Strombidium rassoulzadegani: A model species for chloroplast retention in Oligotrich Ciliates

Frontiers in Marine Science

Volumn 5, Issue JUN, 2018, Pages

  McManus, George B ^a   Liu, Weiwei ^a,b   Cole, Rachel A ^a   Biemesderfer, Daniel ^a   Mydosh, Jennifer L ^a  

^a UNIVERSITY OF CONNECTICUT   (United States)

^b SOUTH CHINA SEA INSTITUTE OF OCEANOLOGY   (China)

Author keywords

Chloroplast; Encystment; Kleptoplasty; Mixotrophy; Oligotrich

Indexed keywords

EID: 85048630860     PISSN: None     EISSN: 22967745     Source Type: Journal    
DOI: 10.3389/fmars.2018.00205     Document Type: Article

References (36)

1. Blackbourn, D. J., Taylor, F. J. R., and Blackbourn, J. (1973). Foreign organelle retention by ciliates. J. Protozool. 20, 286-288. doi: 10.1111/j.1550-7408.1973.tb00877.x
2. Chen, B., Liu, H., and Lau, M. T. S. (2010). Grazing and growth responses of a marine oligotrichous ciliate fed with two nanoplankton: does food quality matter for micrograzers? Aquatic Ecol. 44, 113-119. doi: 10.1007/s10452-009-9264-5
3. Faure-Fremiet, E. (1948). Le rythme de maree du S. oculatum Gruber. Bull. Biol. France Belgique 82, 3-23
4. Flynn, K. J., and Mitra, A. (2009). Building the 'perfect beast': modelling mixotrophic plankton. J. Plankton Res. 31, 965-992. doi: 10.1093/plankt/fbp044
5. Flynn, K. J., Stoecker, D. K., Mitra, A., Raven, J. A., Glibert, P. M., Hansen, P. J., et al. (2013). Misuse of the phytoplankton-zooplankton dichotomy: the need to assign organisms as mixotrophs within plankton functional types. J. Plankton Res. 35, 3-11. doi: 10.1093/plankt/fbs062
6. Guillard, R. R., and Ryther, J. H. (1962). Studies of marine planktonic diatoms. I. Cyclotella nana Hustedt, and Detonula confervacea (cleve). Gran. Can. J. Microbiol. 8, 229-239. doi: 10.1139/m62-029
7. Johnson, M. D. (2011). Acquired phototrophy in ciliates: a review of cellular interactions and structural adaptations. J. Eukaryot. Microbiol. 58, 185-195. doi: 10.1111/j.1550-7408.2011.00545.x
8. Johnson, M. D., Oldach, D., Delwiche, C. F., and Stoecker, D. K. (2007). Retention of transcriptionally active cryptophyte nuclei by the ciliate Myrionecta rubra. Nature 445, 426-428. doi: 10.1038/nature05496
9. Jonsson, P. R. (1994). Tidal rhythm of cyst formation in the rock pool ciliate Strombidium-oculatum Gruber (Ciliophora, Oligotrichida)-a description of the functional biology and an analysis of the tidal synchronization of encystment. J. Exp. Mar. Biol. Ecol. 175, 77-103. doi: 10.1016/0022-0981(94)90177-5
10. Katz, L. A., McManus, G. B., Snoeyenbos-West, O. L. O., Griffin, A., Pirog, K., Costas, B., et al. (2005). Reframing the 'Everything is everywhere' debate: evidence for high gene flow and diversity in ciliate morphospecies. Aquat. Microbial Ecol. 41, 55-65. doi: 10.3354/ame041055
11. Kim, G. H., Han, J. H., Kim, B., Han, J. W., Nam, S. W., Shin, W., et al. (2016). Cryptophyte gene regulation in the kleptoplastidic, karyokleptic ciliate Mesodinium rubrum. Harmful Algae 52, 23-33. doi: 10.1016/j.hal.2015.12.004
12. Lasek-Nesselquist, E., Wisecaver, J. H., Hackett, J. D., and Johnson, M. D. (2015). Insights into transcriptional changes that accompany organelle sequestration from the stolen nucleus of Mesodinium rubrum. BMC Genomics 16:805. doi: 10.1186/s12864-015-2052-9
13. Laval-Peuto, M., and Febvre, M. (1986). On plastid symbiosis in Tontonia appendiculariformis (Ciliophora, Oligotrichina). Biosystems 19, 137-158. doi: 10.1016/0303-2647(86)90026-2
14. Laval-Peuto, M., Salvano, P., Gayol, P., and Greuet, C. (1986). Mixotrophy in marine planktonic ciliates: ultrastructural study of Tontonia appendiculariformis (Ciliophora, Oligotrichina). Mar. Microb. Food Webs. 1, 81-104
15. McManus, G. B., and Fuhrman, J. A. (1986). Photosynthetic pigments in the ciliate Laboea strobila from Long Island Sound, USA. J. Plankton Res. 8, 317-327. doi: 10.1093/plankt/8.2.317
16. McManus, G. B., Schoener, D. M., and Haberlandt, K. (2012). Chloroplast symbiosis in a marine ciliate: ecophysiology and the risks and rewards of hosting foreign organelles. Front. Microbiol. 3:321. doi: 10.3389/fmicb.2012.00321
