Cite this paper:
CHAI Zhaoyang, HU Zhangxi, LIU Yuyang, TANG Yingzhong. Proof of homothally of Pheopolykrikos hartmannii and details of cyst germination process[J]. Journal of Oceanology and Limnology, 2020, 38(1): 114-123

Proof of homothally of Pheopolykrikos hartmannii and details of cyst germination process

CHAI Zhaoyang1, HU Zhangxi1,2,3, LIU Yuyang1,4, TANG Yingzhong1,2,3
1 Key Laboratory of Marine Ecology and Environmental Sciences, Institute of Oceanology, Chinese Academy of Sciences, Qingdao 266071, China;
2 Laboratory of Marine Ecology and Environmental Science, Qingdao National Laboratory of Marine Science and Technology, Qingdao 266237, China;
3 Center for Ocean Mega-Science, Chinese Academy of Sciences, Qingdao 266071, China;
4 University of Chinese Academy of Sciences, Beijing 100049, China
Abstract:
Resting cysts play crucial roles in the ecology of dinoflagellates, especially in wintering or surviving unfavorable conditions, seeding harmful algal blooms (HABs), and facilitating the geographic expansion. Encystment of dinoflagellates is tightly coupled with sexual reproduction in most cases, which can occur either through homothallism (self-fertilization) or heterothallism (intercrossing of +/-strains). The types of sexual reproduction have important ecological implications. The toxic and HAB-forming dinoflagellate, Pheopolykrikoides hartmannii has been previously reported to be heterothallic. Here, we provide visual confirmation of homothally of P. hartmannii and the first detailed visual recording of cyst germination based on the observations of a clonal isolate from Jiaozhou Bay, China. To document the homothallism, we first observed cell pairs in sexual mating, planozygotes with two longitudinal flagella, and cysts with typical morphology as described previously from the clonal culture. We then germinated a single cyst, established a new clonal culture from one of the two daughter cells after the first cell division of the germling (i.e. from the diploid germling to two haploid cells), and produced cysts again from the newly established clonal culture. For the observation of the germination time-series, we took micrographs and videos to show all germination processes, particularly with an interesting observation of the short amoeboid stage of the germling releasing from the archeopyle (~15 s), which was a landmark of the germination process and has not been reported elsewhere. This definitive evidence of homothallic sexuality and cyst production in P. hartmannii provides a new insight into the biology and ecology of the species, particularly a mechanism that may partly account for the population dynamics and ubiquitous distribution of the species.
Key words:    germination|harmful algal blooms (HABs)|heterothallism|homothallism|resting cyst|Pheopolykrikos hartmannii   
Received: 2019-03-21   Revised:
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Articles by HU Zhangxi
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References:
Anderson D M, Morel F M M. 1979. The seeding of two red tide blooms by the germination of benthic Gonyaulax tamarensis hypnocysts. Estuarine and Coastal Marine Science, 8(3):279-293.
Anderson D M, Wall D. 1978. Potential importance of benthic cysts of Gonyaulax tamarensis and G. excavata in initiating toxic dinoflagellate blooms. Journal of Phycology, 14(2):224-234.
Anderson D M. 1989. Cysts as factors in Pyrodinium bahamense ecology. In:Hallegraeff G M, Maclean J L eds. Biology, Epidemiology and Management of Pyrodinium Red Tides. The Fisheries Department, Ministry of Development, Brunei Darussalem, and International center for Living Aquatic Resources Management, Metro Manila. p.81-88.
Badylak S, Phlips E J. 2004. Spatial and temporal patterns of phytoplankton composition in subtropical coastal lagoon, the Indian River Lagoon, Florida, USA. Journal of Plankton Research, 26(10):1 229-1 247.
Bernstein H, Byerly H C, Hopf F A, Michod R E. 1985.Genetic damage, mutation, and the evolution of sex.Science, 229(4719):1 277-1 281.
Blackburn S I, Bolch C J S, Haskard K A, Hallegraeff G M. 2001. Reproductive compatibility among four global populations of the toxic dinoflagellate Gymnodinium catenatum (Dinophyceae). Phycologia, 40(1):78-87.
Blackburn S I, Parker N. 2005. Microalgal life cycles:encystment and excystment. In:Anderson R A ed. Algal Culturing Techniques. Elsevier Academic Press, Burlington. p.399-417.
Boc A, Diallo A B, Makarenkov V. 2012. T-REX:a web server for inferring, validating and visualizing phylogenetic trees and networks. Nucleic Acids Research, 40(w1):w573-w579.
Bravo I, Figueroa R I. 2014. Towards an ecological understanding of dinoflagellate cyst functions.Microorganisms, 2(1):11-32.
Bringué M, Pospelova V, Field D B. 2014. High resolution sedimentary record of dinoflagellate cysts reflects decadal variability and 20th century warming in the Santa Barbara Basin. Quaternary Science Reviews, 105:86-101.
