Proof of homothally of <italic style="font-style: italic">Pheopolykrikos hartmannii</italic> and details of cyst germination process

Zhaoyang CHAI; Zhangxi HU; Yuyang LIU; Yingzhong TANG

doi:10.1007/s00343-019-9077-x

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

Ecology | Updated：2023-04-27

- Proof of homothally of Pheopolykrikos hartmannii and details of cyst germination process
- Journal of Oceanology and Limnology Vol. 38, Issue 1, Pages: 114-123(2020)
- Affiliations：
  
  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
- Author bio：
  
  TANG Yingzhong, yingzhong.tang@qdio.ac.cn
- Funds：
- DOI：10.1007/s00343-019-9077-x
  CLC：
- Received：21 March 2019，
  
  Accepted：26 April 2019，
  
  Online First：15 May 2019，
  
  Published：2020-01
- Accepted：
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Zhaoyang CHAI, Zhangxi HU, Yuyang LIU, et al. Proof of homothally of Pheopolykrikos hartmannii and details of cyst germination process[J]. Journal of Oceanology and Limnology, 2020, 38(1): 114-123.
DOI：

Zhaoyang CHAI, Zhangxi HU, Yuyang LIU, et al. Proof of homothally of Pheopolykrikos hartmannii and details of cyst germination process[J]. Journal of Oceanology and Limnology, 2020, 38(1): 114-123. DOI： 10.1007/s00343-019-9077-x.

摘要

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.

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Keywords

references

D M Anderson , F M M Morel . The seeding of two red tide blooms by the germination of benthic Gonyaulax tamarensis hypnocysts . Estuarine and Coastal Marine Science , 1979 . 8 ( 3 ): 279 - 293 . DOI: 10.1016/0302-3524(79)90098-7 http://doi.org/10.1016/0302-3524(79)90098-7 .

D M Anderson , D Wall . Potential importance of benthic cysts of Gonyaulax tamarensis and G. excavata in initiating toxic dinoflagellate blooms . Journal of Phycology , 1978 . 14 ( 2 ): 224 - 234 . DOI: 10.1111/j.1529-8817.1978.tb02452.x http://doi.org/10.1111/j.1529-8817.1978.tb02452.x .

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.

S Badylak , E J Phlips . Spatial and temporal patterns of phytoplankton composition in subtropical coastal lagoon, the Indian River Lagoon, Florida, USA . Journal of Plankton Research , 2004 . 26 ( 10 ): 1 http://www.wanfangdata.com.cn/details/detail.do?_type=perio&id=HighWire000002128820 http://www.wanfangdata.com.cn/details/detail.do?_type=perio&id=HighWire000002128820 , .

H Bernstein , H C Byerly , F A Hopf , R E Michod . Genetic damage, mutation, and the evolution of sex . Science , 1985 . 229 ( 4719 ): 1 http://cn.bing.com/academic/profile?id=32be680098b926ce844634a36250116d&encoded=0&v=paper_preview&mkt=zh-cn http://cn.bing.com/academic/profile?id=32be680098b926ce844634a36250116d&encoded=0&v=paper_preview&mkt=zh-cn , .

S I Blackburn , C J S Bolch , K A Haskard , G M Hallegraeff . Reproductive compatibility among four global populations of the toxic dinoflagellate Gymnodinium catenatum (Dinophyceae) . Phycologia , 2001 . 40 ( 1 ): 78 - 87 . DOI: 10.2216/i0031-8884-40-1-78.1 http://doi.org/10.2216/i0031-8884-40-1-78.1 .

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.

A Boc , A B Diallo , V Makarenkov . T-REX:a web server for inferring, validating and visualizing phylogenetic trees and networks . Nucleic Acids Research , 2012 . 40 ( w1 ): w573 - w579 . DOI: 10.1093/nar/gks485 http://doi.org/10.1093/nar/gks485 .

I Bravo , R I Figueroa . Towards an ecological understanding of dinoflagellate cyst functions . Microorganisms , 2014 . 2 ( 1 ): 11 - 32 . DOI: 10.3390/microorganisms2010011 http://doi.org/10.3390/microorganisms2010011 .

