Abstract
Imagine that in 1678 you are Christiaan Huygens or Antonie van Leeuwenhoek seeing paramecia swim gracefully across the field of view of your new microscope. These unicellular, free-living, and swimming cells might have remained a curiosity if not for the ability of H.S. Jennings (Behavior of the lower organisms. Indiana University Press, Bloomington, 1906) and T.M. Sonneborn (Proc Natl Acad Sci USA 23:378–385, 1937) to recognize them for their behavior and genetics, both Mendelian and non-Mendelian. Following many years of painstaking work by Sonneborn and other researchers, Paramecium now serves as a modern model organism that has made specific contributions to cell and molecular biology and development. We will review the continuing usefulness and contributions of Paramecium species in this chapter.
Even without a microscope, Paramecium species is visible to the naked eye because of their size (50–300 μ long). Paramecia are holotrichous ciliates, that is, unicellular organisms in the phylum Ciliophora that are covered with cilia. It was the beating of these cilia that propelled them across the slides of the first microscopes and continue to fascinate us today. Over time, Paramecium became a favorite model organism for a large variety of studies. Denis Lyn has called Paramecium the “white rat” of the Ciliophora for their manipulability and amenity to research. We will touch upon the use of Paramecium species to examine swimming behavior, ciliary structure and function, ion channel function, basal body duplication and patterning, non-Mendelian cortical inheritance, programmed DNA rearrangements, regulated secretion and exocytosis, and cell trafficking. In particular, we will focus on the use of P. tetraurelia and P. caudatum.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Allen RD (1971) Fine structure of membranous and microfibrillar systems in the cortex of Paramecium caudatum. J Cell Biol 49:1–20
Allen S, Nowacki M (2017) Necessity is the mother of invention: ciliates, transposons, and transgenerational inheritance. Trends Genet 33:197–207
Arnaiz O, Cain S, Cohen J, Sperling L (2007) ParameciumDB: a community resource that integrates the Paramecium tetraurelia genome sequence with genetic data. Nucleic Acids Res 35:D439–D444
Arnaiz O, Malinowska A, Klotz C, Sperling L, Dadlez M, Cohen J (2009) Cildb: a knowledgebase for centrosomes and cilia. Database (Oxford) 2009:bap022
Arnaiz O, Mathy N, Baudry D, Malinsky S, Aury J, Denby W, Garnier O, Labadie K, Lauderdale B, LeMouel A, Marmington A, Nowacki M, Poulain J, Prajer M, Wincker P, Meyer E, Duharcourt S, Duret L, Betermier M, Sperling L (2012) The Paramecium germline genome provides a niche for intragenic parasitic DNA: evolutionary dynamics of internal eliminated sequences. PLoS Genet 8:e1002984
Arnaiz O, Van Dijk E, Bétermier M, Lhuillier-Akakpo M, de Vanssay A, Duharcourt S, Sallet E, Gouzy J, Sperling L (2017) Improved methods and resources for Paramecium genomics: transcription units, gene annotation and gene expression. BMC Genomics 18:483
Aubusson-Fleury A, Lemullois M, de Loubresse N-G, Laligné C, Cohen J, Rosnet O, Jerka-Dziadosz M, Beisson J, Koll F (2012) The conserved centrosomal protein FOR20 is required for assembly of the transition zone and basal body docking at the cell surface. J Cell Sci 125:4395–4404
Aubusson-Fleury A, Lemullois M, Bengueddach H, Abdallah S, Shi L, Cohen J, Tassin AM, Koll F (2015) Transition zone: the sequential assembly of its components parallels its dual role in basal body anchoring and ciliary function. Cilia 4(Suppl 1):P26
Aury JM, Jaillon O, Duret L, Noel B, Jubin C, Porcel BM, Segurens B, Daubin V, Anthouard V, Aiach N, Arnaiz O, Billaut A, Beisson J, Blanc I, Bouhouche Camara F, Duharcourt S, Guigo R, Gogendeau D, Katinka M, Keller AM, Kissmehl R, Klotz C, Koll F, LeMouel A, Lepere G, Malinsky S, Nowacki M, Nowak JK, Plattner H, Poulain J, Ruiz F, Serrano V, Zagulski M, Dessen P, Betermier M, Weissenbach J, Scarpelli C, Schachter V, Sperling L, Meyer E, Cohen J, Wincker P (2006) Global trends of whole-genome duplications revealed by the ciliate Paramecium tetraurelia. Nature 444:171–178
