Advanced SearchSearch Tips
Ingestion of the unicellular cyanobacterium Synechococcus by the mixotrophic red tide ciliate Mesodinium rubrum
facebook(new window)  Pirnt(new window) E-mail(new window) Excel Download
  • Journal title : ALGAE
  • Volume 30, Issue 4,  2015, pp.281-290
  • Publisher : The Korean Society of Phycology
  • DOI : 10.4490/algae.2015.30.4.281
 Title & Authors
Ingestion of the unicellular cyanobacterium Synechococcus by the mixotrophic red tide ciliate Mesodinium rubrum
Yoo, Yeong Du; Seong, Kyeong Ah; Myung, Geumog; Kim, Hyung Seop; Jeong, Hae Jin; Palenik, Brian; Yih, Wonho;
  PDF(new window)
We explored phagotrophy of the phototrophic ciliate Mesodinium rubrum on the cyanobacterium Synechococcus. The ingestion and clearance rates of M. rubrum on Synechococcus as a function of prey concentration were measured. In addition, we calculated grazing coefficients by combining the field data on abundance of M. rubrum and co-occurring Synechococcus spp. with laboratory data on ingestion rates. The ingestion rate of M. rubrum on Synechococcus sp. linearly increased with increasing prey concentrations up to approximately 1.9 × 106 cells mL-1, to exhibit sigmoidal saturation at higher concentrations. The maximum ingestion and clearance rates of M. rubrum on Synechococcus were 2.1 cells predator-1 h-1 and 4.2 nL predator-1 h-1, respectively. The calculated grazing coefficients attributable to M. rubrum on cooccurring Synechococcus spp. reached 0.04 day-1. M. rubrum could thus sometimes be an effective protistan grazer of Synechococcus in marine planktonic food webs. M. rubrum might also be able to form recurrent and massive blooms in diverse marine environments supported by the unique and complex mixotrophic arrays including phagotrphy on hetrotrophic bacteria and Synechococcus as well as digestion, kleptoplastidy and karyoklepty after the ingestion of cryptophyte prey.
grazing impact;ingestion;Mesodinium;mixotrophy;Synechococcus;
 Cited by
Apple, J. K., Strom, S. L., Palenik, B. & Brahamsha, B. 2011. Variability in protist grazing and growth on different marine Synechococcus isolates. Appl. Environ. Microbiol. 77:3074-3084. crossref(new window)

Berge, T., Hansen, P. J. & Moestrup, Ø. 2008. Feeding mechanism, prey specificity and growth in light and dark of the plastidic dinoflagellate Karlodinium armiger. Aquat. Microb. Ecol. 50:279-288. crossref(new window)

Boenigk, J., Matz, C., Jürgens, K. & Arndt, H. 2001. The influence of preculture conditions and food quality on the ingestion and digestion process of three species of heterotrophic nanoflagellates. Microb. Ecol. 42:168-176.

Burkill, P. H., Leakey, R. J. G., Owens, N. J. P. & Mantoura, R. F. C. 1993. Synechococcus and its importance to the microbial foodweb of the northwestern Indian Ocean. Deep Sea Res. II Top. Stud. Oceanogr. 40:773-782. crossref(new window)

Christaki, U., Courties, C., Karayanni, H., Giannakourou, A., Maravelias, C., Kormas, K. A. & Lebaron, P. 2002. Dynamic characteristics of Prochlorococcus and Synechococcus consumption by bacterivorous nanoflagellates. Microb. Ecol. 43:341-352. crossref(new window)

Christaki, U., Jacquet, S., Dolan, J. R., Vaulot, D. & Rassoulzadegan, F. 1999. Growth and grazing on Prochlorococcus and Synechococcus by two marine ciliates. Limnol. Oceanogr. 144:52-61.

