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The study of symbiosis and interactions between ciliates and algae: current status and future directions
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    Abstract:

    Ubiquitous ciliate-algae symbiosis plays a key role in the water environment. In this review, we summarized the current knowledge on ecological functions of ciliate-algae symbiosis. Moreover, the steps of symbiosis establishment and the interactions between Paramecium bursaria and Chlorella sp., the symbiotic relationship and interaction between Mesodinium rubrum and cryptophytes were summarized. Furthermore, several key biological questions on ciliate-algae symbiosis were raised, including the molecular mechanisms of the functions of Paramecium digestive vacuole (DV) and perialgal vacuole (PV) membrane, the establishment process of the symbiosis between M. rubrum and cryptophytes, and the roles of M. rubrum in the symbiotic process. Finally, we prospected the future directions on ciliate-algae symbiosis study.

    Reference
    [1] ANTON dB. Die Erscheinung der Symbiose[M]. Vortrag, Berlin, Boston: de Gruyter. 1879.
    [2] DOUGLAS AE. Are endosymbioses mutualistic?[J]. Trends in Ecology & Evolution, 1989, 4(11): 350-352.
    [3] HEATH KD, TIFFIN P. Context dependence in the coevolution of plant and rhizobial mutualists[J]. Proceedings Biological Sciences, 2007, 274(1620): 1905-1912.
    [4] MULLER-PARKER G, DAVY SK. Temperate and tropical algal-sea anemone symbioses[J]. Invertebrate Biology, 2001, 120(2): 104-123.
    [5] Nejman D, Livyatan I, Fuks G, Gavert N, Zwang Y, Geller LT, Rotter-Maskowitz A, Weiser R, Mallel G, Gigi E, Meltser A, Douglas GM, Kamer I, Gopalakrishnan V, Dadosh T, Levin-Zaidman S, Avnet S, Atlan T, Cooper ZA, Arora R, et al. The human tumor microbiome is composed of tumor type-specific intracellular bacteria[J]. Science, 2020, 368(6494): 973-980.
    [6] QIU DJ, HUANG LM, LIU S, LIN SJ. Nuclear, mitochondrial and plastid gene phylogenies of Dinophysis Miles (Dinophyceae): evidence of variable types of chloroplasts[J]. PLoS One, 2011, 6(12): e29398.
    [7] STOECKER DK, SILVER MW, MICHAELS AE, DAVIS LH. Enslavement of algal chloroplasts by four Strombidium spp. (Ciliophora, oligotrichida)[J]. Marine microbial food webs, 1988, 3(2): 79-100.
    [8] NOWACK ECM, MELKONIAN M. Endosymbiotic associations within protists[J]. Philosophical Transactions of the Royal Society of London Series B, Biological Sciences, 2010, 365(1541): 699-712.
    [9] ANDERSON OR. Living together in the plankton: a survey of marine protist symbioses[J]. Acta Protozoologica, 2014, 53(1): 29-38.
    [10] DAVY SK, ALLEMAND D, WEIS VM. Cell biology of cnidarian-dinoflagellate symbiosis[J]. Microbiology and Molecular Biology Reviews: MMBR, 2012, 76(2): 229-261.
    [11] DECELLE J, COLIN S, FOSTER RA. Photosymbiosis in Marine Planktonic Protists[M]. Marine Protists. Tokyo: Springer Japan, 2015: 465-500.
    [12] JEPHCOTT TG, ALVES-DE-SOUZA C, GLEASON FH, van OGTROP FF, SIME-NGANDO T, KARPOV SA, GUILLOU L. Ecological impacts of parasitic chytrids, syndiniales and perkinsids on populations of marine photosynthetic dinoflagellates[J]. Fungal Ecology, 2016, 19: 47-58.
    [13] KEMPF SC. Symbiosis between the zooxanthella Symbiodinium (=Gymnodinium) microadriaticum (freudenthal) and four species of nudibranchs[J]. The Biological Bulletin, 1984, 166(1): 110-126.
