Korean Journal of Environmental Biology (환경생물)

Korean Society of Environmental Biology (한국환경생물학회)
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Infection of marine diatom Coscinodiscus wailesii(Bacillariophyceae) by the parasitic nanoflagellate Pirsonia diadema(Stramenopiles) from Yongho Bay in Korea

  • Yoo, Jiae (Division of Earth Environmental System Science, Pukyong National University) ;
  • Kim, Sunju (Division of Earth Environmental System Science, Pukyong National University)
  • Received : 2020.11.12
  • Accepted : 2020.11.17
  • Published : 2020.12.31
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Abstract

The infection of marine diatom Coscinodiscus wailesii by a parasitic protist from the Yongho Bay of Busan, Korea was observed during the diatom bloom events in 2017 through 2018. The morphological and molecular features suggested that the parasitic nanoflagellate Pirsonia diadema was responsible for the infection. During the study period, the parasite prevalence ranged from 0.3% to 3.3%, and infected C. wailesii cells were observed only at surface seawater temperatures ranging between 10.9 and 19.9℃, although the host population appeared at temperatures above 25℃. The parasite and host system was successfully established as cultures. Using the cultures, we determined the morphological features over the infection cycle, parasite generation time, parasite prevalence as a function of inoculum size, and zoospore infectivity and survival time. The diatom C. wailesii was readily infected by the parasite P. diadema, with a parasite prevalence reaching up to 100% and a zoospore to host inoculum ratio above 20:1. The survival and infectivity of the parasite zoospores decreased with age. While the zoospores could survive up to 88 hours, they quickly lost their ability to infect after 48 hours. These results could lead to a better understanding of the biology and ecology of the parasitoid infecting the giant-sized diatoms in coastal waters.

Keywords

Acknowledgement

This research was supported by a Research Grant of Pukyong National University 2019.