Beisson J, Sonneborn TM (1965) Cytoplasmic inheritance of the organization of the cell cortex in Paramecium aurelia. Proc Natl Acad Sci USA 53:275–282
Beisson J, Clerot JC, Fleuro-Aubusson A, Garreau de Loubresse N, Ruiz F, Klotz C (2001) Basal body-associated nucleation center for the centrin-based cortical cytoskeletal network in Paramecium. Protist 152:339–354
Beisson J, Betermier M, Bre M-H, Cohen J, Duharcourt S, Duret L, Kung C, Malinsky S, Meyer E, Preer J, Sperling L (2010) Paramecium tetraurelia: renaissance of an early unicellular model. In: Crotty D, Grann A (eds) Emerging model organisms, vol 2. Cold Spring Harbor Press, New York, pp 1–30
Bischerour J, Bhullar S, Wilkes C, Regnier V, Mathy N, Dubois E, Singh A, Swart E, Arnaiz O, Sperling L, Nowacki M, Betermier M (2018) Six domesticated PiggyBac transposases together carry out programmed DNA elimination in Paramecium. eLife 7:e37927
Brehm P, Eckert R (1978) An electrophysiological study of the regulation of ciliary beating fre quency in Paramecium. J Physiol 283:557–568
Buonanno F, Harumoto T, Ortenzi C (2013) The defensive function of trichocysts in Paramecium tetraurelia against metazoan predators compared with the chemical defense of two species of toxin-containing ciliates. Zool Sci 30:255–261
Capdeville Y, Benwakrim A (1996) The major ciliary membrane proteins in Paramecium primaurelia are all glycosylphosphatidylinositol-anchored proteins. Eur J Cell Biol 70:339–346
Chalker DL, Stover NA (2007) Genome evolution: a double take for Paramecium. Curr Biol 17:R97–R99
Chang S-Y, Van Houten JL, Robles LJ, Lui SS, Kung C (1976) An extensive behavioural and genetic analysis of the Pawn mutants in Paramecium aurelia. Gene Res 23:165–173
Cohen J, Beisson J (1980) Genetic analysis of the relationships between the cell surface and the nuclei in Paramecium tetraurelia. Genetics 95:797–818
Dunlap K (1977) Localization of calcium channels in Paramecium caudatum. J Physiol 271:119–133
Eckert R (1972) Bioelectric control of ciliary activity. Science 176:473–481
Eckert R, Naitoh Y (1972) Bioelectric control of locomotion in the ciliates. J Protozool 19:237–243
Galvani A, Sperling L (2002) RNA interference by feeding in Paramecium. Trends Genet 18:11–12
Görtz H-D (1988) Endocytobiosis. In: Görtz H-D (ed) Paramecium. Springer, Berlin
Haga N, Saimi Y, Takahashi M, Kung C (1983) Intra- and interspecific complementation of membrane-inexcitable mutants of Paramecium. J Cell Biol 97:378–382
Hamasaki T, Barkalow K, Richmond J, Satir P (1991) cAMP-stimulated phosphorylation of an axonemal polypeptide that copurifies with the 22S dynein arm regulates microtubule translocation velocity and swimming speed in Paramecium. Proc Natl Acad Sci USA 88:7918–7922
Hausmann K, Allen RD (2010) Electron microscopy of Paramecium (Ciliata). In: Müller-Reichert T (ed) Methods in cell biology, vol 96. Academic Press, New York, pp 143–173
Haynes WJ, Vaillant B, Preston RR, Saimi Y, Kung C (1998) The cloning by complementation of the pawn-A gene in Paramecium. Genetics 149:947–957
Haynes WJ, Ling KY, Preston RR, Saimi Y, Kung C (2000) The cloning and molecular analysis of pawn-B in Paramecium tetraurelia. Genetics 155:1105–1117
Haynes WJ, Kung C, Saimi Y, Preston RR (2002) An exchanger-like protein underlies the large Mg2+ current in Paramecium. Proc Natl Acad Sci USA 99:15717–15722
Husser M, Hardt M, Blanchard MP, Hentschel J, Klauke N, Plattner H (2004) One-way calcium spill-over during signal transduction in Paramecium cells: from cortex into cilia but not the reverse. Cell Calcium 36:349–358
Iftode F, Cohen J, Ruiz F, Rueda AT, Chen-Shan L, Adoutte A (1989) Development of surface pattern during division in Paramecium. I. Mapping of duplication and reorganization of cortical cytoskeletal structures in the wild type. Development 105:191–211
Jennings H (1906) Behavior of the lower organisms. Indiana University Press, Bloomington
Kissmehl R, Sehring I, Wagner E, Plattner H (2004) Immunolocalization of actin in Paramecium cells. J Histochem Cytochem 52:1543–1559
