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Photobiological Aspects of the Mutualistic Association Between Paramecium bursaria and Chlorella

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Endosymbionts in Paramecium

Part of the book series: Microbiology Monographs ((MICROMONO,volume 12))

Abstract

The main benefit involved in the mutualistic relationship between Paramecium bursaria and Chlorella has been traditionally interpreted as an adaptation to the struggle against starvation and nutrient limitation. However, other benefits such as the minimization of mortality and protection against damage by sunlight have been proposed recently. Here, we explore the photobiological adaptations and responses of P. bursaria and its algal symbionts when exposed to photosynthetically active and ultraviolet radiation, as well as the role of (photo-)oxidative and antioxidative defenses in the symbiosis. We conclude that the benefits are multiple and should be considered as a whole when assessing the selective advantage of living in mutualistic symbiosis.

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References

  • Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373–399

    Article  PubMed  CAS  Google Scholar 

  • Asada K (1999) The water-water cycle in chloroplasts: scavenging of active oxygen and dissipation of excess photons. Annu Rev Plant Physiol Plant Mol Biol 50:601–639

    Article  PubMed  CAS  Google Scholar 

  • Aury J-M, Jaillion O, Duret L et al (2006) Global trends of whole-genome duplications revealed by the ciliate Paramecium tetraurelia. Nature 444:171–178

    Article  PubMed  CAS  Google Scholar 

  • Berger J (1980) Feeding behavior of Didinium nasutum on Paramecium bursaria with normal or apochlorotic zoochlorellae. J Gen Microbiol 118:397–404

    Google Scholar 

  • Berk SG, Parks LH, Ting RS (1991) Photoadaptation alters the ingestion rate of Paramecium bursaria, a mixotrophic ciliate. Appl Environ Microbiol 57:2312–2316

    PubMed  CAS  Google Scholar 

  • Berninger U-G, Finlay BJ, Canter HM (1986) The spatial distribution and ecology of zoochlorellae-bearing ciliates in a productive pond. J Protozool 33:557–563

    Google Scholar 

  • Cockell CS (1998) Ultraviolet radiation, evolution and the Ï€-electron system. Biol J Linn Soc 62:449–457

    Article  Google Scholar 

  • Dionisio-Sese L, Maruyama T, Miyachi S (2001) Photosynthesis of Prochloron as affected by environmental factors. Mar Biotechnol 3:74–79

    Article  PubMed  CAS  Google Scholar 

  • Doebeli M, Knowlton N (1998) The evolution of interspecific mutualisms. Proc Natl Acad Sci USA 95:8676–8680

    Article  PubMed  CAS  Google Scholar 

  • Dolan J (1992) Mixotrophy in ciliates: a review of Chlorella symbiosis and chloroplast retention. Mar Microb Food Webs 6:115–132

    Google Scholar 

  • Dolan J, Pérez MT (2000) Costs, benefits and characteristics of mixotrophy in marine oligotrichs. Freshwat Biol 45:227–238

    Article  Google Scholar 

  • Dunlap WC, Shick JM (1998) Ultraviolet radiation-absorbing mycosporine-like amino acids in coral reef organisms: a biochemical and environmental perspective. J Phycol 34:418–430

    Article  Google Scholar 

  • Dunlap WC, Shick JM, Yamamoto Y (2000) UV protection in marine organisms. I. Sunscreens, oxidative stress and antioxidants. In: Yoshikawa T, Toyokuni S, Yamamoto M, Naito Y (eds) Free radicals in chemistry, biology and medicine. OICA International, London, pp 200–214

    Google Scholar 

  • Engelmann TW (1882) Ueber Licht- und Farbenperception niederster Organismen. Arch Ges Physiol 29:387–400

    Article  Google Scholar 

  • Finlay BJ, Maberly SC, Esteban GF (1996) Spectacular abundance of ciliates in anoxic pond water: contribution of symbiont photosynthesis to host respiratory oxygen requirements. FEMS Microbiol Ecol 20:229–235

    Article  CAS  Google Scholar 

  • Fridovich I (1998) Oxygen toxicity: a radical explanation. J Exp Biol 201:1203–1209