    [14] KEMPF SC. A ‘primitive’ symbiosis between the aeolid nudibranch Berghia verrucicornis (A. Costa, 1867) and a Zooxanthella[J]. Journal of Molluscan Studies, 1991, 57(Supplement_Part_4): 75-85.
    [15] KERNEY R, KIM E, HANGARTER RP, HEISS AA, BISHOP CD, HALL BK. Intracellular invasion of green algae in a salamander host[J]. Proceedings of the National Academy of Sciences of the United States of America, 2011, 108(16): 6497-6502.
    [16] DECELLE J, PROBERT I, BITTNER L, DESDEVISES Y, COLIN S, de VARGAS C, GALÍ M, SIMÓ R, NOT F. An original mode of symbiosis in open ocean plankton[J]. Proceedings of the National Academy of Sciences of the United States of America, 2012, 109(44): 18000-18005.
    [17] LEVY S, ELEK A, GRAU-BOVÉ X, MENÉNDEZ-BRAVO S, IGLESIAS M, TANAY A, MASS T, SEBÉ-PEDRÓS A. A stony coral cell atlas illuminates the molecular and cellular basis of coral symbiosis, calcification, and immunity[J]. Cell, 2021, 184(11): 2973-2987.e18.
    [18] QIU DJ, HUANG LM, HUANG H, YANG JH, LIN SJ. Two functionally distinct ciliates dwelling in Acropora corals in the South China Sea near Sanya, Hainan Province, China[J]. Applied and Environmental Microbiology, 2010, 76(16): 5639-5643.
    [19] SECORD D, AUGUSTINE L. Biogeography and microhabitat variation in temperate algal-invertebrate symbioses: zooxanthellae and zoochlorellae in two Pacific intertidal sea anemones, Anthopleura elegantissima and A. xanthogrammica[J]. Invertebrate Biology, 2000, 119(2): 139-146.
    [20] NAM SW, SHIN W, KANG MS, YIH W, PARK MG. Ultrastructure and molecular phylogeny of Mesodinium coatsi sp. nov., a benthic marine ciliate[J]. Journal of Eukaryotic Microbiology, 2015, 62(1): 102-120.
    [21] MOELLER HV, JOHNSON MD. Preferential plastid retention by the acquired phototroph Mesodinium chamaeleon[J]. Journal of Eukaryotic Microbiology, 2018, 65(2): 148-158.
    [22] KIM M, PARK MG. Unveiling the hidden genetic diversity and chloroplast type of marine benthic ciliate Mesodinium species[J]. Scientific Reports, 2019, 9: 14081.
    [23] SECKBACH J, GRUBE M. Symbioses and Stress: Joint Ventures in Biology[M]. Dordrecht: Springer Netherlands, 2010.
    [24] BELL EM, LAYBOURN-PARRY J. Mixotrophy in the antarctic phytoflagellate, pyramimonas gelidicola (Chlorophyta: Prasinophyceae)1[J]. Journal of Phycology, 2003, 39(4): 644-649.
    [25] ESTEBAN GF, FENCHEL T, FINLAY BJ. Mixotrophy in ciliates[J]. Protist, 2010, 161(5): 621-641.
    [26] JEONG HJ. Mixotrophy in red tide algae raphidophytes1[J]. Journal of Eukaryotic Microbiology, 2011, 58(3): 215-222.
    [27] STOECKER DK, JOHNSON MD, de VARGAS C, NOT F. Acquired phototrophy in aquatic protists[J]. Aquatic Microbial Ecology, 2009, 57: 279-310.
    [28] CARON DA, MICHAELS AF, SWANBERG NR, HOWSE FA. Primary productivity by symbiont-bearing planktonic sarcodines (Acantharia, Radiolaria, Foraminifera) in surface waters near Bermuda[J]. Journal of Plankton Research, 1995, 17(1): 103-129.
