Global molecular variation of Paramecium jenningsi complex (Ciliophora, Protista): a starting point for further, detailed biogeography surveys

References

• Aufderheide, K. J., Daggett, P.-M., & Nerad, T. A. (1983). Paramecium sonneborni n. sp., a new member of the Paramecium aurelia species complex. The Journal of Protozoology, 30, 128–131. doi: 10.1111/j.1550-7408.1983.tb01046.x
   Google Scholar
• Azovsky, A. I., Tikhonenkov, D. V., & Mazei, Y. A. (2016). An estimation of the global diversity and distribution of the smallest eukaryotes: Biogeography of marine benthic heterotrophic flagellates. Protist, 167, 411–424. doi: 10.1016/j.protis.2016.07.001
   PubMed Web of Science ®Google Scholar
• Bandelt, H., Forster, P., & Röhl, A. (1999). Median-joining networks for inferring intraspecific phylogenies. Molecular Biology and Evolution, 16, 37–48. doi: 10.1093/oxfordjournals.molbev.a026036
   PubMed Web of Science ®Google Scholar
• Beale, G. H., & Preer, J. R. Jr (2008). Paramecium: Genetics and epigenetics. Boca Raton, FL: CRC Press, Taylor & Francis Group.
   Google Scholar
• Beliavskaia, A., Kiselev, A., & Rautian, M. (2016). New Paramecium species “Candidatus Paramecium ossipovi”. Abstracts of the International Scientific Forum “Protist- 2106”, Moscow, Russia, 6–10 June 2016. Protistology, 22, 148–155.
   Google Scholar
• Bengtsson-Palme, J., Richardson, R. T., Meola, M., Wurzbacher, C., Tremblay, É. D., Thorell, K., … Nilsson, R. H. (2018). Metaxa2 database builder: Enabling taxonomic identification from metagenomic or metabarcoding data using any genetic marker. Bioinformatics, 34, 4027–4033. doi: 10.1093/bioinformatics/bty482
   PubMed Web of Science ®Google Scholar
• Benson, D. A., Karsch-Mizrachi, I., Clark, K., Lipman, D. J., Ostell, J., & Sayers, E. W. (2012). GenBank. Nucleic Acids Research, 40, D48–D53. doi: 10.1093/nar/gkr1202
   PubMed Web of Science ®Google Scholar
• Boenigk, J., Wodniok, S., Bock, C., Beisser, D., Hempel, C., Grossmann, L., … Jensen, M. (2018). Geographic distance and mountain ranges structure freshwater protist communities on a European scalе. Metabarcoding and Metagenomics, 2, e21519. doi: 10.3897/mbmg.2.21519
   Google Scholar
• Boscaro, V., Fokin, S. I., Schrallhammer, M., Schweikert, M., & Petroni, G. (2013). Revised systematics of Holospora-like bacteria and characterization of “Candidatus Gortzia infectiva”, a novel macronuclear symbiont of Paramecium jenningsi. Microbial Ecology, 65, 255–267. doi: 10.1007/s00248-012-0110-2
   PubMed Web of Science ®Google Scholar
• Chantangsi, C., Lynn, D. H., Brandl, M. T., Cole, J. C., Hetrick, N., & Ikonomi, P. (2007). Barcoding ciliates: A comprehensive study of 75 isolates of the genus Tetrahymena. International Journal of Systematic and Evolutionary Microbiology, 57, 2412–2425. doi: 10.1099/ijs.0.64865-0
   PubMed Web of Science ®Google Scholar
• Chen, T. T. (1956). Varieties and mating types in Paramecium bursaria. II. Variety and mating types found in China. Journal of Experimental Zoology, 132, 255–268. doi: 10.1002/jez.1401320205
   Google Scholar
• Darling, K. F., Kucera, M., & Wade, C. M. (2007). Global molecular phylogeography reveals persistent Arctic circumpolar isolation in a marine planktonic protist. Proceedings of the National Academy of Sciences of the United States of America, 104, 5002–5007. doi: 10.1073/pnas.0700520104
   PubMed Web of Science ®Google Scholar
• Debroas, D., Domaizon, I., Humbert, J.-F., Jardillier, L., Lepère, C., Oudart, A., & Taïb, N. (2017). Overview of freshwater microbial eukaryotes diversity: A first analysis of publicly available metabarcoding data. Federation of European Microbiological Society Microbiology Ecology, 93. https://doi.org/10.1093/femsec/fix023.