    PubMed  CAS  Google Scholar 

  • Garcia-Pichel F (1994) A model for internal self-shading in planktonic organisms and its implications for the usefulness of ultraviolet sunscreens. Limnol Oceanogr 39:1704–1717

    Article  Google Scholar 

  • Geraschenko BI, Nishihara N, Ohara T, Tosuji H, Kosaka T, Hosoya H (2000) Flow cytometry as a strategy to study the endosymbiosis of algae in Paramecium bursaria. Cytometry 41:209–215

    Article  Google Scholar 

  • Giese AC (1945) The ultraviolet action spectrum for retardation of Paramecium. J Cell Comp Physiol 26:47–55

    Article  Google Scholar 

  • Giese AC (1968) Ultraviolet action spectra in perspective: with special reference to mutation. Photochem Photobiol 8:527–546

    Article  PubMed  CAS  Google Scholar 

  • Görtz H-D (1982) Infection of Paramecium bursaria with bacteria and yeasts. J Cell Sci 58:445–453

    PubMed  Google Scholar 

  • Görtz H-D (1988) Endocytobiosis. In: Görtz H-D (ed) Paramecium. Springer, Berlin, pp 393–405

    Google Scholar 

  • Gu F, Chen L, Ni B, Zhang, X (2002) A comparative study on the electron microscopic enzymo-cytochemistry of Paramecium bursaria from light and dark cultures. Eur J Protistol 38:267–278

    Article  Google Scholar 

  • Halliwell B, Gutteridge JMC (1999) Free radicals in biology and medicine. Oxford University Press, New York

    Google Scholar 

  • Herre EA, Knowlton N, Mueller UG, Rehner SA (1999) The evolution of mutualisms: exploring the paths between conflict and cooperation. Trends Ecol Evol 14:49–53

    Article  PubMed  Google Scholar 

  • Hörtnagl P, Sommaruga R (2007) Photo-oxidative stress in symbiotic and aposymbiotic strains of the ciliate Paramecium bursaria. Photochem Photobiol Sci 6:842–847

    Article  PubMed  Google Scholar 

  • Iwatsuki K, Naitoh Y (1981) The role of symbiotic Chlorella in photoresponses of Paramecium bursaria. Proc Jpn Acad Ser B 57:318–323

    Article  Google Scholar 

  • Jones RI (1994) Mixotrophy in planktonic protists as a spectrum of nutritional strategies. Mar Microb Food Webs 8:87–96

    Google Scholar 

  • Kang M, Moroni A, Gazzarrini S, Van Etten JL (2003) Are chlorella viruses a rich source of ion channel genes? FEBS Lett 552:2–6

    Article  PubMed  CAS  Google Scholar 

  • Karakashian SJ, Karakashian MW, Rudzinska MA (1968) Electron microscopic observations on the symbiosis of Paramecium bursaria and its intracellular algae. J Protozool 15:113–128

    Google Scholar 

  • Karentz D, McEuen FS, Land MC, Dunlap WC (1991) Survey of mycosporine-like amino acid compounds in Antarctic marine organisms: potential protection from ultraviolet exposure. Mar Biol 108:157–166

    Article  CAS  Google Scholar 

  • Kawano T, Kadono T, Kosaka T, Hosoya H (2004) Green paramecia as an evolutionary winner of oxidative symbiosis: a hypothesis and supportive data. Z Naturforsch 59:538–542

    CAS  Google Scholar 

  • Kieber DJ, Peake BM, Scully NS (2003) Reactive oxygen species in aquatic ecosystems. In: Helbling EW, Zagarese H (eds) UV effects in aquatic organisms and ecosystems. Royal Society of Chemistry, Cambridge, pp 251–288

    Google Scholar 

  • Landis WG (1988) Ecology. In: Görtz H-D (ed) Paramecium. Springer, Berlin, pp 419–436

    Google Scholar 

  • Lesser MP (2006) Oxidative stress in marine environment: biochemistry and physiological ecology. Annu Rev Physiol 68:253–278

    Article  PubMed  CAS  Google Scholar 

  • Li L, Song W (2006) Phylogenetic positions of two cyrtophorid ciliates, Dysteria procera and Hartmannula derouxi (Ciliophora: Phyllopharyngea: Dysteriida) inferred from the complete small subunit ribosomal RNA gene sequences. Acta Protozool 45:265–270