Brosnahan M L, Ralston D K, Fischer A D, Solow A R, Anderson D M. 2017. Bloom termination of the toxic dinoflagellate Alexandrium catenella:vertical migration behavior, sediment infiltration, and benthic cyst yield.Limnology and Oceanography, 62(6):2 829-2 849.
Burt A. 2000. Perspective:sex, recombination, and the efficacy of selection-was Weismann right? Evolution, 54(2):337-351.
Dale B. 1986. Life cycle strategies of oceanic dinoflagellates.UNESCO Technical Papers in Marine Science, 49:65-72.
Elbrächter M. 2003. Dinophyte reproduction:progress and conflicts. Journal of Phycology, 39(4):629-632.
Figueroa R I, Bravo I, Garcés E, Ramilo I. 2006. Nuclear features and effect of nutrients on Gymnodinium catenatum (Dinophyceae) sexual stages. Journal of Phycology, 42(1):67-77.
Figueroa R I, Bravo I. 2005. A study of the sexual reproduction and determination of mating type of Gymnodinium nolleri(Dinophyceae) in culture. Journal of Phycology, 41(1):74-83.
Figueroa R I, Rengefors K, Bravo I, Bensch S. 2010. From homothally to heterothally:Mating preferences and genetic variation within clones of the dinoflagellate Gymnodinium catenatum. Deep Sea Research Part II:Topical Studies in Oceanography, 57(3-4):190-198.
Fukuyo Y, Takano H, Chihara M, Matsuoka K. 1990. Red Tide Organisms in Japan-An Illustrated Taxonomic Guide.Uchida Rokakuho, Tokyo.
Gárate-Lizárraga I, Band-Schmidt C J, Grayeb del Alamo T. 2008. Myrionecta, Gyrodinium and Katodinium bloom in Gulf of California. Harmful Algae News, 37:6-7.
Garcés E, Zingone A, Montresor M, Reguera B, Dale B. 2002.LIFEHAB:life histories of microalgal species causing harmful blooms. Office for the Official Publications of the European Communities, Luxembourg.
Godhe A, Karunasagar I, Karunasagar I, Karlson B. 2000.Dinoflagellate cysts in recent marine sediments from SW India. Botanica Marina, 43(1):39-48.
Goodenough U. 1985. An essay on the origins and evolution of eukaryotic sex. In:Halvorns H, Monroy O A eds. The Origin and Evolution of Sex, Marine Biological Laboratory Lectures in Biology. Alan R. Liss, Inc., New York. p.123-140. Guillard R R L. 1975. Culture of phytoplankton for feeding marine invertebrates. In:Smith W L, Chanley M H eds. Culture of Marine Invertebrate Animals. Springer, Boston. p.26-60.
Hallegraeff G M, Bolch C J. 1991. Transport of toxic dinoflagellate cysts via ships' ballast water. Marine Pollution Bulletin, 22(1):27-30.
Head M J. 1996. Modern dinoflagellate cysts and their biological affinities. In:Jansonius J, McGregor D C eds.Palynology:Principles and Applications. American Association of Stratigraphic Palynologists Foundation, Dallas. p.1 197-1 248.
Hoppenrath M, Bachvaroff T R, Handy S M, Delwiche C F, Leander B S. 2009. Molecular phylogeny of ocelloidbearing dinoflagellates (Warnowiaceae) as inferred from SSU and LSU rDNA sequences. BMC Evolutionary Biology, 9:116.
Hoppenrath M, Yubuki N, Bachvaroff T R, Leander B S. 2010.Re-classification of Pheopolykrikos hartmannii as Polykrikos (Dinophyceae) based partly on the ultrastructure of complex extrusomes. European Journal of Protistology, 46(1):29-37.
Hu Z X, Deng Y Y, Li Y H, Tang Y Z. 2018. The morphological and phylogenetic characterization for the dinoflagellate Margalefidinium fulvescens (=Cochlodinium fulvescens) isolated from the Jiaozhou Bay, China. Acta Oceanologica Sinica, 37(10):11-17.
Huang C J, Dong Q X. 2001. Taxonomic and biological studies on organisms causing a large scale red tide in Zhujiang River Estuary in spring, 1998 III. Oceanologia et Limnologia Sinica, 32(1):1-6.
Kim K Y, Iwataki M, Kim C H. 2008. Research Note:molecular phylogenetic affiliations of Dissodinium pseudolunula, Pheopolykrikos hartmannii, Polykrikos cf. schwartzii and Polykrikos kofoidii to Gymnodinium sensu stricto species (Dinophyceae). Phycological Research, 56(2):89-92.
Matsuoka K, Fukuyo Y, Hallegraeff G M, Anderson D M, Cembella A D. 2003. Taxonomy of cysts. In:Hallegraeff G M, Anderson D M, Cembella A D eds. Manual on Harmful Marine Microalgae. UNESCO, Paris. p.563-592.
Matsuoka K, Fukuyo Y. 1986. Cyst and motile morphology of a colonial dinoflagellate Pheopolykrikos hartmannii(Zimmermann) comb. nov. Journal of Plankton Research, 8(4):811-818.
