ALGAE

  • 제39권3호
  • /
  • Pages.129-147
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  • 2024
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  • 1226-2617(pISSN)
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  • 2093-0860(eISSN)
한국조류학회(藻類) (The Korean Society of Phycology)
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Ultrastructure and molecular phylogeny of Mesodinium annulatum sp. nov. (Mesodiniidae, Cyclotrichiida), a new member of the Mesodinium rubrum / Mesodinium major complex

  • Seung Won Nam (Nakdonggang National Institute of Biological Resources) ;
  • Miran Kim (Honam National Institute of Biological Resources) ;
  • Seok Won Jang (Nakdonggang National Institute of Biological Resources) ;
  • Myung Gil Park (LOHABE, Department of Oceanography, Chonnam National University) ;
  • Wonho Yih (Marine Life Research and Education Center, Kunsan National University) ;
  • Hyung Seop Kim (Department of Oceanography, Kunsan National University) ;
  • Woongghi Shin (Department of Biology, Chungnam National University)
  • 투고 : 2024.07.26
  • 심사 : 2024.09.10
  • 발행 : 2024.09.23
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초록

The species complex Mesodinium rubrum / major, common red tide-forming ciliates, has been intensively studied with regards to its ecological roles in global marine ecosystems and the evolutionary aspects of its "stolen" organelles (kleptoplasty and karyoklepty). Nonetheless, the taxonomy of the species within the complex remains unclear. A new marine Mesodinium species isolated from Gomso Bay, Korea, was cultivated under mixotrophic conditions by providing Teleaulax amphioxeia, a red cryptomonad, as prey. Cells of the new isolate consisted of two portions separated by two types of polykinetids. The number of polykinetid associated with the equatorial ciliary belt was approximately 38, and each consisting of two rows of up to 18 alternating kinetosomes each. There was an equal number of cirral polykinetids, each consisting of 16 kinetosomes organized into four longitudinal rows having five, five, four, and two kinetosomes, respectively (in anti-clockwise direction). The two kinds of kinetids and their associated microtubules and fibers were structurally similar to those of M. rubrum from Denmark. However, the Korean Mesodinium species was characterized by its broad posterior portion, 20-22 tentacles, and a cytopharyngeal annulus. Molecular phylogeny based on internal transcribed spacer sequences placed the Korean isolate in clade B of the M. rubrum / major species complex, rather than in clade F representing the neotype of M. rubrum. Based on morphological, ultrastructural, and molecular data, we propose the Korean strain as a new marine Mesodinium species, M. annulatum.

키워드

과제정보

We appreciate Dr. Wayne Coats, an Emeritus scientist of Smithsonian Environmental Research Center, and two anonymous reviewers for their thoughtful advice and proofreading. This research was supported by a grant from the Nakdonggang National Institute of Biological Resources (NNIBR), funded by the Ministry of Environment (MOE) of the Republic of Korea (grant No. NNIBR20241108), the National Research Foundation (NRF) of Korea (grant No. NRF-2019R1I1A3A01058442), and the Korea Environment Industry & Technology Institute (KEITI), through the project to make multi-ministerial national biological research resources a more advanced program funded by the MOE (grant No. 2021003420004).