    CAS  Google Scholar 

  • Lobban CS, Schefter M, Simpson AGB, Pochon X, Pawlowski J, Foissner W (2002) Maristentor dinoferus n. gen., n. sp., a giant heterotrich ciliate (Spirotrichea: Heterotrichida) with zooxanthellae, from coral reefs on Guam, Mariana Islands. Mar Biol 140:411–423

    Article  Google Scholar 

  • Lobban CS, Hallam SJ, Mukherjee P, Petrich JW (2007) Photophysics and multifunctionality of hypericin-like pigments in heterotrich ciliates: a phylogenetic perspective. Photochem Photobiol 83:1074–1094

    Article  PubMed  CAS  Google Scholar 

  • Machemer H (1974) Frequency and directional responses of cilia to membrane potential changes in Paramecium. J Comp Physiol 92:293–316

    Article  Google Scholar 

  • Malanga G, Puntarulo S (1995) Oxidative stress and antioxidant content in Chlorella vulgaris after exposure to ultraviolet-B radiation. Physiol Plant 94:672–679

    Article  CAS  Google Scholar 

  • Martin-Webb EB (1999) The effect of solar ultraviolet radiation on marine planktonic ciliates survival and the penetration of ultraviolet irradiance on Georges Bank, Ph. D. thesis, University of Rhode Island, Kingston

    Google Scholar 

  • Matsuoka K, Nakaoka Y (1988) Photoreceptor potential causing phototaxis of Paramecium bursaria. J Exp Biol 137:477–485

    Google Scholar 

  • McTavish C, Sommerville J (1980) Macronuclear DNA organization and transcription in Paramecium primaurelia. Chromosoma 78:147–164

    Article  PubMed  CAS  Google Scholar 

  • Meier R, Wiessner W (1988) Infection of algae-free Paramecium bursaria with symbiotic Chlorella sp., isolated from green paramecia, I: effect of incubation period. Eur J Protistol 24:69–74

    Google Scholar 

  • Meier R, Wiessner W (1989) Infection of algae-free Paramecium bursaria with symbiotic Chlorella sp., isolated from green paramecia, II: a timed study. J Cell Sci 93:571–579

    Google Scholar 

  • Miyake AF, Buonanno P, Saltalamacchia P, Masaki ME, Iio H (2003) Chemical defense by means of extrusive cortical granules in the heterotrich ciliate Climacostomum virens. Eur J Protistol 39:25–36

    Article  Google Scholar 

  • Modenutti BE, Balseiro EG, Moeller R (1998) Vertical distribution and resistance to ultraviolet radiation of a planktonic ciliate, Stentor araucanus. Verh Int Ver Limnol 26:1636–1640

    Google Scholar 

  • Muscatine L, Karakashian SJ, Karakashian MW (1967) Soluble extracellular products of algae symbiotic with a ciliate, a sponge and a mutant Hydra. Comp Biochem Physiol 20:1–12

    Article  CAS  Google Scholar 

  • Nakaoka Y, Kinugawa K, Kurotani T (1987) Ca2+-dependent photoreceptor potential in Paramecium bursaria. J Exp Biol 131:107–115

    CAS  Google Scholar 

  • Nakaoka Y, Tokioka R, Shinozawa T, Fujita J, Usukura J (1991) Photoreception of Paramecium cilia: localization of photosensitivity and binding with anti-frog-rhodopsin lgG. J Cell Sci 99:67–72

    PubMed  CAS  Google Scholar 

  • Niess D, Reisser W, Wiessner W (1981)The role of endosymbiotic algae in photoaccumulation of green Paramecium bursaria. Planta 152:268–271

    Article  Google Scholar 

  • Niess D, Reisser W, Wiessner W (1982) Photobehaviour of Paramecium bursaria infected with different symbiotic and aposymbiotic species of Chlorella. Planta 156:475–480

    Article  Google Scholar 

  • Nishihara N, Horjike S, Oka Y, Takahashi T, Kosaka T, Hosoya H (1999) Microtubule-dependent movement of symbiotic algae and granules in Paramecium bursaria. Cell Motil Cytoskeleton 43:85–98