Matsuoka K. 1985. Archeopyle structure in modern gymnodinialean dinoflagellate cysts. Review of Palaeobotany and Palynology, 44(3-4):217-231.
Montresor M, Sgrosso S, Procaccini G, Kooistra W H C F. 2003. Intraspecific diversity in Scrippsiella trochoidea(Dinophyceae):evidence for cryptic species. Phycologia, 42(1):56-70.
Mudie P J, Marret F, Mertens K N, Shumilovskikh L, Leroy S A G. 2017. Atlas of modern dinoflagellate cyst distributions in the Black Sea Corridor:from Aegean to Aral Seas, including Marmara, Black, Azov and Caspian Seas. Marine Micropaleontology, 134:1-152.
Nehring S. 1993. Mechanisms for recurrent nuisance algal blooms in coastal zones:resting cyst formation as lifestrategy of dinoflagellates. In:Sterr H, Hofstade J, Plag H P eds. Interdisciplinary Discussion of Coastal Research and Coastal Management Issues and Problems. Lang, Frankfurt/M. p.454-467.
Pfiester L A, Anderson D M. 1987. Dinoflagellate reproduction.In:Taylor F J R ed. The Biology of Dinoflagellates.Blackwell Scientific Publications, Oxford. p.621-629.
Pfiester L A. 1984. Sexual reproduction. In:Spector D L ed.Dinoflagellates. Academic Press, Massachusetts. p.181-200.
Pospelova V, Esenkulova S, Johannessen S C, O'Brien M C, Macdonald R W. 2010. Organic-walled dinoflagellate cyst production, composition and flux from 1996 to 1998 in the central Strait of Georgia (BC, Canada):a sediment trap study. Marine Micropaleontology, 75(1-4):17-37.
Pospelova V, Kim S J. 2010. Dinoflagellate cysts in recent estuarine sediments from aquaculture sites of southern South Korea. Marine Micropaleontology, 76(1-2):37-51.
Price A M, Pospelova V. 2011. High-resolution sediment trap study of organic-walled dinoflagellate cyst production and biogenic silica flux in Saanich Inlet (BC, Canada).Marine Micropaleontology, 80(1-2):18-43.
Rengefors K, Karlsson I, Hansson L A. 1998. Algal cyst dormancy:a temporal escape from herbivory. Proceedings of the Royal Society B Biological Sciences, 265(1403):1 353-1 358.
Smayda T J. 2007. Reflections on the ballast water dispersal -harmful algal bloom paradigm. Harmful Algae, 6(4):601-622.
Stamatakis A, Hoover P, Rougemont J. 2008. A rapid bootstrap algorithm for the RA×ML Web servers. Systematic Biology, 57(5):758-771.
Steidinger K A, Garccés E. 2006. Importance of life cycles in the ecology of harmful microalgae. In:Granéli E, Turner J T eds. Ecology of Harmful Algae. Springer, Netherlands.p.37-49.
Tang Y Z, Egerton T A, Kong L S, Marshall H G. 2008.Morphological variation and phylogenetic analysis of the dinoflagellate Gymnodinium aureolum from a tributary of Chesapeake Bay. Journal of Eukaryotic Microbiology, 55(2):91-99.
Tang Y Z, Gobler C J. 2012. The toxic dinoflagellate Cochlodinium polykrikoides (Dinophyceae) produces resting cysts. Harmful Algae, 20:71-80.
Tang Y Z, Gobler C J. 2015. Sexual resting cyst production by the dinoflagellate Akashiwo sanguinea:a potential mechanism contributing to the ubiquitous distribution of a harmful alga. Journal of Phycology, 51(2):298-309.
Tang Y Z, Harke M J, Gobler C J. 2013. Morphology, phylogeny, dynamics, and ichthyotoxicity of Pheopolykrikos hartmannii (Dinophyceae) isolates and blooms from New York, USA. Journal of Phycology, 49(6):1 084-1 094.
Taylor F J R. 1980. On dinoflagellate evolution. Biosystems, 13(1-2):65-108.
Tillmann U, Hoppenrath M. 2013. Life cycle of the pseudocolonial dinoflagellate Polykrikos kofoidii(Gymnodiniales, Dinoflagellata). Journal of Phycology, 49(2):298-317.
Wall D, Dale B. 1968. Modern dinoflagellate cysts and evolution of the Peridiniales. Micropaleontology, 14(3):265-304.
Zimmermann W. 1930. Neue und wenig bekannte Kleinalgen von Neapel I-V. Zeitschrift für Botany, 23:419-442.
Zingone A, Garcés E, Wyatt T, Silvert B, Bolch C. 2002. The importance of life cycles in the ecology of harmful algal blooms. In:Garcés E, Zingone A, Montresor M, Reguera B, Dale B eds. LIFEHAB:Life Histories of Microalgal Species Causing Harmful Blooms. Office for the Official Publications of the European Community, Luxembourg, Office for the Official Publications of the European Community, p.134-137.
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