988) The marine dinoflagellate genus Dinophysis (Dinophyceae): photosynthetic, neritic and non-photosynthetic, oceanic species. Phycologia 27: 25–42
Hansen P. J. (1992) Prey size selection, feeding rates and growth dynamics of heterotrophic dinoflagellates with special emphasis on Gyrodinium spirale. Mar. Biol. 114: 327–334
Hansen P. J., Miranda L., Azanza R. (2004) Green Noctiluca scintillans: a dinoflagellate with its own greenhouse. Mar. Ecol. Prog. Ser. 275: 79–87
Horiguchi T., Pienaar R. N. (1992) Amphidinium latum Lebour (Dinophyceae), a sand-dwelling dinoflagellate feeding on cryptomonads. Jpn. J. Phycol. 40: 353–363
Hu H., Yu M., Zhang, X. (1980) Discovery of phycobilin in Gymnodinium cyaneum Hu sp. nov. and its phylogenetic significance. Kexue Tongbao 25: 882–884
Jakobsen H. H., Hansen P. J., Larsen J. (2000) Growth and grazing responses of two chloroplast-retaining dinoflagellates: effect of irradiance and prey species. Mar. Ecol. Prog. Ser. 201: 121–128
Jeffrey S. W., Vesk M. (1976) Further evidence for a membranebound endosymbiont within the dinoflagellate Peridinium foliaceum. J. Phycol. 12: 450–455
Johnson M. D. (2011a) Acquired phototrophy in ciliates: a review of cellular interactions and structural adaptations. J. Eukaryot. Microbiol. 58: 185–195
Johnson M. D. (2011b) The acquisition of phototrophy: adaptive strategies of hosting endosymbionts and organelles. Photosynth. Res. 107: 117–132
Keeling P. J. (2010) The endosymbiotic origin, diversification and fate of plastids. Phil. Trans. R. Soc. B 365: 729–748
Kim S., Kang Y. G., Kim H. S., Yih W., Coats D. W., Park M. G. (2008) Growth and grazing responses of the mixotrophic dinoflagellate Dinophysis acuminata as functions of light intensity and prey concentration. Aquat. Microb. Ecol. 51: 301–310
Kim M., Kim S., Yih W., Park M. G. (2012a) The marine dinoflagellate genus Dinophysis can retain plastids of multiple algal origins at the same time. Harmful Algae 13: 105–111
Kim M., Nam S. W., Shin W., Coats D. W., Park M. G. (2012b) Dinophysis caudata (Dinophyceae) sequesters and retains plastids from the mixotrophic ciliate prey Mesodinium rubrum. J. Phycol. 48: 569–579
Koike K., Takishita K. (2008) Anucleated cryptophytes vestiges in the gonyaulacalean dinoflagellates Amylax buxus and Amylax triacantha (Dinophyceae). Phycol. Res. 56: 301–311
Koike K., Sekiguchi H., Kobiyama A., Takishita K., Kawachi M., Koike K., Ogata T. (2005) A novel type of kleptoplastidy in Dinophysis (Dinophyceae): presence of a haptophyte-type plastid in Dinophysis mitra. Protist 156: 225–237
Larsen J. (1988) An ultrastructural study of Amphidinium poecilochroum (Dinophyceae), a phagotrophic dinoflagellate feeding on small species of cryptophytes. Phycologia 27: 366–377
Lessard E. J., Swift E. (1986) Dinoflagellate from the north Atlantic classified as phototrophic or heterotrophic by epifluorescence microscopy. J. Plankton Res. 6: 1209–1215
Lewitus A. J., Glasgow Jr. H. B., Burkholder J. M. (1999) Kleptoplastidy in the toxic dinoflagellates Pfiesteria piscicida (Dinophyceae). J. Phycol. 35: 303–312
Lucas I. A. N. (1991) Symbionts of the tropical Dinophysiales (Dinophyceae). Ophelia 33: 213–224
Lucas I. A. N., Vesk M. (1990) The fine structure of two photosynthetic species of Dinophysis (Dinophysiales, Dinophyceae). J. Phycol. 26: 345–357
Nishitani G., Nagai S., Hayakawa S., Kosaka Y., Sakurada K., Kamiyama T., Gojobori T. (2012) Multiple plastids collected by the dinoflagellate Dinophysis mitra through kleptoplastidy. Appl. Environ. Microbiol. 78: 813–821
Nowack E. C. M., Melkonian M. (2010) Endosymbiotic associations within protists. Phil. Trans. R. Soc. B 365: 699–712
Onuma R., Horiguchi T. (2013) Morphological transition in kleptochloroplasts after ingestion in the dinoflagellates Amphidinium poecilochroum and Gymnodinium aeruginosum (Dinophyceae). Protist 164: 622–642