    Article  PubMed  CAS  Google Scholar 

  • Norris, RD (1996) Symbiosis as an evolutionary innovation in the radiation of Paleocene planktic foraminifera. Paleobiology 22:461–480

    Google Scholar 

  • Pado R (1972) Spectral activity of light and phototaxis in Paramecium bursaria. Acta Protozool 11:387–393

    Google Scholar 

  • Pérez MT, Dolan JR, Fukai E (1997) Planktonic oligotrich ciliates in the NW Mediterranean growth rates and consumption by copepods. Mar Ecol Prog Ser 155:89–101

    Article  Google Scholar 

  • Pringsheim EG (1928) Physiologische Untersuchungen an Paramecium bursaria. Ein Beitrag zur Symbioseforschung. Arch Protistenkd 64:289–418

    Google Scholar 

  • Queimaliños CP, Modenutti BE, Balseiro EG (1999) Symbiotic association of the ciliate Ophrydium naumanni with Chlorella causing a deep chlorophyll a maximum in an oligotrophic South Andes lake. J Plankton Res 21:67–178

    Article  Google Scholar 

  • Reisser W (1980) The regulation of the algal population size in Paramecium bursaria. In: Schenk HEA, Schwemmler W (eds) Endocytobiology, vol 2. de Gruyter, Berlin, pp 97–104

    Google Scholar 

  • Reisser W, Häder D-P (1984) Role of endosymbiotic algae in photokinesis and photophobic responses of ciliates. Photochem Photobiol 39:673–678

    Article  Google Scholar 

  • Reisser W, Fisher-Defoy D, Staudinger J, Schelling N, Hausmann K (1984) The endosymbiotic unit of Climacostomum virens and Chlorella sp. 1: morphological and physiological studies of the algal partner and its localization in the host cell. Protoplasma 119:93–99

    Google Scholar 

  • Reyes-Prieto A, Moustafa A, Bhattacharya D (2008) Multiple genes of apparent algal origin suggest ciliates may once have been photosynthetic. Curr Biol 18:956–962

    Article  PubMed  CAS  Google Scholar 

  • Saji M, Oosawa F (1974) Mechanism of photoaccumulation in Paramecium bursaria. J Protozool 21:556–561

    PubMed  CAS  Google Scholar 

  • Schlegel M, Elwood HJ, Sogin ML (1991) Molecular evolution in hypotrichous ciliates: sequence of the small subunit RNA genes from Onychodromus quadricornutus and Oxytricha granulifera (Oxytrichidae, Hypotrichida, Ciliophora). J Mol Evol 32:64–69

    Article  PubMed  CAS  Google Scholar 

  • Shick JM, Dunlap WC (2002) Mycosporine-like amino acids and related gadusols: biosynthesis, accumulation, and UV-protective functions in aquatic organisms. Annu Rev Physiol 64:223–262

    Article  PubMed  CAS  Google Scholar 

  • Shick JM, Lesser MP, Jokiel PJ (1996) Effects of ultraviolet radiation on corals and other coral reef organisms. Global Change Biol 2:527–545

    Article  Google Scholar 

  • Shick JM, Romaine-Lioud S, Ferrier-Pages C, Gattuso J-P (1999) Ultraviolet-B radiation stimulates shikimate pathway-dependent accumulation of mycosporine-like amino acids in the coral Stylophora pistillata despite decreases in its population of symbiotic dinoflagellates. Limnol Oceanogr 44:1667–1682

    Article  CAS  Google Scholar 

  • Sommaruga R, Garcia-Pichel F (1999) UV-absorbing mycosporine-like compounds in planktonic and benthic organisms from a high-mountain lake. Arch Hydrobiol 144:255–269

    CAS  Google Scholar 

  • Sommaruga R, Whitehead K, Shick JM, Lobban CS (2006) Mycosporine-like amino acids in the zooxanthella-ciliate symbiosis Maristentor dinoferus. Protist 157:185–191

    Article  PubMed  CAS  Google Scholar 

  • Sonntag B, Summerer M, Sommaruga R (2007) Sources of mycosporine-like amino acids in planktonic Chlorella-bearing ciliates (Ciliophora). Freshwat Biol 52:1476–1485