    [29] GUTIERREZ-RODRIGUEZ A, STUKEL MR, LOPES dos SANTOS A, BIARD T, SCHAREK R, VAULOT D, LANDRY MR, NOT F. High contribution of rhizaria (Radiolaria) to vertical export in the California current ecosystem revealed by DNA metabarcoding[J]. The ISME Journal, 2019, 13(4): 964-976.
    [30] DOLAN JR. Microzooplankton diversity: relationships of tintinnid ciliates with resources, competitors and predators from the Atlantic Coast of Morocco to the Eastern Mediterranean[J]. Deep Sea Research Part I: Oceanographic Research Papers, 2002, 49(7): 1217-1232.
    [31] URRUTXURTU I. Seasonal dynamics of ciliated protozoa and their potential food in an eutrophic estuary (Bay of Biscay)[J]. Estuarine, Coastal and Shelf Science, 2003, 57(5/6): 1169-1182.
    [32] STABELL T, ANDERSEN T, KLAVENESS D. Ecological significance of endosymbionts in a mixotrophic ciliate-an experimental test of a simple model of growth coordination between host and symbiont[J]. Journal of Plankton Research, 2002, 24(9): 889-899.
    [33] JOHNSON MD. Acquired phototrophy in ciliates: a review of cellular interactions and structural Adaptations1[J]. Journal of Eukaryotic Microbiology, 2011, 58(3): 185-195.
    [34] MORDRET S, ROMAC S, HENRY N, COLIN S, CARMICHAEL M, BERNEY C, AUDIC S, RICHTER DJ, POCHON X, de VARGAS C, DECELLE J. The symbiotic life of Symbiodinium in the open ocean within a new species of calcifying ciliate (Tiarina sp.)[J]. The ISME Journal, 2016, 10(6): 1424-1436.
    [35] KODAMA Y, SUZUKI H, DOHRA H, SUGII M, KITAZUME T, YAMAGUCHI K, SHIGENOBU S, FUJISHIMA M. Comparison of gene expression of Paramecium bursaria with and without Chlorella variabilis symbionts[J]. BMC Genomics, 2014, 15(1): 183.
    [36] PRÖSCHOLD T, PITSCH G, DARIENKO T. Micractinium tetrahymenae (trebouxiophyceae, chlorophyta), a new endosymbiont isolated from ciliates[J]. Diversity, 2020, 12(5): 200.
    [37] NOT F, PROBERT I, GERIKAS RIBEIRO C, CRENN K, GUILLOU L, JEANTHON C, VAULOT D. Photosymbiosis in Marine Pelagic Environments[M]. The Marine Microbiome. Cham: Springer International Publishing, 2016: 305-332.
    [38] DZIALLAS C, ALLGAIER M, MONAGHAN MT, GROSSART HP. Act together-implications of symbioses in aquatic ciliates[J]. Frontiers in Microbiology, 2012, 3: 288.
    [39] LOWE CD, MINTER EJ, CAMERON DD, BROCKHURST MA. Shining a light on exploitative host control in a photosynthetic endosymbiosis[J]. Current Biology: CB, 2016, 26(2): 207-211.
    [40] HORAS EL, METZGER SM, PLATZER B, KELLY JB, BECKS L. Context-dependent costs and benefits of endosymbiotic interactions in a ciliate-algae system[J]. Environmental Microbiology, 2022, 24:5924-5935.
    [41] HINES HN. Molecular investigation of the ciliate Spirostomum semivirescens, with first transcriptome and new geographical records[J]. Protist, 2018, 169(6): 875-886.
    [42] KODAMA Y, MIYAZAKI S. Autolysis of Chlorella variabilis in starving Paramecium bursaria help the host cell survive against starvation stress[J]. Current Microbiology, 2021, 78(2): 558-565.
    [43] SOMMARUGA R. Mycosporine-like amino acids in the Zooxanthella-ciliate symbiosis Maristentor dinoferus[J]. Protist, 2006, 157(2): 185-191.
