Direct evidence for symbiont sequestration in the marine red tide ciliate Mesodinium rubrum

Aquatic Microbial Ecology

Volumn 66, Issue 1, 2012, Pages 63-75

  Hansen, P J ^a   Moldrup, M ^a   Tarangkoon, W ^a,b   Garcia Cuetos, L ^a   Moestrup, O ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

^b RAJAMANGALA UNIVERSITY OF TECHNOLOGY SRIVIJAYA   (Thailand)

Author keywords

Cryptophytes; Ingestion; Mesodinium rubrum; Symbionts

Indexed keywords

CILIOPHORA; CRYPTOPHYTA; DINOPHYCEAE; MESODINIUM RUBRUM; MYRIONECTA RUBRA; TELEAULAX; TELEAULAX ACUTA; TELEAULAX AMPHIOXEIA;

EID: 84859241516     PISSN: 09483055     EISSN: None     Source Type: Journal    
DOI: 10.3354/ame01559     Document Type: Article

References (44)

1. Bhattacharya D, Helmchen T, Bibeau C (1995) Comparisons of nuclear-encoded small subunit ribosomal RNAs reveal the evolutionary position of the Glaucocystophyta. Mol Biol Evol 12: 415-420
2. Douglas S, Zauner S, Fraunholz M, Beaton M and others (2001) The highly reduced genome of an enslaved algal nucleus. Nature 410: 1091-1096 (Pubitemid 32391039)
3. Felsenstein J (1981) Evolutionary trees from DNA se quences: a maximum likelihood approach. J Mol Evol 17: 368-376 (Pubitemid 11016207)
4. Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39: 783-791
5. Frommlet J, Iglesias-Rodríguez D (2008) Microsatellite geno typing of single cells of the dinoflagellate species Lingulodinium polyedrum (Dinophyceae): a novel ap proach for marine microbial population studies. J Phycol 44: 1116-1125
6. Garcia-Cuetos L, Moestrup Ø, Hansen PJ, Daugbjerg N (2010) The toxic dinoflagellate Dinophysis acuminata harbors permanent chloroplasts of cryptomonad origin, not kleptochloroplasts. Harmful Algae 9: 25-38
7. Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52: 696-704 (Pubitemid 37365050)
8. Guillard RRL (1975) Culture of phytoplankton for feeding marine invertebrates. In: WL Smith WL, Chanley MH (eds) Culture of marine invertebrate animals. Plenum Pub, New York, NY, p 29-60
9. Gustafson DE Jr, Stoecker DK, Johnson MD, Van Heukelem WF, Sneider K (2000) Cryptophyte algae are robbed of their organelles by the marine ciliate Mesodinium rubrum. Nature 405: 1049-1052 (Pubitemid 30447787)
10. Hackett JD, Mengmong T, Kulis DM, Fux E, Hess P, Bire R, Anderson DM (2009) DSP toxin production de novo in cultures of Dinophysis acuminata (Dinophyceae) from North America. Harmful Algae 8: 873-879
11. Hall TA (1999) Bioedit: a user friendly biological sequence alignment editor and analysis program from windows 95/97/NT. Nucleic Acids Symp Ser 41:95-98
12. Hansen PJ, Fenchel T (2006) The bloom-forming ciliate Mesodinium rubrum harbors a single permanent endosymbiont. Mar Biol Res 2: 169-177 (Pubitemid 44091982)
13. Hansen G, Daugbjerg N, Franco JM (2003) Morphology, toxin composition and LSU rDNA phylogeny of Alexandrium minutum (Dinophyceae) from Denmark, with some morphological observations on other European strains. Harmful Algae 2: 317-335 (Pubitemid 37379186)
14. Hibberd DJ (1977) Observation on ultrastructure of cryptomonad endosymbiont of red-water ciliate Mesodinium rubrum. J Mar Biol Ass UK 57: 45-61
15. Hill DRA (1991) The systematic of cryptomonads. In: Patterson DJ, Larsen J (eds) Biology of free-living heterotrophic flagellates. Syst Assoc Spec 45:235-240
16. Hoef-Emden K (2008) Molecular phylogeny of phycocyanin-containing cryptophytes: evolution of biliproteins and geographic distribution. J Phycol 44: 985-993
17. Hoef-Emden K, Marin B, Melkonian M (2002) Nuclear and nucleomorph SSU rDNA phylogeny in the Cryptophyta and the evolution of cryptophyte diversity. J Mol Evol 55: 161-179 (Pubitemid 34734780)
18. Huelsenbeck JP, Ronquist F (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17: 754-755 (Pubitemid 32851390)
19. Johnson MD, Stoecker DK (2005) Role of feeding in growth and photophysiology of Myrionecta rubra. Aquat Microb Ecol 39: 303-312 (Pubitemid 40962706)