M Bringué , V Pospelova , D B Field . High resolution sedimentary record of dinoflagellate cysts reflects decadal variability and 20th century warming in the Santa Barbara Basin . Quaternary Science Reviews , 2014 . 105 86 - 101 . DOI: 10.1016/j.quascirev.2014.09.022 http://doi.org/10.1016/j.quascirev.2014.09.022 .

M L Brosnahan , D K Ralston , A D Fischer , A R Solow , D M Anderson . Bloom termination of the toxic dinoflagellate Alexandrium catenella :vertical migration behavior, sediment infiltration, and benthic cyst yield . Limnology and Oceanography , 2017 . 62 ( 6 ): 2 829 - 2 849 . DOI: 10.1002/lno.10664 http://doi.org/10.1002/lno.10664 .

A Burt . Perspective:sex, recombination, and the efficacy of selection-was Weismann right? . Evolution , 2000 . 54 ( 2 ): 337 - 351 . http://d.old.wanfangdata.com.cn/Periodical/tpyxb201104001 http://d.old.wanfangdata.com.cn/Periodical/tpyxb201104001 , .

B Dale . Life cycle strategies of oceanic dinoflagellates . UNESCO Technical Papers in Marine Science , 1986 . 49 65 - 72 . http://d.old.wanfangdata.com.cn/NSTLQK/10.1080-09670260600937833/ http://d.old.wanfangdata.com.cn/NSTLQK/10.1080-09670260600937833/ , .

M Elbrächter . Dinophyte reproduction:progress and conflicts . Journal of Phycology , 2003 . 39 ( 4 ): 629 - 632 . DOI: 10.1046/j.1529-8817.2003.39041.x http://doi.org/10.1046/j.1529-8817.2003.39041.x .

R I Figueroa , I Bravo , E Garcés , I Ramilo . Nuclear features and effect of nutrients on Gymnodinium catenatum (Dinophyceae) sexual stages . Journal of Phycology , 2006 . 42 ( 1 ): 67 - 77 . DOI: 10.1111/j.1529-8817.2006.00181.x http://doi.org/10.1111/j.1529-8817.2006.00181.x .

R I Figueroa , I Bravo . A study of the sexual reproduction and determination of mating type of Gymnodinium nolleri (Dinophyceae) in culture . Journal of Phycology , 2005 . 41 ( 1 ): 74 - 83 . DOI: 10.1111/j.1529-8817.2005.04045.x http://doi.org/10.1111/j.1529-8817.2005.04045.x .

R I Figueroa , K Rengefors , I Bravo , S Bensch . 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 , 2010 . 57 ( 3-4 ): 190 - 198 . DOI: 10.1016/j.dsr2.2009.09.016 http://doi.org/10.1016/j.dsr2.2009.09.016 .

Fukuyo Y, Takano H, Chihara M, Matsuoka K. 1990. Red Tide Organisms in Japan-An Illustrated Taxonomic Guide.Uchida Rokakuho, Tokyo.

I Gárate-Lizárraga , C J Band-Schmidt , del Alamo T Grayeb . Myrionecta , Gyrodinium and Katodinium bloom in Gulf of California . Harmful Algae News , 2008 . 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.

A Godhe , I Karunasagar , I Karunasagar , B Karlson . Dinoflagellate cysts in recent marine sediments from SW India . Botanica Marina , 2000 . 43 ( 1 ): 39 - 48 . http://www.wanfangdata.com.cn/details/detail.do?_type=perio&id=03d544b56e6172b3c5c23a199dcfaff3 http://www.wanfangdata.com.cn/details/detail.do?_type=perio&id=03d544b56e6172b3c5c23a199dcfaff3 , .

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.

G M Hallegraeff , C J Bolch . Transport of toxic dinoflagellate cysts via ships' ballast water . Marine Pollution Bulletin , 1991 . 22 ( 1 ): 27 - 30 . DOI: 10.1016/0025-326X(91)90441-T http://doi.org/10.1016/0025-326X(91)90441-T .