    [44] WILKERSON FP, GRUNSEICH G. Formation of blooms by the symbiotic ciliate Mesodinium rubrum: the significance of nitrogen uptake[J]. Journal of Plankton Research, 1990, 12(5): 973-989.
    [45] YAMADA T, ONIMATSU H, van ETTEN JL. Chlorella viruses[J]. Advances in Virus Research, 2006, 66: 293-336.
    [46] GARCIA-CUETOS L, MOESTRUP Ø, HANSEN PJ. Studies on the genus Mesodinium II. Ultrastructural and molecular investigations of five marine species help clarifying the taxonomy[J]. The Journal of Eukaryotic Microbiology, 2012, 59(4): 374-400.
    [47] Dierssen H, McManus GB, Chlus A, Qiu D, Gao BC, Lin S. Space station image captures a red tide ciliate bloom at high spectral and spatial resolution[J]. Proceedings of the National Academy of Sciences of the United States of America, 2015, 112(48): 14783-14787.
    [48] HERFORT L, PETERSON TD, McCUE LA, CRUMP BC, PRAHL FG, BAPTISTA AM, CAMPBELL V, WARNICK R, SELBY M, ROEGNER GC, ZUBER P. Myrionecta rubra population genetic diversity and its cryptophyte chloroplast specificity in recurrent red tides in the Columbia River Estuary[J]. Aquatic Microbial Ecology, 2011, 62(1): 85-97.
    [49] WILLIAMS JA. Blooms of Mesodinium rubrum in Southampton Water-do they shape mesozooplankton distribution?[J]. Journal of Plankton Research, 1996, 18(9): 1685-1697.
    [50] SIEGEL RW. Hereditary endosymbiosis in Paramecium bursaria[J]. Experimental Cell Research, 1960, 19(2): 239-252.
    [51] KARAKASHIAN SJ. Growth of Paramecium bursaria as influenced by the presence of algal symbionts[J]. Physiological Zoology, 1963, 36(1): 52-68.
    [52] WEIS D. Regulation of host and symbiont population size in Paramecium bursaria[J]. Experientia, 1969, 25(6): 664-666.
    [53] TAYLOR FJR, BLACKBOURN DJ, BLACKBOURN J. The red-water ciliate Mesodinium rubrum and its “incomplete symbionts”: a review including new ultrastructural observations[J]. Journal of the Fisheries Research Board of Canada, 1971, 28(3): 391-407.
    [54] QIU DJ, HUANG LM, LIN SJ. Cryptophyte farming by symbiotic ciliate host detected in situ[J]. Proceedings of the National Academy of Sciences of the United States of America, 2016, 113(43): 12208-12213.
    [55] BOMFORD R. Infection of Alga-free Paramecium bursaria with strains of Chlorella, Scenedesmus, and a yeast[J]. The Journal of Protozoology, 1965, 12(2): 221-224.
    [56] TAKEDA H. Species-specificity of Chlorella for establishment of symbiotic association with Paramecium bursaria-does infectivity depend upon sugar components of the cell wall?[J]. European Journal of Protistology, 1998, 34(2): 133-137.
    [57] LASEK-NESSELQUIST E, WISECAVER JH, HACKETT JD, JOHNSON MD. Insights into transcriptional changes that accompany organelle sequestration from the stolen nucleus of Mesodinium rubrum[J]. BMC Genomics, 2015, 16: 805.
    [58] KIM GH, HAN JH, KIM B, HAN JW, NAM SW, SHIN W, PARK JW, YIH W. Cryptophyte gene regulation in the kleptoplastidic, karyokleptic ciliate Mesodinium rubrum[J]. Harmful Algae, 2016, 52: 23-33.
    [59] REISSER W, RADUNZ A, WIESSNER W. Participation of algal surface structures in the cell recognition process during infection of aposymbiotic Paramecium bursaria with symbiotic chlorellae[J]. Cytobios, 1982, 33(129): 39-50.
    [60] NISHIHARA N, HORIIKE S, TAKAHASHI T, KOSAKA T, SHIGENAKA Y, HOSOYA H. Cloning and characterization of endosymbiotic algae isolated from Paramecium bursaria[J]. Protoplasma, 1998, 203(1): 91-99.