참고문헌

  1. Bary, B. M. & Stuckey, R. G. 1950. An occurrence in Wellington Harbour of Cyclotrichium meunieri Powers, a ciliate causing red water, with some additions to its morphology. Trans. R. Soc. N. Z. 78:86-92.
  2. Crawford, D. W. 1993. Some observations on morphological variation in the red-water ciliate Mesodinium rubrum. J. Mar. Biol. Assoc. U. K. 73:975-978. doi.org/10.1017/S002531540003486X
  3. De Puytorac, P. 1970. Definitions of ciliate descriptive terms. J. Protozool. 17:358.
  4. Fenchel, T. 1968. On "red water" in the Isefjord (inner Danish waters) caused by the ciliate Mesodinium rubrum. Ophelia 5:245-253. doi.org/10.1080/00785326.6812.10407613
  5. Foissner, W. 2014. An update of 'basic light and scanning electron microscopic methods for taxonomic studies of ciliated protozoa'. Int. J. Syst. Evol. Microbiol. 64:271-292. doi.org/10.1099/ijs.0.057893-0
  6. Garcia-Cuetos, L., Moestrup, O. & Hansen, P. J. 2012. Studies on the genus Mesodinium II. Ultrastructural and molecular investigations of five marine species help clarifying the taxonomy. J. Eukaryot. Microbiol. 59:374-400. doi.org/10.1111/j.1550-7408.2012.00630.x
  7. Grain, J. 1969. Le cinetosome et ses derives chez les cilies. Ann. Biol. 8:53-97.
  8. Grain, J., Puytorac, D. & Ca, G. 1982. Quelques precisions sur l'ultrastructure et la position systematique de Cilie Mesodinium rubrum, et sur la constitution de ses symbiontes chloroplastiques. Protistologica 18:7-21.
  9. Herfort, L., Maxey, K., Voorhees, I., et al. 2017. Use of highly specific molecular markers reveals positive correlation between abundances of Mesodinium cf. major and its preferred prey, Teleaulax amphioxeia, during red water blooms in the Columbia river Estuary. J. Eukaryotic Microbiol. 64:740-755. doi.org/10.1111/jeu.12407
  10. Herfort, L., Peterson, T. D., McCue, L. A., et al. 2011. Myrionecta rubra population genetic diversity and its cryptophyte chloroplast specificity in recurrent red tides in the Columbia River estuary. Aquat. Microb. Ecol. 62:85-97. doi.org/10.3354/ame01460
  11. Hibberd, D. J. 1977. Observations on the ultrastructure of the cryptomonad endosymbiont of the red-water ciliate Mesodinium rubrum. J. Mar. Biol. Assoc. U. K. 57:45-61. doi.org/10.1017/S0025315400021226
  12. Johnson, M. D., Beaudoin, D. J., Laza-Martinez, A., et al. 2016. The genetic diversity of Mesodinium and associated cryptophytes. Front. Microbiol. 7:2017. doi.org/10.3389/fmicb.2016.02017
  13. Johnson, M. D., Tengs, T., Oldach, D. W., Delwiche, C. F. & Stoecker, D. K. 2004. Highly divergent SSU rRNA genes found in the marine ciliates Myrionecta rubra and Mesodinium pulex. Protist 155:347-359. doi.org/10.1078/1434461041844222
  14. Kim, M., Kang, M. & Park, M. G. 2019. Growth and chloroplast replacement of the benthic mixotrophic ciliate Mesodinium coatsi. J. Eukaryot. Microbiol. 66:625-636. doi.org/10.1111/jeu.12709
  15. Kim, M. & Park, M. G. 2019. Unveiling the hidden genetic diversity and chloroplast type of marine benthic ciliate Mesodinium species. Sci. Rep. 9:14081. doi.org/10.1038/s41598-019-50659-2
  16. Lindholm, T. 1985. Mesodinium rubrum: a unique photosynthetic ciliate. In Jannasch, H. W. & Williams, P. J. (Eds.) Advances in Aquatic Microbiology. Academic Press, New York, pp. 1-48.
  17. Lindholm, T., Lindroos, P. & Mork, A.-C. 1988. Ultrastructure of the photosynthetic ciliate Mesodinium rubrum. Biosystems 21:141-149. doi.org/10.1016/0303-2647(88)90007-X