References

  1. Bulman SR, SF Kuhn, JW Marshall and E Schnepf. 2001. A phylogenetic analysis of the SSU rRNA from members of the Plasmodiophorida and Phagomyxida. Protist 152:43-51. https://doi.org/10.1078/1434-4610-00042
  2. Bruning K. 1991. Infection of the diatom Asterionella by a chytrid. 2. Effects of light on survival and epidemic development of the parasite. J. Plank. Res. 13: 119-129. https://doi.org/10.1093/plankt/13.1.119
  3. Chakravarty DK. 1974. On the ecology of the infection of the marine diatom Coscinodiscus granii by Lagenisma coscinodisci in the Weser Estuary. Ver6ff. Inst. Meeresforsch. Bremem., Suppl. 5:115-122.
  4. Coats DW and MG Park. 2002. Parasitism of photosynthetic dinoflagellates by three strains of Amoebophrya (Dinophyta): parasite survival, infectivity, generation time, and host specificity. J. Phycol. 38:520-528. https://doi.org/10.1046/j.1529-8817.2002.01200.x
  5. Drebes G. 1966. Ein parasitischer Phycomycet (Lagenidiales) in Coscinodiscus. Helgol. Meeresunters. 13:426-435. https://doi.org/10.1007/BF01611959
  6. Drebes G. 1968. Lagenisma coscinodisci gen. nov., spec. nov., ein Vertreter der Lagenidiales in der marinen Diatomee Coscinodiscus. Veroff. Inst. Meeresforsch. Bremerh. Sonderb. 3:67-70.
  7. Drebes G and E Schnepf. 1988. Paulsenella Chatton (Dinophyta), ectoparasites of marine diatoms: development and taxonomy. Helgol. Meeresunters. 42:563-581. https://doi.org/10.1007/BF02365627
  8. Drebes G and E Schnepf. 1998. Gyrodinium undulans Hulburt, a marine dinoflagellate feeding on the bloom forming diatom Odontella aurita, and on copepod and rotifer eggs. Helgol. Meeresunters. 52:1-14. https://doi.org/10.1007/BF02908731
  9. Frenken T, M Velthuis, LN de Senerpont Domis, S Stephan, R Aben, S Kosten, E van Donk and DB van de Waal. 2016. Warming accelerates termination of a phytoplankton spring bloom by fungal parasites. Glob. Change Biol. 22:299-309. https://doi.org/10.1111/gcb.13095
  10. Gotelli D. 1971. Lagenisma coscinodisci, a parasite of the marine diatom Coscinodiscus occurring in the Puget Sound, Washington. Mycologia 63:171-174. https://doi.org/10.1080/00275514.1971.12019095
  11. Grahame ES. 1976. The occurrence of Lagenisma coscinodisci in Palmeria hardmanianafrom Kingston harbour, Jamaica. Br. Phycol. J. 11:57-61. https://doi.org/10.1080/00071617600650091
  12. Johansson M and DW Coats. 2002. Ciliate grazing on the parasite Amoebophrya sp. decreases infection of the red-tide dinoflagellate Akashiwo sanguinea. Aquat. Microb. Ecol. 28:69-78. https://doi.org/10.3354/ame028069
  13. Kim S and MG Park. 2014. Amoebophrya spp. from the bloom-forming dinoflagellate Cochlodinium polykrikoides: parasites not nested in the "Amoebophrya ceratii complex". J. Eukryot. Microbiol. 61:173-181. https://doi.org/10.1111/jeu.12097
  14. Kim S, CB Jeon and MG Park. 2017. Morphological observations and phylogenetic position of the parasitoid nanoflagellate Pseudopirsonia sp. (Cercozoa) infecting the marine diatom Coscinodiscuswailesii(Bacillariophyta). Algae 32:181-187. https://doi.org/10.4490/algae.2017.32.7.28
  15. Kuhn SF. 1997. Victoriniella multiformis, gen. et spec. nov.(incerta sedis), a polymorphic parasitoid protist infecting the marine diatom Coscinodiscus wailesii Gran & Angst(North Sea, German Bight). Arch. Protistenkd. 148:115-123. https://doi.org/10.1016/S0003-9365(97)80039-5
  16. Kuhn SF. 1998. Infection of Coscinodiscus spp. by the parasitoid nanoflagellate Pirsonia diadema: II. Selective infection behaviour for host species and individual host cells. J. Plankton Res. 20:443-454. https://doi.org/10.1093/plankt/20.3.443
  17. Kuhn SF, G Drebes and E Schnepf. 1996. Five new species of the nanoflagellate Pirsonia in the German Bight, North Sea, feeding on planktic diatoms. Helgolander Meeresunters. 50:205-222. https://doi.org/10.1007/BF02367152
  18. Kuhn SF, L Medlin and G Eller. 2004. Phylogenetic position of the parasitoid nanoflagellate Pirsonia inferred from nuclear-encoded small subunit ribosomal DNA and a description of Pseudopirsonia n. gen. and Pseudopirsonia mucosa (Drebes) comb. nov. Proist 155:143-156.
  19. Larkin MA, G Blackshields, NP Brown, R Chenna, PA McGettigan, H McWilliam, F Valentin, I Wallace, A Wilm, R Lopez, JD Thompson, TJ Gibson and DG Higgins. 2007. Clustal W and Clustal X version 2.0. Bioinformatics 23:2947-2948. https://doi.org/10.1093/bioinformatics/btm404
  20. Maddison WP and DR Maddison. 2019. Mesquite: a modular system for evolutionary analysis. Version 3.61 http://www.mesquiteproject.org.
  21. Mague TH, E Friberg, DJ Hughes and I Morris. 1980. Extracellular release of carbon by marine phytoplankton; a physiological approach. Limnol. Oceanogr. 25:262-279. https://doi.org/10.4319/lo.1980.25.2.0262
  22. Moon-van der Staay SY, GWM van der Staay, L Guillou, D Vaulot, H Claustre, LK Medlin. 2000. Abundance and diversity of prymnesiophytes in the picoplankton community from the equatorial Pacific Ocean inferred from 18S rDNA sequences. Limnol. Oceanogr. 45:98-109. https://doi.org/10.4319/lo.2000.45.1.0098
  23. Ronquist F, M Teslenko, P van der Mark, DL Ayres, A Darling, S Hohna, B Larget, L Liu, MA Suchard and JP Huelsenbeck. 2012. MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst. Biol. 61:539-542. https://doi.org/10.1093/sysbio/sys029
  24. Roy S, RP Harris and SA Poulet. 1989. Inefficient feeding by Calanus helgolandicus and Temora longicornis on Coscinodiscus wailesii: quantitative estimation using chlorophyll-type pigments and effects on dissolved free amino acids. Mar. Ecol. Prog. Ser. 52:145-153. https://doi.org/10.3354/meps052145
  25. Schnepf E, G Drebes and M Elb acter. 1990. Pirsonia guinardiae, gen. et spec. nov.: a parasitic flagellate on the marine diatom Guinardia flaccida with an unusual mode of food uptake. Helgol. Meeresunters. 44:275-293. https://doi.org/10.1007/BF02365468
  26. Scholz B, L Guillou, AV Marano, S Neuhauser, BK Sullivan, U Karsten, FC Kupper and FH Gleason. 2016. Zoosporic parasites infecting marine diatoms-A black box that needs to be opened. Fungal Ecol. 19:59-76. https://doi.org/10.1016/j.funeco.2015.09.002
  27. Schweikert M and E Schnepf. 1997. Light and electron microspical observations on Pirsonia punctigerae spec. nov. a nanoflagellate feeding on the marine centric diatom Thalassiosira punctigera. Eur. J. Protistol. 33:168-177. https://doi.org/10.1016/S0932-4739(97)80033-8
  28. Sheldon RW, WH Sutcliffe and MA Paranjape. 1977. Structure of pelagic food-chain and relationship between plankton and fish production. J. Fish. Res. Board Can. 34:2344-2353. https://doi.org/10.1139/f77-314
  29. Sherr EB, BF Sherr and J McDaniel. 1991. Clearance rates of < 6 ㎛ fluorescently labeled algae (FLA) by estuarine protozoa: potential impact of flagellates and ciliates. Mar. Ecol. Prog. Ser. 59:81-92.
  30. Stamatakis A. 2014. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. BioInformatics 30:1312-1313. https://doi.org/10.1093/bioinformatics/btu033
  31. Steele JH. 1970. Marine Food Chains. University of California Press. Berkely, California.
  32. Tillmann U, KJ Hesse and A Tillmann. 1999. Large-scale parasitic infection of diatoms in the Northfrisian Wadden Sea. J. Sea Res. 42:255-261. https://doi.org/10.1016/S1385-1101(99)00029-5
  33. Wetsteyn LPMJ and L Peperzak. 1991. Field observations in the Oosterschelde (The Netherlands) on Coscinodiscus concinnus and Coscinodiscus granii (Bacillariophyceae) infected by the marine fungus Lagenisma coscinodisci (Oomycetes). Hydrobiol. Bull. 25:15-21. https://doi.org/10.1007/BF02259584
  34. Yamaguchi A and T Horiguchi. 2005. Molecular phylogenetic study of the heterotrophic dinoflagellate genus Protoperidinium (Dinophyceae) inferred from small subunit rRNA gene sequences. Phycol. Res. 53:30-42. https://doi.org/10.1111/j.1440-1835.2005.tb00355.x