    [61] KODAMA Y, FUJISHIMA M. Infection of Paramecium bursaria by symbiotic Chlorella species[M]//Endosymbionts in Paramecium[J]. Berlin, Heidelberg: Springer Berlin Heidelberg, 2009: 31-55.
    [62] KODAMA Y, SUMITA H. The ciliate Paramecium bursaria allows budding of symbiotic Chlorella variabilis cells singly from the digestive vacuole membrane into the cytoplasm during algal reinfection[J]. Protoplasma, 2022, 259(1): 117-125.
    [63] GUSTAFSON DE, STOECKER DK, JOHNSON MD, van HEUKELEM WF, SNEIDER K. Cryptophyte algae are robbed of their organelles by the marine ciliate Mesodinium rubrum[J]. Nature, 2000, 405(6790): 1049-1052.
    [64] CHENG YH, LIU CF J, YU YH, JHOU YT, FUJISHIMA M, TSAI IJ, LEU JY. Genome plasticity in Paramecium bursaria revealed by population genomics[J]. BMC Biology, 2020, 18(1): 180.
    [65] POWERS PBA. Cyclotrichium meunieri sp. nov. (protozoa, ciliata); cause of red water in the gulf of maine[J]. The Biological Bulletin, 1932, 63(1): 74-80.
    [66] TAYLOR FJR, BLACKBOURN DJ, BLACKBOURN J. Ultrastructure of the chloroplasts and associated structures within the marine ciliate Mesodinium rubrum (lohmann)[J]. Nature, 1969, 224(5221): 819-821.
    [67] BLACKBOURN DJ, TAYLOR FJR, BLACKBOURN J. Foreign organelle retention by ciliates[J]. Journal of Eukaryotic Microbiology, 1973, 20(2): 286-288.
    [68] STOECKER DK, SILVER MW, MICHAELS AE, DAVIS LH. Obligate mixotrophy inLaboea strobila, a ciliate which retains chloroplasts[J]. Marine Biology, 1988, 99(3): 415-423.
    [69] STOECKER DK, SILVER MW. Replacement and aging of chloroplasts in Strombidium capitatum (Ciliophora: oligotrichida)[J].Marine Biology, 1990, 107(3): 491-502.
    [70] HIBBERD DJ. Observations on the ultrastructure of the cryptomonad endosymbiont of the red-water ciliate Mesodinium rubrum[J]. Journal of the Marine Biological Association of the United Kingdom, 1977, 57(1): 45-61.
    [71] OAKLEY BR, Taylor F. Evidence for a new type of endosymbiotic organization in a population of the ciliate Mesodinium rubrum from British Columbia[J]. Biosystems, 1978, 10(4): 361-369.
    [72] LINDHOLM T, Lindroos P, Mörk AC. Ultrastructure of the photosynthetic ciliate Mesodinium rubrum[J]. Biosystems, 1988, 21(2): 141-149.
    [73] JUEL HANSEN P, FENCHEL T. The bloom-forming ciliate Mesodinium rubrum harbours a single permanent endosymbiont[J]. Marine Biology Research, 2006, 2(3): 169-177.
    [74] KARAKASHIAN MW. Intracellular digestion and symbiosis in Paramecium bursaria[J]. Experimental Cell Research, 1973, 81(1): 111-119.
    [75] KARAKASHIAN SJ. Inhibition of lysosomal fusion with symbiont-containing vacuoles in Paramecium bursaria[J]. Experimental Cell Research, 1981, 131(2): 387-393.
    [76] WOOTTON EC, ZUBKOV MV, JONES DH, JONES RH, MARTEL CM, THORNTON CA, ROBERTS EC. Biochemical prey recognition by planktonic protozoa[J]. Environmental Microbiology, 2007, 9(1): 216-222.