Kissmehl R, Schilde C, Wassmer T, Danzer C, Nuehse K, Lutter K, Plattner H (2007) Molecular identification of 26 syntaxin genes and their assignment to the different trafficking pathways in Paramecium. Traffic 8(5):523–542
Klauke N, Blanchard MP, Plattner H (2000) Polyamine triggering of exocytosis in Paramecium involves and extracellular Ca2+/(polyvalent)cation-sensing receptor, subplasmalemmal Ca-store mobilization and store-operated Ca2+-influx via unspecific cation channels. J Membr Biol 174:141–156
Kung C (1971) Genic mutants with altered system of excitation in Paramecium aurelia. II. Mutagenesis, screening and genetic analysis of the mutants. Genetics 69:29–45
Kung C, Chang S, Satow Y, Van Houten J, Hansma H (1975) Genetic dissection of behavior in Paramecium. Science 188:898–904
Kung C, Preston RR, Maley ME, Ling KY, Kanabrocki JA, Seavey BR, Saimi Y (1992) In vivo Paramecium mutants show that calmodulin orchestrates membrane responses to stimuli. Cell Calcium 13:413–425
Kutomi O, Hori M, Ishida M, Tominaga T, Kamachi H, Koll F, Cohen J, Yamada N, Noguchi M (2012) Outer dynein arm light chain 1 is essential for controlling the ciliary response to cyclic AMP in Paramecium tetraurelia. Eukaryot Cell 11:645–653
Le Mouel A, Butler A, Caron F, Meyer E (2003) Developmentally regulated chromosome fragmentation linked to imprecise elimination of repeated sequences in paramecia. Eukaryot Cell 2:1076–1090
Lodh S, Yano J, Valentine MS, Van Houten JL (2016) Voltage-gated calcium channels of Paramecium. J Exp Biol 219:3028–3038
Louka P, Vasudevan KK, Guha M, Joachimiak E, Wloga D, Tomasi RFX, Baroud CN, Dupuis-Williams P, Galati DF, Pearson CG, Rice LM, Moresco JJ, Yates JR, Jiang YY, Lechtreck K, Dentler W, Gaertig J (2018) Proteins that control the geometry of microtubules at the ends of cilia. J Cell Biol 217:4298–4313
Machemer H (1988a) Electrophysiology. In: Gortz H-D (ed) Paramecium. Springer, Berlin, pp 186–215
Machemer H (1988b) Motor control of cilia. In: Görtz H-D (ed) Paramecium. Springer, Berlin, pp 216–235
Machemer H, Ogura A (1979) Ionic conductances of membranes in ciliated and deciliated Paramecium. J Physiol 296:49–60
Marker S, Carradec Q, Tanty V, Arnaiz O, Meyer E (2014) A forward genetic screen reveals essential and non-essential RNAi factors in Paramecium tetraurelia. Nucleic Acids Res 23:1–13
Matsuda A, Saim Y, Takahashi M (2000) An unusual complementation in non-excitable mutants in Paramecium. Genet Res 76:125–133
Miyake A, Haroumoto T (1996) Defensive function of trichocysts in Paramecium against the predatory ciliate Monadenium balbiani. Eur J Protistol 32:128–133
Nabi MA (2018) Multiple functions of the striated rootlet proteins of the Paramecium basal body. PhD thesis, University of Vermont
Noguchi M, Kurahashi S, Kamachi H, Inoue H (2004) Control of the ciliary beat by cyclic nucleo tides in intact cortical sheets from Paramecium. Zool Sci 21:1167–1175
Oami K, Takahashi M (2003) K+-induced Ca2+ conductance responsible for the prolonged backward swimming in K+-agitated mutant of Paramecium caudatum. J Membr Biol 195:85–92
Orias E, Singh DP, Meyer E (2017) Genetics and epigenetics of mating type determination in Paramecium and Tetrahymena. Annu Rev Microbiol 71:133–156
Paquette CA, Rakochy V, Bush A, Van Houten JL (2001) Glycophosphatidylinositol-anchored proteins in Paramecium tetraurelia: possible role in chemoresponse. J Exp Biol 204:2899–2910
Plattner H (2010) Membrane trafficking in protozoa: SNARE proteins, H+ -ATPase, actin, and other key players in ciliates. Int Rev Cell Mol Biol 280:79–184
Plattner H (2013) Calcium regulation in the protozoan model, Paramecium tetraurelia. J Eukaryot Microbiol 61:95–114
Plattner H (2016) Trichocysts—Paramecium’s projectile-like secretory organelles. J Eukaryot Microbiol 64:106–133
Plattner H, Klauke N (2001) Calcium in ciliated Protozoa: sources, regulation and calcium-regulated cell functions. Int Rev Cytol 201:115–208
Preston RR (1990) Genetic dissection of Ca2+dependent ion channel function in Paramecium. BioEssays 12:273–228
Preston RR, Kung C (1994) Isolation and characterization of Paramecium mutants defective in their response to magnesium. Genetics 137:759–769