Crawford, D. W. 1989. Mesodinium rubrum: the phytoplankter that wasn’t. Mar. Ecol. Prog. Ser. 58:161-174. crossref(new window)

Dolan, J. R. & Šimek, K. 1998. Ingestion and digestion of an autotrophic picoplankter, Synechococcus, by a heterotrophic nanoflagellate, Bodo saltans. Limnol. Oceanogr. 43:1740-1746. crossref(new window)

Fenchel, T. & Hansen, P. J. 2006. Motile behaviour of the bloom-forming ciliate Mesodinium rubrum. Mar. Biol. Res. 2:33-40. crossref(new window)

Ferris, M. J. & Palenik, B. 1998. Niche adaptation in ocean cyanobacteria. Nature 396:226-228. crossref(new window)

Frost, B. W. 1972. Effects of size and concentration of food particles on the feeding behavior of the marine planktonic copepod Calanus pacificus. Limnol. Oceanogr. 17:805-815. crossref(new window)

Glibert, P. M., Heil, C. A., Hollander, D. J., Revilla, M., Hoare, A., Alexander, J. & Murasko, S. 1972. Evidence for dissolved organic nitrogen and phosphorus uptake during a cyanobacterial bloom in Florida Bay. Mar. Ecol. Prog. Ser. 280:73-83.

Glover, H. E., Campbell, L. & Prézelin, B. B. 1986. Contribution of Synechococcus spp. to size-fractioned primary productivity in three water masses in the Northwest Atlantic Ocean. Mar. Biol. 91:193-203. crossref(new window)

Guillard, R. R. L. & Ryther, J. H. 1962. Studies of marine planktonic diatoms. I. Cyclotella nana Hustedt and Detonula confervacea (Cleve) Grun. Can. J. Microbiol. 8:229-239. crossref(new window)

Guillou, L., Jacquet, S., Chrétiennot-Dinet, M. -J. & Vaulot, D. 2001. Grazing impact of two small heterotrophic flagellates on Prochlorococcus and Synechococcus. Aquat. Microb. Ecol. 26:201-207. crossref(new window)

Hansen, P. J., Bjørnsen, P. K. & Hansen, B. W. 1997. Zooplankton grazing and growth: scaling within the 2-2,000-μm body size range. Limnol. Oceanogr. 42:687-704. crossref(new window)

Hansen, P. J., Moldrup, M., Tarangkoon, W., Garcia-Cuetos, L. & Moestrup, Ø. 2012. Direct evidence for symbiont sequestration in the marine red tide ciliate Mesodinium rubrum. Aquat. Microb. Ecol. 66:63-75. crossref(new window)

Hansen, P. J., Nielsen, L. T., Johnson, M., Berge, T. & Fylnn, K. J. 2013. Acquired phototrophy in Mesodinium and Dinophysis: a review of cellular organization, prey selectivity, nutrient uptake and bioenergetics. Harmful Algae 28:126-139. crossref(new window)

Heinbokel, J. F. 1978. Studies on the functional role of tintinnids in the Southern California Bight. I. Grazing and growth rates in laboratory cultures. Mar. Biol. 47:177-189. crossref(new window)

Herfort, L., Peterson, T. D., McCue, L. A., Crump, B. C., Prahl, F. G., Baptista, A. M., Campbell, V., Warnick, R., Selby, M., Roegner, G. C. & Zuber, P. 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. crossref(new window)

Huang, S., Wilhelm, S. W., Harvey, H. R., Taylor, K., Jiao, N. & Chen, F. 2012. Novel lineages of Prochlorococcus and Synechococcus in the global oceans. ISME J. 6:285-297. crossref(new window)

Jeong, H. J., Park, J. Y., Nho, J. H., Park, M. O., Ha, J. H., Seong, K. A., Jeng, C., Seong, C. N., Lee, K. Y. & Yih, W. H. 2005. Feeding by the red-tide dinoflagellates on the cyanobacterium Synechococcus. Aquat. Microb. Ecol. 41:131-143. crossref(new window)

Jeong, H. J., Seong, K. A., Kang, N. S., Yoo, Y. D., Nam, S. W., Park, J. Y., Shin, W., Glibert, P. M. & Johns, D. 2010. Feeding by raphidophytes on the cyanobacterium Synechococcus sp. Aquat. Microb. Ecol. 58:181-195. crossref(new window)

Jeong, H. J., Shim, J. H., Kim, J. S., Park, J. Y., Lee, C. W. & Lee, Y. 1999. Feeding by the mixotrophic thecate dinoflagellate Fragilidium cf. mexicanum on red-tide and toxic dinoflagellates. Mar. Ecol. Prog. Ser. 176:263-277. crossref(new window)