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.

M Hoppenrath , T R Bachvaroff , S M Handy , C F Delwiche , B S Leander . Molecular phylogeny of ocelloidbearing dinoflagellates (Warnowiaceae) as inferred from SSU and LSU rDNA sequences . BMC Evolutionary Biology , 2009 . 9 116 DOI: 10.1186/1471-2148-9-116 http://doi.org/10.1186/1471-2148-9-116 .

M Hoppenrath , N Yubuki , T R Bachvaroff , B S Leander . Re-classification of Pheopolykrikos hartmannii as Polykrikos (Dinophyceae) based partly on the ultrastructure of complex extrusomes . European Journal of Protistology , 2010 . 46 ( 1 ): 29 - 37 . DOI: 10.1016/j.ejop.2009.08.003 http://doi.org/10.1016/j.ejop.2009.08.003 .

Z X Hu , Y Y Deng , Y H Li , Y Z Tang . The morphological and phylogenetic characterization for the dinoflagellate Margalefidinium fulvescens (= Cochlodinium fulvescens ) isolated from the Jiaozhou Bay, China . Acta Oceanologica Sinica , 2018 . 37 ( 10 ): 11 - 17 . DOI: 10.1007/s13131-018-1295-0 http://doi.org/10.1007/s13131-018-1295-0 .

C J Huang , Q X Dong . Taxonomic and biological studies on organisms causing a large scale red tide in Zhujiang River Estuary in spring, 1998 Ⅲ . Oceanologia et Limnologia Sinica , 2001 . 32 ( 1 ): 1 - 6 . http://www.wanfangdata.com.cn/details/detail.do?_type=perio&id=hyyhz200101001 http://www.wanfangdata.com.cn/details/detail.do?_type=perio&id=hyyhz200101001 , .

K Y Kim , M Iwataki , C H Kim . Research Note:molecular phylogenetic affiliations of Dissodinium pseudolunula , Pheopolykrikos hartmannii , Polykrikos cf. schwartzii and Polykrikos kofoidii to Gymnodinium sensu stricto species (Dinophyceae) . Phycological Research , 2008 . 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.

K Matsuoka , Y Fukuyo . Cyst and motile morphology of a colonial dinoflagellate Pheopolykrikos hartmannii (Zimmermann) comb . nov. Journal of Plankton Research , 1986 . 8 ( 4 ): 811 - 818 . DOI: 10.1093/plankt/8.4.811 http://doi.org/10.1093/plankt/8.4.811 .

K Matsuoka . Archeopyle structure in modern gymnodinialean dinoflagellate cysts . Review of Palaeobotany and Palynology , 1985 . 44 ( 3-4 ): 217 - 231 . DOI: 10.1016/0034-6667(85)90017-X http://doi.org/10.1016/0034-6667(85)90017-X .

M Montresor , S Sgrosso , G Procaccini , W H C F Kooistra . Intraspecific diversity in Scrippsiella trochoidea (Dinophyceae):evidence for cryptic species . Phycologia , 2003 . 42 ( 1 ): 56 - 70 . DOI: 10.2216/i0031-8884-42-1-56.1 http://doi.org/10.2216/i0031-8884-42-1-56.1 .

P J Mudie , F Marret , K N Mertens , L Shumilovskikh , S A G Leroy . 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 , 2017 . 134 1 - 152 . DOI: 10.1016/j.marmicro.2017.05.004 http://doi.org/10.1016/j.marmicro.2017.05.004 .

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.

V Pospelova , S Esenkulova , S C Johannessen , M C O'Brien , R W Macdonald . 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 , 2010 . 75 ( 1-4 ): 17 - 37 . DOI: 10.1016/j.marmicro.2010.02.003 http://doi.org/10.1016/j.marmicro.2010.02.003 .

V Pospelova , S J Kim . Dinoflagellate cysts in recent estuarine sediments from aquaculture sites of southern South Korea . Marine Micropaleontology , 2010 . 76 ( 1-2 ): 37 - 51 . DOI: 10.1016/j.marmicro.2010.04.003 http://doi.org/10.1016/j.marmicro.2010.04.003 .