    Article  CAS  Google Scholar 

  • Stabell T, Andersen T, Klaveness D (2002) Ecological significance of endosymbionts in a mixotrophic ciliate – an experimental test of a simple model of growth coordination between host and symbiont. J Plankton Res 24:889–899

    Article  Google Scholar 

  • Stoecker DK (1998) Conceptual models of mixotrophy in planktonic protists and some ecological and evolutionary implications. Eur J Protistol 34:281–290

    Google Scholar 

  • Summerer M, Sonntag B, Sommaruga R (2007) An experimental test of the symbiosis specificity between the ciliate Paramecium bursaria and strains of the unicellular green alga Chlorella. Environ Microbiol 9:2117–2122

    Article  PubMed  CAS  Google Scholar 

  • Summerer M, Sonntag B, Sommaruga R (2008) Ciliate-symbiont specificity of freshwater endosymbiotic Chlorella (Trebouxiophyceae, Chlorophyta). J Phycol 44:77–84

    Article  CAS  Google Scholar 

  • Summerer M, Sonntag B, Hörtnagl P, Sommaruga R (2009) Symbiotic ciliates receive protection against UV damage from their algae: A test with Paramecium bursaria and Chlorella. Protist doi:10.1016/j.protis.2008.11.005

    Google Scholar 

  • Tartarotti B, Baffico G, Temporetti P, Zagarese HE (2004) Mycosporine-like amino acids in planktonic organisms living under different UV exposure conditions in Patagonian lakes. J Plankton Res 26:753–762

    Article  PubMed  CAS  Google Scholar 

  • Tokioka R, Matsuoka K, Nakaoka Y, Kito Y (1991) Extraction of retinal from Paramecium bursaria. Photochem Photobiol 53:149–151

    Article  CAS  Google Scholar 

  • Tonooka Y, Watanabe T (2002) A natural strain of Paramecium bursaria lacking symbiotic algae. Eur J Protistol 38:55–58

    Article  Google Scholar 

  • Tonooka Y, Mizukami Y, Fujishima M (2008) One-base excess adaptor ligation method for walking uncloned genomic DNA. Appl Microbiol Biotechnol 78:173–180

    Article  PubMed  CAS  Google Scholar 

  • Van Etten JL (2003) Unusual life style of giant chlorella viruses. Annu Rev Genet 37:153–195

    Article  PubMed  CAS  Google Scholar 

  • Woelfl S, Geller W (2002) Chlorella-bearing ciliates dominate in an oligotrophic North Patagonian Lake (Lake Pirehueico, Chile): abundance, biomass and symbiotic photosynthesis. Freshwat Biol 47:231–242

    Article  Google Scholar 

  • Zigman S, Reddan J, Schultz JB, McDaniel T (1996) Structural and functional changes in catalase induced by near-UV radiation. Photochem Photobiol 63:818–824

    Article  PubMed  CAS  Google Scholar 

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Acknowledgements

We thank M.T. Pérez and M. Summerer for critical reading of the original manuscript. We are also indebted to M. Summerer for providing Figs. 1–3, P. Hörtnagl for providing Fig. 5, and T. Kawano for providing Fig. 4 in color. This work was supported by the Austrian Science Fund (project FWF 16559) granted to R.S.

End Note The original light intensity in the paper by Kawano et al. (2004) was given in lux, which can only be converted to micromole photons per square meter per second when the wavelength dependency is considered. Here a factor of 0.0165 was applied to facilitate comparison with other studies.

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  1. Laboratory of Aquatic Photobiology and Plankton Ecology, Institute of Ecology, University of Innsbruck, Technikerstr. 25, 6020, Innsbruck, Austria

    Ruben Sommaruga & Bettina Sonntag

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  1. Ruben Sommaruga
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  2. Bettina Sonntag
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Correspondence to Bettina Sonntag .

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  1. Graduate School of Science and Eng., Dept. of Environmental Sci. and Eng., Yamaguchi University, Yoshida 1677-1, Yamaguchi, 753-8512, Japan

    Masahiro Fujishima

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Sommaruga, R., Sonntag, B. (2009). Photobiological Aspects of the Mutualistic Association Between Paramecium bursaria and Chlorella . In: Fujishima, M. (eds) Endosymbionts in Paramecium. Microbiology Monographs, vol 12. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-540-92677-1_5

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