Jeong, H. J., Yoo, Y. D., Kang, N. S., Lim, A. S., Seong, K. A., Lee, S. Y., Lee, M. J., Lee, K. H., Kim, H. S., Shin, W., Nam, S. W., Yih, W. & Lee, K. 2012. Heterotrophic feeding as a newly identified survival strategy of the dinoflagellate Symbiodinium. Proc. Natl. Acad. Sci. U. S. A. 109:12604-12609. crossref(new window)

Jeong, H. J., Yoo, Y. D., Lee, K. H., Kim, T. H., Seong, K. A., Kang, N. S., Lee, S. Y., Kim, J. S., Kim, S. & Yih, W. 2013. Red tides in Masan Bay, Korea in 2004-2005. I. Daily variations in the abundance of red-tide organisms and environmental factors. Harmful Algae 30(Suppl. 1):S75-S88. crossref(new window)

Johnson, M. D., Oldach, D., Delwiche, C. F. & Stoecker, D. K. 2007. Retention of transcriptionally active cryptophyte nuclei by the ciliate Myrionecta rubra. Nature 445:426-428. crossref(new window)

Johnson, M. D. & Stoecker, D. K. 2005. Role of feeding in growth and photophysiology of Myrionecta rubra. Aquat. Microb. Ecol. 39:303-312. crossref(new window)

Johnson, P. W. & Sieburth, J. M. 1979. Chroococcoid cyanobacteria in the sea: a ubiquitous and diverse phototrophic biomass. Limnol. Oceanogr. 24:928-935. crossref(new window)

Landry, M. R., Kirshtein, J. & Constantinou, J. 1996. Abundances and distributions of picoplankton populations in the Central Equatorial Pacific from 12°N to 12°S, 140°W. Deep Sea Res. Part II Top. Stud. Oceanogr. 43:871-890. crossref(new window)

Lee, K. H., Jeong, H. J., Yoon, E. Y., Jang, S. H., Kim, H. S. & Yih, W. 2014. Feeding by common heterotrophic dinoflagellates and a ciliate on the red-tide ciliate Mesodinium rubrum. Algae 29:153-163. crossref(new window)

Li, W. K. W. 1994. Primary production of prochlorophytes, cyanobacteria, and eukaryotic ultraphytoplankton: measurements from flow cytometric sorting. Limnol. Oceanogr. 39:169-175. crossref(new window)

Lignell, R., Seppälä, J., Kuuppo, P., Tammimen, T., Andersen, T. & Gismervik, I. 2003. Beyond bulk properties: responses of coastal summer plankton communities to nutrient enrichment in the northern Baltic Sea. Limnol. Oceanogr. 48:189-209. crossref(new window)

Lindholm, T. 1985. Mesodinium rubrum: a unique photosynthetic ciliate. Adv. Aquat. Microbiol. 3:1-48.

Liu, H., Dagg, M. J. & Strom, S. 2005. Grazing by the calanoid copepod Neocalanus cristatus on the microbial food web in the coastal Gulf of Alaska. J. Plankton Res. 27:647-662. crossref(new window)

Liu, M., Xiao, T., Sun, J., Wei, H., Wu, Y., Zhao, Y. & Zhang, W. 2013. Bacterial community structures associated with a natural spring phytoplankton bloom in the Yellow Sea, China. Deep Sea Res. Part II Top. Stud. Oceanogr. 97:85-92. crossref(new window)

Marañón, E., Behrenfeld, M. J., González, N., Mouriño, B. & Zubkov, M. V. 2003. High variability of primary production in oligotrophic waters of the Atlantic Ocean: uncoupling from phytoplankton biomass and size structure. Mar. Ecol. Prog. Ser. 257:1-11. crossref(new window)

Menden-Deuer, S. & Lessard, E. J. 2000. Carbon to volume relationships for dinoflagellates, diatoms, and other protist plankton. Limnol. Oceanogr. 45:569-579. crossref(new window)

Murrell, M. C. & Lores, E. M. 2004. Phytoplankton and zooplankton seasonal dynamics in a subtropical estuary: importance of cyanobacteria. J. Plankton Res. 26:371-382. crossref(new window)

