DOI QR코드

DOI QR Code

Characterizations of five heterotrophic nanoflagellates newly recorded in Korea

  • Jeong, Dong Hyuk (Department of Oceanography, Kyungpook National University) ;
  • Park, Jong Soo (Department of Oceanography, Kyungpook National University)
  • Received : 2021.06.09
  • Accepted : 2021.08.20
  • Published : 2021.11.30

Abstract

Heterotrophic nanoflagellates (HNFs, 2-20 ㎛ in size) are substantially capable of controlling bacterial abundance in aquatic environments, and microbial taxonomists have studied ecologically important and abundant HNFs for a long time. However, the classifications of HNFs have rarely been reported in Korea on the basis of morphology and 18S rDNA sequencing. Here, previously reported five HNFs from non-Korean habitats were isolated from Korean coastal seawater or intertidal sediments for the first time. Light microscopic observations and 18S rDNA phylogenetic trees revealed that the five isolated species were Cafeteria burkhardae strain PH003, Cafeteria graefeae strain UL001, Aplanochytrium minuta (formerly Labyrinthuloides minuta) strain PH004, Neobodo curvifilus strain KM017 (formerly Procryptobia sorokini), and Ancyromonas micra (formerly Planomonas micra) strain IG005. Being morphologically and phylogenetically indistinct from its closest species, all isolates from Korea were therefore regarded as identical species detected in other countries. Thus, this result indicates an expansion of known habitats that range from those of the five isolates in natural ecosystems on Earth.

Keywords

Acknowledgement

We thank to Sang Yoon Woo, Hyeon Been Lee, and Je Bak An for assistance with sampling. This work was supported by the National Institute of Biological Resources of Korea (NIBR202002207 and NIBR202130203) and the National Research Foundation of Korea (NRF) grant, funded by the Korean government to JSP (NRF-2019R1A2C2002379).