Park M. G., Kim S., Kim H. S., Myung G., Kang Y. G., Yih W. (2006) First successful culture of the marine dinoflagellate Dinophysis acuminata. Aquat. Microb. Ecol. 45: 101–106
Park M. G., Park J. S., Kim M., Yih W. (2008) Plastid dynamics during survival of Dinophysis caudata without its ciliate prey. J. Phycol. 44: 1154–1163
Park M. G., Kim M., Kang M. (2013) A dinoflagellate Amylax triacantha with plastids of the cryptophyte origin: phylogeny, feeding mechanism, and growth and grazing responses. J. Eukaryot. Microbiol. 60: 363–376
Qiu D., Huang L., Liu S., Lin S. (2011) Nuclear, mitochondrial and plastid gene phylogenies of Dinophysis miles (Dinophyceae): Evidence of variable types of chloroplasts. PLoS ONE 6: e29398. doi:10.1371/journal.pone.0029398
Riisgaard K., Hansen P. J. (2009) Role of food uptake for photosynthesis
growth and survival of the mixotrophic dinoflagellate Dinophysis acuminata. Mar. Ecol. Prog. Ser. 381: 51–62
Saito H., Furuya K., Lirdwitayaprasit T. (2006) Photoautotrophic growth of Noctiluca scintillans with the endosymbiont Pedinomonas noctilucae. Plankton Benthos Res. 1: 97–101
Schnepf E., Elbrächter M. (1988) Cryptophycean-like double membrane-bound chloroplast in the dinoflagellate, Dinophysis Ehrenb.: evolutionary, phylogenetic and toxicological implications. Bot. Acta 101: 196–203
Schnepf E., Elbrächter M. (1999) Dinophyte chloroplasts and phylogeny – A review. Grana 38: 81–97
Schnepf E., Winter S., Mollenhauer D. (1989) Gymnodinium aeruginosum (Dinophyta): A blue-green dinoflagellate with a vestigial, anucleate, cryptophyte endosymbiont. Pl. Syst. Evol. 164: 75–91
Schweiker M., Elbrächter M. (2004) First ultrastructural investigations of the consortium between a phototrophic eukaryotic endocytobiont and Podolampas bipes (Dinophyceae). Phycologia 43: 614–623
Skovgaard A. (1998) Role of chloroplast retention in marine dinoflagellates. Aquat. Microb. Ecol. 15: 293–301
Stoecker D. K., Johnson M. D., de Vargas C., Not F. (2009) Acquired phototrophy in aquatic protists. Aquat. Microb. Ecol. 57: 279–310
Strom S. L. (2001) Light-aided digestion, grazing and growth in herbivorous protists. Aquat. Microb. Ecol. 23: 253–261
Sweeney B. M. (1971) Laboratory studies of a green Noctiluca from New Guinea. J. Phycol. 7: 53–58
Sweeney B. M. (1976) Pedinomonas noctilucae (Prasinophyceae), the flagellate symbiotic in Noctiluca (Dinophyceae) in Southeast Asia. J. Phycol. 12: 460–464
Tarangkoon W., Hansen G., Hansen P. J. (2010) Spatial distribution of symbiont-bearing dinoflagellates in the Indian Ocean in relation to oceanographic regimes. Aquat. Microb. Ecol. 58: 197–213
Wilcox L. W., Wedemayer G. J. (1984) Gymnodinium acidotum Nygaard (Pyrrophyta), a dinoflagellate with an endosymbiotic cryptomonad. J. Phycol. 20: 236–242
Wilcox L. W., Wedemayer G. J. (1985) Dinoflagellate with bluegreen chloroplasts derived from an endosymbiotic eukaryote. Science 227: 192–194
Xia S., Zhang Q., Zhu H., Cheng Y., Liu G., Hu Z. (2013) Systematics of a kleptoplastidal dinoflagellate, Gymnodinium eucyaneum Hu (Dinophyceae), and its cryptomonad endosymbiont. PLoS ONE 8: e53820. doi:10.1371/journal.pone.0053820
Yamaguchi H., Nakayama T., Kai A., Inouye I. (2011) Taxonomy and phylogeny of a new kleptoplastidal dinoflagellate, Gymnodinium myriopyrenoides sp. nov. (Gymnodiniales, Dinophyceae), and its cryptophyte symbiont. Protist 162: 650–667
Information: Acta Protozoologica, 2014, Volume 53, Issue 1, pp. 39 - 50
Article type: Original article
LOHABE, Department of Oceanography lack of country
LOHABE, Department of Oceanography lack of country
Research Institute for Basic Sciences, Chonnam National University, Gwangju, Republic of Korea
Published at: 2014
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