Myung, G., Kim, H. S., Park, J. S., Park, M. G. & Yih, W. 2011. Population growth and plastid type of Myrionecta rubra depend on the kinds of available cryptomonad prey. Harmful Algae 10:536-541. crossref(new window)

Myung, G., Kim, H. S., Park, J. W., Park, J. S. & Yih, W. 2013. Sequestered plastids in Mesodinium rubrum are functionally active up to 80 days of phototrophic growth without cryptomonad prey. Harmful Algae 27:82-87. crossref(new window)

Myung, G., Yih, W., Kim, H. S., Park, J. S. & Cho, B. C. 2006. Ingestion of bacterial cells by the marine photosynthetic ciliate Myrionecta rubra. Aquat. Microb. Ecol. 44:175-180. crossref(new window)

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. crossref(new window)

Ong, L. J. & Glazer, A. N. 1991. Phycoerythrins of marine unicellular cyanobacteria. I. Bilin types and locations and energy transfer pathways in Synechococcus spp. phycoerythrins. J. Biol. Chem. 266:9515-9527.

Park, J. S., Myung, G., Kim, H. S., Cho, B. C., Yih, W. 2007. Growth responses of the marine photosynthetic ciliate Myrionecta rubra to different cryptomonad strains. Aquat. Microb. Ecol. 48:83-90. crossref(new window)

Park, M. G., Kim, S., Kim, H. S., Myung, G., Kang, Y. G. & Yih, W. 2006. First successful culture of the marine dinoflagellate Dinophysis acuminata. Aquat. Microb. Ecol. 45:101-106. crossref(new window)

Phlips, E. J., Zeman, C. & Hansen, P. 1989. Growth, photosynthesis, nitrogen fixation and carbohydrate production by a unicellular cyanobacterium, Synechococcus sp. (Cyanophyta). J. Appl. Phycol. 1:137-145. crossref(new window)

Powell, L. M., Bowman, J. P., Skerratt, J. H., Franzmann, P. D. & Burton, H. R. 2005. Ecology of a novel Synechococcus clade occurring in dense populations in saline Antarctic lakes. Mar. Ecol. Prog. Ser. 291:65-80. crossref(new window)

Reguera, B., Velo-Suárez, L., Raine, R. & Park, M. G. 2012. Harmful Dinophysis species: a review. Harmful Algae 14:87-106. crossref(new window)

Sherr, B. F., Sherr, E. B. & Fallon, R. D. 1987. Use of monodispersed, fluorescently labeled bacteria to estimate in situ protozoan bacterivory. Appl. Environ. Microbiol. 53:958-965.

Strom, S. L., Brahamsha, B., Fredrickson, K. A., Apple, J. K. & Rodríguez, A. G. 2012. A giant cell surface protein in Synechococcus WH8102 inhibits feeding by a dinoflagellate predator. Environ. Microbiol. 14:807-816. crossref(new window)

Sullivan, L. J. & Gifford, D. J. 2004. Diet of the larval ctenophore Mnemiopsis leidyi A. Agassiz (Ctenophora, Lobata). J. Plankton Res. 26:417-431. crossref(new window)

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. crossref(new window)

Walker, T. D. & Marchant, H. J. 1989. The seasonal occurrence of chroococcoid cyanobacteria at an Antarctic coastal site. Polar Biol. 9:193-196. crossref(new window)

Waterbury, J. B., Watson, S. W., Guillard, R. R. L. & Brand, L. E. 1979. Widespread occurrence of a unicellular, marine, planktonic cyanobacterium. Nature 277:293-294. crossref(new window)

Yih, W., Kim, H. S., Jeong, H. J., Myung, G. & Kim, Y. G. 2004a. Ingestion of cryptophyte cells by the marine photosynthetic ciliate Mesodinium rubrum. Aquat. Microb. Ecol. 36:165-170. crossref(new window)

Yih, W., Kim, H. S., Myung, G. & Kim, Y. G. 2004b. Rapid feeding on live organisms of the phototrophic ciliate Mesodinium rubrum by Farrer's Scallop Chlamys farreri. J. Mar. Biotechnol. 6:142-145.

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. crossref(new window)