Preston RR, Martinac Y, SC KC (1992) Genetic analysis of ion channels of prokaryotes and lower eukaryotes. Curr Opin Genet Dev 2:780–784
Ruiz F, Vayssie L, Klotz C, Sperling L, Madeddu L (1998) Homology-dependent gene silencing in Paramecium. Mol Biol Cell 9:931–943
Satir P, Heuser T, Sale W (2014) A structural basis for how motile cilia beat. Bioscience 64:1073–1083
Satow Y, Kung C (1980a) Ca-induced K+-outward current in Paramecium tetraurelia. J Exp Biol 88:293–303
Satow Y, Kung C (1980b) Membrane currents of Pawn mutants of the pwA group in Paramecium tetraurelia. J Exp Biol 84:57–71
Schilde C, Wassmer T, Mansfeld J, Plattner H, KissmehI R (2006) A multigene family encoding R-SNAREs in the ciliate Paramecium tetraurelia. Traffic 7:440–455
Schilde C, Schönemann B, Sehring IM, Plattner H (2010) Distinct subcellular localization of a group of synaptobrevin-like SNAREs in Paramecium tetraurelia and effects of silencing SNARE-specific chaperone NSF. Eukaryot Cell 9:288–305
Schultz JE, Klumpp S, Benz R, Schurhoff-Goeters WJ, Schmid A (1992) Regulation of adenylyl cyclase from Paramecium by an intrinsic potassium conductance. Science 255:600–603
Sehring IM, Reiner C, Mansfeld J, Plattner H, Kissmehl R (2007) A broad spectrum of actin paralogs in Paramecium tetraurelia cells display differential localization and function. J Cell Sci 120:177–190
Singh D, Saudemont B, Guglielmi G, Arnaiz O, Goût JF, Prajer M, Potekhin A, Przybòs E, Aubusson-Fleury A, Bhullar S, Bouhouche K, Lhuillier-Akakpo M, Tanty V, Blugeon C, Alberti A, Labadie K, Aury JM, Sperling L, Duharcourt S, Meyer E (2014) Genome-defence small RNAs exapted for epigenetic mating-type inheritance. Nature 509:447–452
Sonneborn T (1937) Sex, sex inheritance and sex determination in Paramecium aurelia. Proc Natl Acad Sci USA 23:378–385
Sugibayashi R, Harumoto T (2000) Defensive function of trichocysts in Paramecium tetraurelia against heterotrich ciliate Climacostomum virens. Eur J Protistol 36:415–422
Takahashi M (1979) Behavioral mutants in Paramecium caudatum. Genetics 91:393–408
Tassin A-M, Lemullois M, Aubusson-Fleury A (2016) Paramecium tetraurelia basal body structure. Cilia 5:6
Valentine M, Yano Y, Van Houten J (2010) Chemosensory transduction in Paramecium. Jpn J Protozool 41:1–8
Valentine MS, Rajendran A, Yano J, Weeraratne SD, Beisson J, Cohen J, Koll F, Van Houten J (2012) Paramecium BBS genes are key to presence of channels in cilia. Cilia 1:16
Van Houten JL (1979) Membrane potential changes during chemokinesis in Paramecium. Science 204:1100–1103
Van Houten J (1998) Chemosensory transduction in Paramecium. Eur J Protistol 34:301–307
Weber JH, Vishnyakov A, Hambach K, Schultz A, Schultz JE, Linder JU (2004) Adenylyl cyclases from Plasmodium, Paramecium and Tetrahymena are novel ion channel/enzyme fusion proteins. Cell Signal 16:115–125
Yang W, Braun C, Plattner H, Purvee J, Van Houten JL (1997) Cyclic nucleotides in glutamate chemosensory signal transduction of Paramecium. J Cell Sci 110:1567–1572
Yano J, Rajendran A, Valentine MS, Saha M, Ballif BA, Van Houten JL (2013) Proteomic analysis of the cilia membrane of Paramecium tetraurelia. J Proteome 78:113–122
Zagulski M, Nowak JK, LeMouel A, Nowacki M, Migdalski A, Gromadka R, Noel B, Blanc I, Dessen P, Wincker P, Keller AM, Cohen J, Meyer E, Sperling L (2004) High coding density on the largest Paramecium tetraurelia somatic chromosome. Curr Biol 14:1397–1404
Acknowledgments
I thank Dr. Megan Valentine and Dr. Ashik Nabi for contributing images to this chapter.
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2019 Springer Nature Switzerland AG
About this chapter
Cite this chapter
Van Houten, J. (2019). Paramecium Biology. In: Tworzydlo, W., Bilinski, S. (eds) Evo-Devo: Non-model Species in Cell and Developmental Biology. Results and Problems in Cell Differentiation, vol 68. Springer, Cham. https://doi.org/10.1007/978-3-030-23459-1_13
Download citation
DOI: https://doi.org/10.1007/978-3-030-23459-1_13
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-030-23458-4
Online ISBN: 978-3-030-23459-1
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)