    [77] SONG CH, MURATA K, SUZAKI T. Intracellular symbiosis of algae with possible involvement of mitochondrial dynamics[J]. Scientific Reports, 2017, 7: 1221.
    [78] KODAMA Y, FUJISHIMA M. Endosymbiotic Chlorella variabilis reduces mitochondrial number in the ciliate Paramecium bursaria[J]. Scientific Reports, 2022, 12: 8216.
    [79] LOBBAN C, SCHEFTER M, SIMPSON A, POCHON X, PAWLOWSKI J, FOISSNER W. Maristentordinoferus n. Gen, n. sp, a giant heterotrich ciliate (Spirotrichea: Heterotrichida) with zooxanthellae, from coral reefs on Guam, Mariana Islands[J]. Marine Biology, 2002, 140(2): 411-423.
    [80] HOSHINA R, HAYAKAWA MM, KOBAYASHI M, HIGUCHI R, SUZAKI T. Pediludiella daitoensis Gen. et sp. nov. (Scenedesmaceae, Chlorophyceae), a large coccoid green alga isolated from a Loxodes ciliate[J]. Scientific Reports, 2020, 10: 628.
    [81] IWAI S, FUJIWARA K, TAMURA T. Maintenance of algal endosymbionts in Paramecium bursaria: a simple model based on population dynamics[J]. Environmental Microbiology, 2016, 18(8): 2435-2445.
    [82] KADONO T, KAWANO T. Natural historical views on the controlled cell growth and oxidative stress responses in symbiotic associations between ciliated Protozoa and green algae in green paramecia - A mini review[J]. New Technologies & Medicine, 2007, 8(4): 439-445.
    [83] Cernichiari E, Muscatine L, Smith DC. Maltose excretion by the symbiotic algae of Hydra viridis[J]. Proceedings of the Royal Society of London Series B Biological Sciences, 1969, 173(1033): 557-576.
    [84] Douglas AE, Smith DC. The green hydra symbiosis. VIII. Mechanisms in symbiont regulation[J]. Proceedings of the Royal Society of London Series B Biological Sciences, 1984, 221(1224): 291-319.
    [85] McAULEY PJ, DORLING M, HODGE H. Effect of maltose release on uptake and assimilation of ammonium by symbiotic chlorella (chlorophyta)1[J]. Journal of Phycology, 1996, 32(5): 839-846.
    [86] JOHNSON MD, TENGS T, OLDACH D, STOECKER DK. Sequestration, performance, and functional control of cryptophyte plastids in the ciliate myrionecta rubra (Ciliophora)1[J]. Journal of Phycology, 2006, 42(6): 1235-1246.
    [87] JOHNSON MD, OLDACH D, DELWICHE CF, STOECKER DK. Retention of transcriptionally active cryptophyte nuclei by the ciliate Myrionecta rubra[J]. Nature, 2007, 445(7126): 426-428.
    [88] HANSEN PJ, MOLDRUP M, TARANGKOON W, GARCIA-CUETOS L, MOESTRUP. Direct evidence for symbiont sequestration in the marine red tide ciliate Mesodinium rubrum[J]. Aquatic Microbial Ecology, 2012, 66(1): 63-75.
    [89] HOSHINA R, Kusuoka Y. DNA analysis of algal endosymbionts of ciliates reveals the state of algal integration and the surprising specificity of the symbiosis[J]. Protist, 2016, 167(2): 174-184.
    [90] Qiu D, Lin L, Lin S. Reply to Johnson et al.: Functionally active cryptophyte cell membrane and cytoplasm indicate intact symbionts within Mesodinium[J]. Proceedings of the National Academy of Sciences of the United States of America, 2017, 114(7): E1043-E1044.
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ZHOU Qinglan, RAO Xiaozhen, QIU Dajun. The study of symbiosis and interactions between ciliates and algae: current status and future directions[J]. Microbiology China, 2023, 50(6): 2753-2764

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  • Received:September 19,2022
  • Adopted:November 26,2022
  • Online: June 05,2023
  • Published: June 25,2023
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