A M Price , V Pospelova . High-resolution sediment trap study of organic-walled dinoflagellate cyst production and biogenic silica flux in Saanich Inlet (BC, Canada) . Marine Micropaleontology , 2011 . 80 ( 1-2 ): 18 - 43 . DOI: 10.1016/j.marmicro.2011.03.003 http://doi.org/10.1016/j.marmicro.2011.03.003 .

K Rengefors , I Karlsson , L A Hansson . Algal cyst dormancy:a temporal escape from herbivory . Proceedings of the Royal Society B Biological Sciences , 1998 . 265 ( 1403 ): 1 353 - 1 358 . DOI: 10.1098/rspb.1998.0441 http://doi.org/10.1098/rspb.1998.0441 .

T J Smayda . Reflections on the ballast water dispersal -harmful algal bloom paradigm . Harmful Algae , 2007 . 6 ( 4 ): 601 - 622 . DOI: 10.1016/j.hal.2007.02.003 http://doi.org/10.1016/j.hal.2007.02.003 .

A Stamatakis , P Hoover , J Rougemont . A rapid bootstrap algorithm for the RA×ML Web servers . Systematic Biology , 2008 . 57 ( 5 ): 758 - 771 . DOI: 10.1080/10635150802429642 http://doi.org/10.1080/10635150802429642 .

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.

Y Z Tang , T A Egerton , L S Kong , H G Marshall . Morphological variation and phylogenetic analysis of the dinoflagellate Gymnodinium aureolum from a tributary of Chesapeake Bay . Journal of Eukaryotic Microbiology , 2008 . 55 ( 2 ): 91 - 99 . DOI: 10.1111/j.1550-7408.2008.00305.x http://doi.org/10.1111/j.1550-7408.2008.00305.x .

Y Z Tang , C J Gobler . The toxic dinoflagellate Cochlodinium polykrikoides (Dinophyceae) produces resting cysts . Harmful Algae , 2012 . 20 71 - 80 . DOI: 10.1016/j.hal.2012.08.001 http://doi.org/10.1016/j.hal.2012.08.001 .

Y Z Tang , C J Gobler . Sexual resting cyst production by the dinoflagellate Akashiwo sanguinea :a potential mechanism contributing to the ubiquitous distribution of a harmful alga . Journal of Phycology , 2015 . 51 ( 2 ): 298 - 309 . DOI: 10.1111/jpy.12274 http://doi.org/10.1111/jpy.12274 .

Y Z Tang , M J Harke , C J Gobler . Morphology, phylogeny, dynamics, and ichthyotoxicity of Pheopolykrikos hartmanni i (Dinophyceae) isolates and blooms from New York, USA . Journal of Phycology , 2013 . 49 ( 6 ): 1 084 - 1 094 . DOI: 10.1111/jpy.12114 http://doi.org/10.1111/jpy.12114 .

F J R Taylor . On dinoflagellate evolution . Biosystems , 1980 . 13 ( 1-2 ): 65 - 108 . DOI: 10.1016/0303-2647(80)90006-4 http://doi.org/10.1016/0303-2647(80)90006-4 .

U Tillmann , M Hoppenrath . Life cycle of the pseudocolonial dinoflagellate Polykrikos kofoidii(Gymnodiniales, Dinoflagellata) . Journal of Phycology , 2013 . 49 ( 2 ): 298 - 317 . DOI: 10.1111/jpy.12037 http://doi.org/10.1111/jpy.12037 .

D Wall , B Dale . Modern dinoflagellate cysts and evolution of the Peridiniales . Micropaleontology , 1968 . 14 ( 3 ): 265 - 304 . DOI: 10.2307/1484690 http://doi.org/10.2307/1484690 .

W Zimmermann . Neue und wenig bekannte Kleinalgen von Neapel Ⅰ-Ⅴ . Zeitschrift für Botany , 1930 . 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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Related Institution

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

DOI：10.1007/s00343-019-9077-x

摘要

Abstract

关键词

Keywords

references