References

  1. Arndt, H., D. Dietrich, B. Auer, E.J. Cleven, T. Grafenhan, M. Weitere and A.P. Mylnikov. 2000. Functional diversity of heterotrophic flagellates in aquatic ecosystems. In: B.S. Leadbeater and J.C. Green (eds.), Flagellates: Unity, Diversity and Evolution, Taylor and Francis, London. pp. 240-268.
  2. Cavalier-Smith, T. 1998. Functional diversity of heterotrophic flagellates in aquatic ecosystems. Biological Reviews 73:203-266. https://doi.org/10.1111/j.1469-185X.1998.tb00030.x
  3. Cavalier-Smith, T., E.E. Chao, A. Stechmann, B. Oates and S. Nikolaev. 2008. Planomonadida ord. nov. (Apusozoa): Ultrastructural affinity with Micronuclearia podoventralis and deep divergences within Planomonas gen. nov. Protist 159:535-562. https://doi.org/10.1016/j.protis.2008.06.002
  4. Elwood, H.J., G.J. Olsen and M.L. Sogin. 1985. The smallsubunit ribosomal RNA gene sequences from the hypotrichous ciliates Oxytricha nova and Stylonychia pustulata. Molecular Biology and Evolution 2:399-410.
  5. Fischer, U.R., C. Wieltschnig, A.K.T. Kirschner and B. Velimirov. 2006. Contribution of virus-induced lysis and protozoan grazing to benthic bacterial mortality estimated simultaneously in microcosms. Environmental Microbiology 8:1394-1407. https://doi.org/10.1111/j.1462-2920.2006.01032.x
  6. Frolov, A.O., S.A. Karpov and A.P. Mylnikov. 2001. The ultrastructure of Procryptobia sorokini (Zhukov) comb. nov. and rootlet homology in kinetoplastids. Protistology 2:85-95.
  7. Giovannoni, S.J., E.F. DeLong, G.J. Olsen and N.R. Pace. 1988. Phylogenetic group-specific oligodeoxynucleotide probes for identification of single microbial cells. Journal of Bacteriology 170:720-726. https://doi.org/10.1128/jb.170.2.720-726.1988
  8. Glucksman, E., E.A. Snell and T. Cavalier-Smith. 2013. Phylogeny and evolution of Planomonadida (Sulcozoa): eight new species and new genera Fabomonas and Nutomonas. European Journal of Protistology 49:179-200. https://doi.org/10.1016/j.ejop.2012.08.007
  9. Guillard, R.R. and J.H. Ryther. 1962. Studies of marine planktonic diatoms: I. Cyclotella nana Hustedt, and Detonula confervacea (Cleve) Gran. Canadian Journal of Microbiology 8:229-239. https://doi.org/10.1139/m62-029
  10. Harel, M., E. Ben-Dov, D. Rasoulouniriana, N. Siboni, E. Kramarsky-Winter, Y. Loya, Z. Barak, Z. Wiesman and A. Kushmaro. 2008. A new Thraustochytrid, strain Fng1, isolated from the surface mucus of the hermatypic coral Fungia granulosa. FEMS Microbiology Ecology 64:378-387. https://doi.org/10.1111/j.1574-6941.2008.00464.x
  11. Heiss, A., W.J. Lee, K.-I. Ishida and A.G. Simpson. 2015. Cultivation and characterisation of new species of Apusomonads(the sister group to Opisthokonts), including close relatives of Thecamonas(Chelonemonas n. gen.). Journal of Eukaryotic Microbiology 62:637-649. https://doi.org/10.1111/jeu.12220
  12. Hirose, E., A. Nozawa, A. Kumagai and S.I. Kitamura. 2012. Azumiobodo hoyamushi gen. nov. et sp. nov.(Euglenozoa, Kinetoplastea, Neobodonida): a pathogenic kinetoplastid causing the soft tunic syndrome in ascidian aquaculture. Diseases of Aquatic Organisms 97:227-235. https://doi.org/10.3354/dao02422
  13. Jhin, S.H. and J.S. Park. 2019. A new halophilic heterolobosean flagellate, Aurem hypersalina gen. n. et sp. n., closely related to the Pleurostomum-Tulamoeba clade: implications for adaptive radiation of halophilic eukaryotes. Journal of Eukaryotic Microbiology 66:221-231. https://doi.org/10.1111/jeu.12664
  14. Kang, N.S. and S.Y. Kim. 2018. National list of marine species. National Marine Biodiversity Institute of Korea, Seocheon.
  15. Katoh, K. and D.M. Standley. 2013. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Molecular Biology and Evolution 30:772-780. https://doi.org/10.1093/molbev/mst010
  16. Kim, H.J., J.S. Park, K.H. Park, Y.K. Shin and K.I. Park. 2014. The kinetoplastid parasite Azumiobodo hoyamushi, the causative agent of soft tunic syndrome of the sea squirt Halocynthia roretzi, resides in the East Sea of Korea. Journal of Invertebrate Pathology 116:36-42. https://doi.org/10.1016/j.jip.2013.12.006
  17. Kim, S.Y., Y.O. Kim, K.C. Park, M.K. Shin, W.J. Lee and J.K. Choi. 2012. National list of species of Korea 'Protozoa'. National Institute of Biological Resource, Inchon.
  18. Larsen, J. and D.J. Patterson. 1990. Some flagellates(Protista) from tropical marine sediments. Journal of Natural History 24:801-937. https://doi.org/10.1080/00222939000770571
  19. Lax, G., W.J. Lee, Y. Eglit and A.G. Simpson. 2019. Ploeotids represent much of the phylogenetic diversity of euglenids. Protist 170:233-257. https://doi.org/10.1016/j.protis.2019.03.001