  18. Lynn, D. H. 2008. The ciliated protozoa: characterization, classification, and guide to the literature. Springer, New York, pp. 46, 58, 62, 82, 201-202.
  19. Mitra, A., Flynn, K. J., Tillmann, U., et al. 2016. Defining planktonic protist functional groups on mechanisms for energy and nutrient acquisition: incorporation of diverse mixotrophic strategies. Protist 167:106-120. doi.org/10.1016/j.protis.2016.01.003
  20. Moeller, H. V. & Johnson, M. D. 2018. Preferential plastid retention by the acquired phototroph Mesodinium chamaeleon. J. Eukaryot. Microbiol. 65:148-158. doi.org/10.1111/jeu.12446
  21. Moestrup, O., Garcia-Cuetos, L., Hansen, P. J. & Fenchel, T. 2012. Studies on the genus Mesodinium I: ultrastructure and description of Mesodinium chamaeleon n. sp., a benthic marine species with green or red chloroplasts. J. Eukaryot. Microbiol. 59:20-39. doi.org/10.1111/j.1550-7408.2011.00593.x
  22. Nam, S. W., Park, J. W., Yih, W., Park, M. G. & Shin, W. 2016. The fate of cryptophyte cell organelles in the ciliate Mesodinium cf. rubrum subjected to starvation. Harmful Algae 59:19-30. doi.org/10.1016/j.hal.2016.09.002
  23. Nam, S. W., Shin, W., Coats, D. W., Park, J. W. & Yih, W. 2012. Ultrastructure of the oral apparatus of Mesodinium rubrum from Korea. J. Eukaryot. Microbiol. 59:625-636. doi.org/10.1111/j.1550-7408.2012.00643.x
  24. Nam, S. W., Shin, W., Kang, M., Yih, W. & Park, M. G. 2015. Ultrastructure and molecular phylogeny of Mesodinium coatsi sp. nov., a benthic marine ciliate. J. Eukaryot. Microbiol. 62:102-120. doi.org/10.1111/jeu.12150
  25. 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. doi.org/10.1111/jeu.12041
  26. Reynolds, E. S. 1963. The use of lead citrate at high pH as an electron-opaque stain for electron microscopy. J. Cell Biol. 17:208-212. doi.org/10.1083/jcb.17.1.208
  27. Ronquist, F., Teslenko, M., van der Mark, P., et al. 2012. MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst. Biol. 61:539-542. doi.org/10.1093/sysbio/sys029
  28. Scholin, C. A., Herzog, M., Sogin, M. & Anderson, D. M. 1994. Identification of group- and strain-specific genetic markers for globally distributed Alexandrium (Dinophyceae). II. Sequence analysis of a fragment of the LSU rRNA gene. J. Phycol. 30:999-1011. doi.org/10.1111/j.0022-3646.1994.00999.x
  29. Spurr, A. R. 1969. A low-viscosity epoxy resin embedding medium for electron microscopy. J. Ultrastruct. Res. 26:31-43. doi.org/10.1016/S0022-5320(69)90033-1
  30. Stamatakis, A. 2014. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30:1312-1313. doi.org/10.1093/bioinformatics/btu033
  31. Stein, F. 1862. Neue und nicht genugend bekannte Infusorienformen. Amtl. Ber. Ver. dt. Naturf. Arzte. Karlsbad. 37:161-162.
  32. Tamar, H. 1986. Four marine species of Mesodinium (Ciliophora: Didiniidae). I. Mesodinium velox n. sp. Trans. Am. Microsc. Soc. 105:130-140. doi.org/10.2307/3226385
  33. Tamar, H. 1992. Four marine species of Mesodinium (Ciliophora: Mesodiniidae) II. Mesodinium pulex Clap. & Lachm., 1858. Arch. Protistenkd. 141:284-303. doi.org/10.1016/S0003-9365(11)80058-8
  34. Taylor, F. J. R., Blackbourn, D. J. & Blackbourn, J. 1971. The red-water ciliate Mesodinium rubrum and its "incomplete symbionts": a review including new ultrastructural observations. J. Fish. Res. Board Can. 28:391-407. doi.org/10.1139/f71-052
  35. Yih, W., Kim, H. S., Myung, G., Park, J. W., Yoo, Y. D. & Jeong, H. J. 2013. The red-tide ciliate Mesodinium rubrum in Korean coastal waters. Harmful Algae 30(Suppl 1):S53-S61. doi.org/10.1016/j.hal.2013.10.006