Timing and characteristics of nuclear events during conjugation and genomic exclusion in Paramecium multimicronucleatum

Marine Life Science and Technology
Xue Zhang1, Xiaoteng Lu2, Yong Chi1, Yunpeng Jiang3, Chundi Wang4, Saleh Alfarraj5, Adriana Vallesi6, Feng Gao3
1Institute of Evolution and Marine Biodiversity, Ocean University of China, Qingdao 266003, China
2Department of Biology, Shenzhen MSU-BIT University, Shenzhen, 518172, China
3Key Laboratory of Mariculture (OUC), Ministry of Education, Qingdao, 266003, China
4Laboratory of Marine Protozoan Biodiversity and Evolution, Shandong University, Weihai, 264209, China
5Zoology Department, College of Science, King Saud University, Riyadh 11451, Saudi Arabia
6Laboratory of Eukaryotic Microbiology and Animal Biology, University of Camerino, 62032, Camerino, Italy

Tóm tắt

AbstractCiliated protists are ideal material for studying the origin and evolution of sex, because of their nuclear dimorphism (containing both germline micronucleus and somatic macronucleus in the same cytoplasm), special sexual processes (conjugation and autogamy), and high diversity of mating-type systems. However, the study of sexual process is limited to only a few species, due to the difficulties in inducing or observing conjugation. In the present study, we investigate the conjugation process in Paramecium multimicronucleatum: (1) of the three prezygotic divisions, all micronuclei undergo the first two divisions (meiosis I, II), while a variable number of nuclei undergo the third division (mitosis); (2) the synkaryon divides three times after fertilization, giving rise to eight products that differentiate into four macronuclear anlagen and four micronuclei; (3) cells restore the vegetative stage after two successive cell fissions during which the macronuclear anlagen are distributed into daughter cells without division, while micronuclei divide mitotically; (4) the parental macronucleus begins to fragment following the first meiotic division and finally degenerates completely; (5) the entire process takes about 110 h, of which about 85 h are required for macronuclear development. In addition, we describe for the first time the process of genomic exclusion occurring between amicronucleate and micronucleate cells of P. multimicronucleatum, during which the micronucleate cell contributes a pronucleus to the amicronucleate cell, resulting in both exconjugants being homozygotes. These results provide new insights into the diversity of sexual processes and lay an important cytological basis for future in-depth studies of mating systems in ciliates.

Từ khóa


Tài liệu tham khảo

Allen SL (1967) Genomic exclusion: a rapid means for inducing homozygous diploid lines in Tetrahymena pyriformis, syngen 1. Science 155:575–577

Ammermann D, Schlegel M, Hellmer K-H (1989) North American and Eurasian strains of Stylonychia lemnae (Ciliophora, Hypotrichida) have a high genetic identity, but differ in the nuclear apparatus and in their mating behavior. Eur J Protistol 25:67–74

Angeleska A, Jonoska N, Saito M, Landweber LF (2007) RNA-guided DNA assembly. J Theor Biol 248:706–720

Barnett A (1964) Cytology of conjuǵation in Paramecium multimicronucleatum, syngen 2, stock 11. J Protozool 11:147–153

Barnett A (1966) A circadian rhythm of mating type reversals in Paramecium multimicronucleatum, syngen 2, and its genetic control. J Cell Physiol 67:239

Bell G (1982) The masterpiece of nature: the evolution and genetics of sexuality. University of California Press, Berkeley

Butler A, Laughlin T, Cadilla C, Henry J, Olins D (1984) Physical structure of gene-sized chromatin from the protozoan Oxytricha. Nucleic Acids Res 12:3201–3217

Cech TR (1985) Self-splicing RNA: implications for evolution. Int Rev Cytol 93:3–22

Chen X, Jiang Y, Gao F, Zheng W, Krock TJ, Stover NA, Lu C, Katz LA, Song W (2019) Genome analyses of the new model protist Euplotes vannus focusing on genome rearrangement and resistance to environmental stressors. Mol Ecol Resour 19:1292–1308

Cheng T, Wang Y, Huang J, Chen X, Zhao X, Gao S, Song W (2019) Our recent progress in epigenetic research using the model ciliate, Tetrahymena thermophila. Mar Life Sci Technol 1:4–14

Chi Y, Chen X, Li Y, Wang C, Zhang T, Ayoub A, Warren A, Song W, Wang Y (2021) New contributions to the phylogeny of the ciliate class Heterotrichea (Protista, Ciliophora): analyses at family-genus level and new evolutionary hypotheses. Sci China Life Sci 64:606–620

Corliss JO (1975) Nuclear characteristics and phylogeny in the protistan phylum Ciliophora. Biosystems 7:338–349