17. McManus, G. B., Xu, D., Costas, B. A., and Katz, L. A. (2010). Genetic identities of cryptic species in the Strombidium stylifer/apolatum/oculatum cluster, including a description of Strombidium rassoulzadegani n. sp. J. Euk. Microbiol. 57, 369-378. doi: 10.1111/j.1550-7408.2010.00485.x
18. McManus, G. B., Zhang, H., and Lin, S. (2004). Marine planktonic ciliates that prey on macroalgae and enslave their chloroplasts. Limnol. Oceanogr. 49, 308-313. doi: 10.4319/lo.2004.49.1.0308
19. Medlin, L., Elwood, H. J., Stickel, S., and Sogin, M. L. (1988). The characterization of enzymatically amplified eukaryotic 16S-like rRNA-coding regions. Gene 71, 491-499. doi: 10.1016/0378-1119(88)90066-2
20. Mitra, A., Flynn, K. J., Tillmann, U., Raven, J. A., Caron, D., Stoecker, D. K., 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: 10.1016/j.protis.2016.01.003
21. Montagnes, D. J. S., Berger, J. D., and Taylor, F. J. R. (1996). Growth rate of the marine planktonic ciliate Strombidinopsis cheshiri Snyder and Ohman as a function of food concentration and interclonal variability. J. Exp. Mar. Biol. Ecol. 206, 121-132. doi: 10.1016/S0022-0981(96)02626-3
22. Montagnes, D. J., Lowe, C. D., Poultonb, A., and Jonsson, P. R. (2002a). Redescription of Strombidium oculatum Gruber 1884 (Ciliophora, Oligotrichia). J. Eukaryot. Microbiol. 49, 329-337. doi: 10.1111/j.1550-7408.2002.tb00379.x
23. Montagnes, D. J. S., Wilson, D., Brooks, S. J., Lowe, C., and Campey, M. (2002b). Cyclical behaviour of the tide-pool ciliate Strombidium oculatum. Aquat. Microbial. Ecol. 28, 55-68. doi: 10.3354/ame028055
24. Pedersen, M. F., and Hansen, P. J. (2003). Effects of high pH on the growth and survival of six marine heterotrophic protists. Mar. Ecol. Prog. Ser. 260, 33-41. doi: 10.3354/meps260033
25. Putt, M. (1990). Abundance, chlorophyll content and photosynthetic rates of ciliates inthe Nordic Seas during summer. Deep Sea Res. 37, 1713-1731. doi: 10.1016/0198-0149(90)90073-5
26. Raven, J. A. (1997). Phagotrophy in phototrophs. Limnol. Oceanogr. 42, 198-205. doi: 10.4319/lo.1997.42.1.0198
27. Santoferrara, L. F., Guida, S., Zhang, H., and McManus, G. B. (2014). De Novo transcriptomes of a mixotrophic and a heterotrophic ciliate from marine plankton. PLoS ONE 9:e101418. doi: 10.1371/journal.pone.0101418
28. Schoener, D. M., and McManus, G. B. (2012). Plastid retention, use, and replacement in a kleptoplastidic ciliate. Aquat. Microb. Ecol. 67, 177-187. doi: 10.3354/ame01601
29. Schoener, D. M., and McManus, G. B. (2017). Growth, grazing, and inorganic C and N uptake in a mixotrophic and a heterotrophic ciliate. J. Plankton Res. 39, 379-391. doi: 10.1093/plankt/fbx014
30. Stanton, B. A., Biemesderfer, D., Wade, J. B., and Giebisch, G. (1981). Structural and functional study of the rat distal nephron: effects of potassium adaptation and depletion. Kidney Int. 19, 36-48. doi: 10.1038/ki.1981.5
31. Stoecker, D. K. (1998). Conceptual models of mixotrophy in planktonic protists and some ecological and evolutionary implications. Eur. J. Protistol. 34, 281-290. doi: 10.1016/S0932-4739(98)80055-2
32. Stoecker, D. K., and Silver, M. W. (1987). Chloroplast retention by marine planktonic ciliates. Ann. N. Y. Acad. Sci. 503, 562-565. doi: 10.1111/j.1749-6632.1987.tb40646.x
33. Stoecker, D. K., Johnson, M. D., de Vargas, C., and Not, F. (2009). Acquired phototrophy in aquatic protists. Aquat. Microbial Ecol. 57, 279-310. doi: 10.3354/ame01340
34. Stoecker, D. K., Michaels, A. E., and Davis, L. H. (1987). Large proportion of marine planktonic ciliates found to contain functional chloroplasts. Nature 326, 790-792. doi: 10.1038/326790a0
35. Wisecaver, J. H., and Hackett, J. D. (2010). Transcriptome analysis reveals nuclear-encoded proteins for the maintenance of temporary plastids in the dinoflagellate Dinophysis acuminata. BMC Genomics 11:366. doi: 10.1186/1471-2164-11-366
36. Yang, J., Löder, M. G. J., Boersma, M., and Wiltshire, K. H. (2015). Factors influencing the grazing response of the marine oligotrichous ciliate Strombidium cf. sulcatum. Aquat. Microb. Ecol. 74, 59-71. doi: 10.3354/ame01729