20. Johnson MD, Tengs T, Oldach D, Stoecker DK (2006) Sequestration, performance, and functional control of cryptophyte plastids in the ciliate Myrionecta rubra (Ciliophora). J Phycol 42: 1235-1246 (Pubitemid 44934818)
21. Johnson MD, Oldach D, Delwiche CF, Stoecker DK (2007) Retention of transcriptionally active cryptophyte nuclei by the ciliate Myrionecta rubra. Nature 445: 426-428 (Pubitemid 46160909)
22. Katoh K, Toh H (2008) Recent developments in the MAFFT multiple sequence alignment program. Brief Bioinform 9: 286-298 (Pubitemid 351890825)
23. Lane CE, Archibald JM (2006) Novel nucleomorph genome architecture in the cryptomonad genus Hemiselmis. J Eukaryot Microbiol 53: 515-521 (Pubitemid 44813392)
24. Lane CE, Khan H, MacKinnon M, Fong A, Theophilou S, Archibald JM (2006) Insight into the diversity and evolution of the cryptomonad nucleomorph genome. Mol Biol Evol 23: 856-865 (Pubitemid 43726049)
25. Lindholm T (1985) Mesodinium rubrum - a unique photosynthetic ciliate. Adv Aquat Microb 3: 1-48
26. Moeller HV, Johnson MD, Falkowski PG (2011) Photoacclimation in the phototrophic ciliate Mesodinium rubrum (Ciliophora). J Phycol 47: 324-332
27. Myung G, Kim HS, Park JS, Park MG, Yih W (2011) Population growth and plastid type of Myrionecta rubra depend on the kinds of available cryptomonad prey. Harmful Algae 10: 536-541
28. Nagai S, Nishitani G, Tomaru Y, Sakiyama S, Kamiyama T (2008) Predation by the toxic dinoflagellate Dinophysis fortii on the ciliate Myrionecta rubra and observation of sequestration of ciliate chloroplasts. J Phycol 44: 909-922
29. Nishitani G, Nagai S, Sakiyama S, Kamiyama T (2008a) Successful cultivation of the toxic dinoflagellate Dinophysis caudata (Dinophyceae). Plankton Benthos Res 3: 78-85 (Pubitemid 351976223)
30. Nishitani G, Nagai S, Takano Y, Sakiyama S, Baba K, Kamiyama T (2008b) Growth characteristics and phylogenetic analysis of the marine dinoflagellate Dinophysis infundibulus (Dinophyceae). Aquat Microb Ecol 52: 209-221
31. Nunn GB, Theisen BF, Christensen B, Arctander P (1996) Simplicity-correlated size growth of the nuclear 28S ribosomal RNA D3 expansion segment in the crustacean order Isopoda. J Mol Evol 42: 211-223 (Pubitemid 26102488)
32. Park MG, Kim S, Kim HS, Myung G, Kang YG, Yih W (2006) First successful culture of the marine dinoflagellate Dinophysis acuminata. Aquat Microb Ecol 45: 101-106 (Pubitemid 46025943)
33. Park JS, Myung G, Kim HS, Cho BC, Yih W (2007) Growth responses of the marine photosynthetic ciliate Myrionecta rubra to different cryptomonad strains. Aquat Microb Ecol 48: 83-90 (Pubitemid 351525821)
34. Park MG, Kim M, Kim S, Yih W (2010) Does Dinophysis caudata (Dinophyceae) have permanent plastids? J Phycol 46: 236-242
35. Posada D, Crandall KA (1998) MODELTEST: testing the model of DNA substitution. Bioinformatics 14: 817-818 (Pubitemid 28552116)
36. Riisgaard K, Hansen PJ (2009) Role of food uptake for photosynthesis, growth and survival of the mixotrophic dinoflagellate Dinophysis acuminata. Mar Ecol Prog Ser 381: 51-62
37. Rowley JC, Moran DT (1975) Simple procedure for mounting wrinkle-free sections on formvar-coated slot grids. Ultramicroscopy 1: 151-155
38. Scholin CA, Herzog M, Sogin M, Anderson DM (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
39. Smith M, Hansen PJ (2007) Interaction between Mesodinium rubrum and its prey: importance of irradiance, prey concentration, and pH. Mar Ecol Prog Ser 338: 61-70 (Pubitemid 46983978)
40. *and other methods). Sinauer Associates, Sunderland, MA
41. Taylor FJR, Blackbourn DJ, 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
42. Wilgenbusch JC, Warren DL, Swofford DL (2004) AWTY: a system for graphical exploration of MCMC convergence in Bayesian phylogenetic inference. Available at http://ceb.csit.fsu.edu/awty/
43. Yang Z, Rannala B (1997) Bayesian phylogenetic inference using DNA sequences: a Markov chain Monte Carlo method. Mol Biol Evol 14: 717-724 (Pubitemid 27287292)
44. Yih W, Kim HS, Jeong HJ, Myung G, Kim YG (2004) Ingestion of cryptophyte cells by the marine photosynthetic ciliate Mesodinium rubrum. Aquat Microb Ecol 36: 165-170 (Pubitemid 39104226)