Dawson JA (1919) An experimental study of an amicronucleate Oxytricha. I. Study of the normal animal, with an account of cannibalism. J Exp Zool 29:473–513

Diller WF (1936) Nuclear reorganization processes in Paramecium aurelia, with descriptions of autogamy and ‘hemixis’. J Morphol 59:11–67

Diller WF (1958) Studies on conjugation in Paramecium polycaryum. J Protozool 5:282–292

Dryl S (1959) Antigenic transformation in Paramecium aurelia after homologous antiserum treatment during autogamy and conjugation. J Protozool 6:25

Duan L, Cheng T, Wei F, Qiao Y, Wang C, Warren A, Niu J, Wang Y (2021) New contribution to epigenetic studies: isolation of micronuclei with high purity and DNA integrity in the model ciliated protist, Tetrahymena thermophila. Eur J Protistol 80:125804

Fokin SI, Przybos E, Chivilev SM (2001) Nuclear reorganization variety in Paramecium (Ciliophora: Peniculida) and its possible evolution. Acta Protozool 40:249–262

Gao Y, Gong R, Jiang Y, Pan B, Li Y, Warren A, Jiang J, Gao F (2020) Morphogenetic characters of the model ciliate Euplotes vannus (Ciliophora, Spirotrichea): notes on cortical pattern formation during conjugational and postconjugational reorganization. Eur J Protistol 73:125675

Giese AC (1957) Mating types in Paramecium multimicronucleatum. J Protozool 4:120–124

Gong R, Jiang Y, Vallesi A, Gao Y, Gao F (2020) Conjugation in Euplotes raikovi (Protista, Ciliophora): new insights into nuclear events and macronuclear development from micronucleate and amicronucleate cells. Microorganisms 8:162

Greider CW, Blackburn EH (1985) Identification of a specific telomere terminal transferase activity in Tetrahymena extracts. Cell 43:405–413

Hall T (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98

Hamburger C (1904) Die Konjugation von Paramecium bursaria Focke. Arch Protistenk 4:199–239

Jankowski AW (1961) The process of conjugation in the rare salt-water Paramecium, P. woodruffi. Doklady Acad Nauk SSSR 137:989–992

Jankowski AW (1972) Cytogenetics of Paramecium putrinum. Acta Protozool 10:285–394

Jerome CA, Lynn DH, Simon EM (1996) Description of Tetrahymena empidokyrea n. sp., a new species in the Tetrahymena pyriformis sibling species complex (Ciliophora, Oligohymenophorea), and an assessment of its phylogenetic position using small-subunit rRNA sequences. Can J Zool 74:1898–1906

Jiang Y, Zhang T, Vallesi A, Yang X, Gao F (2019) Time-course analysis of nuclear events during conjugation in the marine ciliate Euplotes vannus and comparison with other ciliates (Protozoa, Ciliophora). Cell Cycle 18:288–298

Katz LA (2001) Evolution of nuclear dualism in ciliates: a reanalysis in light of recent molecular data. Int J Syst Evol Microbiol 51:1587–1592

Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874

Landis EM (1920) An amicronucleate race of Paramecium caudatum. Am Nat 54:453–457

Landis EM (1925) Conjugation of Paramecium multimicronucleata, Powers and Mitchell. J Morphol 40:111–167

Li C, Chen X, Zheng W, Doak TG, Fan G, Song W, Yan Y (2021) Chromosome organization and gene expansion in the highly fragmented genome of the ciliate Strombidium stylifer. J Genet Genomics 48:908–916

Lynn DH (2008) The ciliated protozoa: characterization, classification, and guide to the literature. Springer Science & Business Media, Berlin

Ma M, Xu Y, Yan Y, Li Y, Warren A, Song W (2021) Taxonomy and molecular phylogeny of four karyorelictid species belonging to the genera Apotrachelocerca and Tracheloraphis (Protozoa: Ciliophora), with descriptions of two new species. Zool J Linn Soc 192:690–709

Medlin L, Elwood HJ, Stickel S, Sogin ML (1988) The characterization of enzymatically amplified eukaryotic 16S-like rRNA-coding regions. Gene 71:491–499

Mikami K (1979) Stomatogenesis during sexual and asexual reproduction in an amicronucleate strain of Paramecium caudatum. J Exp Zool 208:121–127

Montagnes D, Roberts E, Lukeš J, Lowe C (2012) The rise of model protozoa. Trends Microbiol 20:184–191

Nakata A (1956) Micronuclear behavior during the conjugation of Haramecium calkinsi. Doubutsugaku Zasshi 65:306–310

Ng SF (1989) Cytidine analogues and stomatogenic recovery in amicronucleate Paramecium tetraurelia and Paramecium jenningsi. J Protozool 36:74–81