  20. Lee, W.J. 2002. Some free-living heterotrophic flagellates from marine sediments of Inchon, and Ganghwa Island, Korea. Korean Journal of Biological Sciences 6:125-143. https://doi.org/10.1080/12265071.2001.9647643
  21. Lee, W.J. 2006. Some free-living heterotrophic flagellates from marine sediments of tropical Australia. Ocean Science Journal 41:75-95. https://doi.org/10.1007/BF03022413
  22. Lee, W.J. 2015. Three newly recorded marine heterotrophic flagellates(Protist), Neometanema parovale, Stephanopogon pattersoni and Thaumatomastix sp. from South Korea. Korean Journal of Environmental Biology 33:148-152. https://doi.org/10.11626/KJEB.2015.33.2.148
  23. Lee, W.J. 2016. Heterotrophic flagellates. In: Choi et al. (ed.), Korean Society of Protistologists Protists of Korea (Vol. 2), Haksul Information Center, Seoul, Korea. pp. 182-216.
  24. Lee, W.J. 2020. First records of nine free-living heterotrophic flagellates from South Korea. Journal of Species Research 9:448-454. https://doi.org/10.12651/JSR.2020.9.4.448
  25. Lee, W.J. and J.S. Park. 2016. Placement of the unclassified Cyranomonas australis Lee 2002 within a novel clade of Cercozoa. European Journal of Protistology 56:60-66. https://doi.org/10.1016/j.ejop.2016.06.004
  26. Medlin, L., H.J. Elwood, S. Stickel and M.L. Sogin. 1988. The characterization of enzymatically amplified eukaryotic 16S-like rRNA-coding regions. Gene 71:491-499. https://doi.org/10.1016/0378-1119(88)90066-2
  27. Mora, C., D.P. Tittensor, S. Adl, A.G. Simpson and B. Worm. 2011. How many species are there on Earth and in the ocean? PLoS Biology 9:e1001127. https://doi.org/10.1371/journal.pbio.1001127
  28. Nguyen, L.T., H.A. Schmidt, A. Von Haeseler and B.Q. Minh. 2015. IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Molecular Biology and Evolution 32:268-274. https://doi.org/10.1093/molbev/msu300
  29. Park, J.S., B.C. Cho and A.G. Simpson. 2006. Halocafeteria seosinensis gen. et sp. nov. (Bicosoecida), a halophilic bacterivorous nanoflagellate isolated from a solar saltern. Extremophiles 10:493-504. https://doi.org/10.1007/s00792-006-0001-x
  30. Park, J.S., H. Kim, D.H. Choi and B.C. Cho. 2003. Active flagellates grazing on prokaryotes in high salinity waters of a solar saltern. Aquatic Microbial Ecology 33:173-179. https://doi.org/10.3354/ame033173
  31. Park, J.S. and A.G. Simpson. 2010. Characterization of halotolerant Bicosoecida and Placididea (Stramenopila) that are distinct from marine forms, and the phylogenetic pattern of salinity preference in heterotrophic stramenopiles. Environmental Microbiology 12:1173-1184. https://doi.org/10.1111/j.1462-2920.2010.02158.x
  32. Park, J.S., A.G. Simpson, W.J. Lee and B.C. Cho. 2007. Ultrastructure and phylogenetic placement within Heterolobosea of the previously unclassified, extremely halophilic heterotrophic flagellate Pleurostomum flabellatum (Ruinen 1938). Protist 158:397-413. https://doi.org/10.1016/j.protis.2007.03.004
  33. Patterson, D.J., K. Nygaard, G. Steinberg and C.M. Turley. 1993. Heterotrophic flagellates and other protists associated with oceanic detritus throughout the water column in the mid. North Atlantic. Journal of the Marine Biological Association of the United Kingdom 73:67-95. https://doi.org/10.1017/S0025315400032653
  34. Perkins, F.O. 1974. Reassignment of Labyrinthula minuta to the genus Labyrinthuloides. Mycologia 66:697-702. https://doi.org/10.2307/3758176
  35. Raghukumar, S. 2002. Ecology of the marine protists, the Labyrinthulomycetes (Thraustochytrids and Labyrinthulids). European Journal of Protistology 38:127-145. https://doi.org/10.1078/0932-4739-00832
  36. Ronquist, F., M. Teslenko, P. van der Mark, D.L. Ayres, A. Darling, S. Hohna, B. Larget, L. Liu, M.A. Suchard and J.P. Huelsenbeck. 2012. MrBAYES 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61:539-542. https://doi.org/10.1093/sysbio/sys029
  37. Schoenle, A., M. Hohlfeld, M. Rosse, P. Filz, C. Wylezich, F. Nitsche and H. Arndt. 2020. Global comparison of bicosoecid Cafeteria-like flagellates from the deep ocean and surface waters, with reorganization of the family Cafeteriaceae. European Journal of Protistology 73:125665. https://doi.org/10.1016/j.ejop.2019.125665
  38. Sherr, B.F., E.B. Sherr and C. Pedros-Alio. 1989. Simultaneous measurement of bacterioplankton production and protozoan bacterivory in estuarine water. Marine Ecology Progress Series 54:209-219. https://doi.org/10.3354/meps054209
  39. Tikhonenkov, D.V., S.H. Jhin, Y. Eglit, K. Miller, A. Plotnikov, A.G. Simpson and J.S. Park. 2019. Ecological and evolutionary patterns in the enigmatic protist genus Percolomonas (Heterolobosea; Discoba) from diverse habitats. PLoS One 14:e0216188. https://doi.org/10.1371/journal.pone.0216188
  40. Watson, S.W. and K.B. Raper. 1957. Labyrinthula minuta sp. nov. Microbiology 17:368-377.