Nowacki M, Vijayan V, Zhou Y, Schotanus K, Doak TG, Landweber LF (2008) RNA-mediated epigenetic programming of a genome-rearrangement pathway. Nature 451:153–158

Nylander JA (2004) MrModeltest v2. Uppsala University

Orias E, Singh DP, Meyer E (2017) Genetics and epigenetics of mating type determination in Paramecium and Tetrahymena. Annu Rev Microbiol 71:133–156

Phadke SS, Zufall RA (2009) Rapid diversification of mating systems in ciliates. Biol J Linn Soc Lond 98:187–197

Prescott DM (1994) The DNA of ciliated protozoa. Microbiol Rev 58:233–267

Raikov IB (1972) Nuclear phenomena during conjugation and autogamy in ciliates. Res protozool. Elsevier, Amsterdam, pp 147–289

Raikov IB (1982) The protozoan nucleus: morphology and evolution. Springer-Verlag, New York

Sela I, Ashkenazy H, Katoh K, Pupko T (2015) GUIDANCE2: accurate detection of unreliable alignment regions accounting for the uncertainty of multiple parameters. Nucleic Acids Res 43:W7–W14

Sheng Y, Duan L, Cheng T, Qiao Y, Stover NA, Gao S (2020) The completed macronuclear genome of a model ciliate Tetrahymena thermophila and its application in genome scrambling and copy number analyses. Sci China Life Sci 63:1534–1542

Singh DP, Saudemont B, Guglielmi G, Arnaiz O, Goût J-F, Prajer M, Potekhin A, Przybòs E, Aubusson-Fleury A, Bhullar S (2014) Genome-defence small RNAs exapted for epigenetic mating-type inheritance. Nature 509:447–452

Sonneborn TM (1938) Mating types in Paramecium aurelia: diverse conditions for mating in different stocks; occurrence, number and interrelations of the types. Proc Am Philos Soc 110:411–434

Stamatakis A (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30:1312–1313

Swart EC, Bracht JR, Magrini V, Minx P, Chen X, Zhou Y, Khurana JS, Goldman AD, Nowacki M, Schotanus K, Jung S, Fulton RS, Ly A, McGrath S, Haub K, Wiggins JL, Storton D, Matese JC, Parsons L, Chang WJ et al (2013) The Oxytricha trifallax macronuclear genome: a complex eukaryotic genome with 16,000 tiny chromosomes. PLoS Biol 11:e1001473

Takahashi T, Suhama M (1991) Regeneration of amicronucleate fragments in the hypotrichous ciliate Pseudourostyla levis. Eur J Protistol 26:308–318

Wang C, Gao Y, Lu B, Chi Y, Zhang T, El-Serehy HA, Al-Farraj SA, Li L, Song W, Gao F (2021) Large-scale phylogenomic analysis provides new insights into the phylogeny of the class Oligohymenophorea (Protista, Ciliophora) with establishment of a new subclass Urocentria nov. subcl. Mol Phylogenet Evol 159:107112

Watanabe T, Shi X, Liu G, Jin M (1996) Cytological studies of conjugation and nuclear processes in Paramecium duboscqui Chatton & Brachon 1933. Eur J Protistol 32:175–182

Wichterman R (1948) The time schedule of mating and nuclear events in the conjugation of Paramecium bursaria. Turtox News 26:2–10

Xu J, Zhao X, Mao F, Basrur V, Ueberheide B, Chait BT, Allis CD, Taverna SD, Gao S, Wang W (2021) A Polycomb repressive complex is required for RNAi-mediated heterochromatin formation and dynamic distribution of nuclear bodies. Nucleic Acids Res 49:5407–5425

Yang X, Gao X, Shi X (2007) Detection of haploid nuclear death in living Paramecium caudatum. Jpn J Protozool 40:123–130

Zhao X, Li Y, Duan L, Chen X, Mao F, Juma M, Liu Y, Song W, Gao S (2020) Functional analysis of the methyltransferase SMYD in the single-cell model organism Tetrahymena thermophila. Mar Life Sci Technol 2:109–122

Zhao L, Gao F, Gao S, Liang Y, Long H, Lv Z, Su Y, Ye N, Zhang L, Zhao C, Wang X, Song W, Zhang S, Dong B (2021) Biodiversity-based development and evolution: the emerging research systems in model and non-model organisms. Sci China Life Sci 64:1236–1280

Zheng W, Wang C, Lynch M, Gao S (2021) The compact macronuclear genome of the ciliate Halteria grandinella: a transcriptome-like genome with 23,000 nanochromosomes. mBio 12:e01964-20.

Zimmer C (2009) On the origin of sexual reproduction. Science 324:1254–1256

Thông tin
Thông tin xuất bản

Marine Life Science and Technology

Thông tin tác giả