   Google Scholar
• del Campo, J., Kolisko, M., Boscaro, V., Santoferrara, L. F., Nenarokov, S., Massana, R., … Parfrey, L. W. (2018). EukRef: Phylogenetic curation of ribosomal RNA to enhance understanding of eukaryotic diversity and distribution. Public Library of Science Biology, 16, e2005849. doi: 10.1371/journal.pbio.2005849
   Google Scholar
• Diller, W. F., & Earl, P. R. (1958). Paramecium jenningsi, n. sp. The Journal of Protozoology, 5, 155–158. doi: 10.1111/j.1550-7408.1958.tb02545.x
   Google Scholar
• Dunthorn, M., Klier, J., Bunge, J., & Stoeck, T. (2012). Comparing the hyper-variable V4 and V9 regions of the small subunit rDNA for assessment of ciliate environmental diversity. Journal of Eukaryotic Microbiology, 59, 185–187. doi: 10.1111/j.1550-7408.2011.00602.x
   PubMed Web of Science ®Google Scholar
• Dunthorn, M., Stoeck, T., Clamp, J., Warren, A., & Mahé, F. (2014). Ciliates and the rare biosphere: A review. Journal of Eukaryotic Microbiology, 61, 404–409. doi: 10.1111/jeu.12121
   PubMed Web of Science ®Google Scholar
• Flis, J. (1967). Ethiopia. In A. Zierhoffer (Ed.), Geografia Powszechna (Vol. 4, pp. 584–597). Warszawa: PWN. (In Polish).
   Google Scholar
• Fenchel, T., & Finlay, B. J. (2004). The ubiquity of small species: Patterns of local and global diversity. BioScience, 54, 777–784.
   Web of Science ®Google Scholar
• Ficetola, G. F., Miaud, C., Pompanon, F., & Taberlet, P. (2008). Species detection using environmental DNA from water samples. Biology Letters, 4, 423–425. doi: 10.1098/rsbl.2008.0118
   PubMed Web of Science ®Google Scholar
• Filker, S., Sommaruga, R., Vila, I., & Stoeck, T. (2016). Microbial eukaryote plankton communities of high-mountain lakes from three continents exhibit strong biogeographic patterns. Molecular Ecology, 25, 2286–2301. doi: 10.1111/mec.13633
   PubMed Web of Science ®Google Scholar
• Finlay, B. J., Esteban, G. F., Brown, S., Fenchel, T., & Hoef-Emden, K. (2006). Multiple cosmopolitan ecotypes within a microbial eukaryote morphospecies. Protist, 157, 377–390. doi: 10.1016/j.protis.2006.05.012
   PubMed Web of Science ®Google Scholar
• Foissner, W. (2006). Biogeography and dispersal of micro-organisms: A review emphasizing Protists. Acta Protozoologica, 45, 111–136.
   Web of Science ®Google Scholar
• Foissner, W., Chao, A., & Katz, L. A. (2008). Diversity and geographic distribution of ciliates (Protista: Ciliophora). Biodiversity and Conservation, 17, 345–363. doi: 10.1007/s10531-007-9254-7
   Web of Science ®Google Scholar
• Fokin, S. I. (1997). Morphological diversity of the micronuclei in Paramecium. Archiv für Protistenkunde, 148, 375–387. doi: 10.1016/S0003-9365(97)80017-6
   Google Scholar
• Fokin, S. I. (2010/2011). Paramecium genus: Biodiversity, some morphological features and the key to the main morphospecies discrimination. Protistology, 6, 227–235.
   Google Scholar
• Fokin, S. I. (2017). Current situation and future perspective of biodiversity in the Paramecium genus. Paramecium [epi] Genome Organization, Dynamics and Evolution, 3–6 October 2017, Nohfelden, Germany, Abstracts, p. 15.
   Google Scholar
• Gentekaki, E., & Lynn, D. H. (2010). Evidence for cryptic speciation in Carchesium polypinum Linnaeus, 1758 (Ciliophora: Peritrichia) inferred from mitochondrial, nuclear, and morphological markers. Journal of Eukaryotic Microbiology, 57, 508–519. doi: 10.1111/j.1550-7408.2010.00505.x
   PubMed Web of Science ®Google Scholar
• Hall, T. A. (1999). BioEdit: A user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series, 41, 95–98.
   Google Scholar
• Krenek, S., Berendonk, T. U., & Fokin, S. I. (2015). New Paramecium (Ciliophora, Oligohymenophorea) congeners shape our view on its biodiversity. Organisms Diversity & Evolution, 15, 215–233. doi: 10.1007/s13127-015-0207-9
   Web of Science ®Google Scholar
• Lara, E., Mataloni, G., Seppey, C. V. M., Singer, D., Schiaffino, M. R., & Izaguire, I. (2015). Freshwater plankton community ecology under high throughput sequencing perspective. VII European Congress of Protistology, the International Society of Protistologists, 5–10 September 2015, Seville, Spain. Abstracts, p. 145.
   Google Scholar
• Leigh, J. W., & Bryant, D. (2015). PopART: Full-feature software for haplotype network construction. Methods in Ecology and Evolution, 6, 1110–1116. doi: 10.1111/2041-210X.12410
   Web of Science ®Google Scholar
• Librado, P., & Rozas, J. (2009). DnaSP v5: A software for comprehensive analysis of DNA polymorphism data. Bioinformatics, 25, 1451–1452. doi: 10.1093/bioinformatics/btp187
   PubMed Web of Science ®Google Scholar
• Mahe, F., Mayor, J., Bunge, J., Chi, J., Siemensmeyer, T., Stoeck, T., … Dunthorn, M. (2015). Comparing high-throughput platforms for sequencing the V4 Region of SSU-rDNA in environmental microbial eukaryotic diversity surveys. Journal of Eukaryotic Microbiology, 62, 338–345. doi: 10.1111/jeu.12187
   PubMed Web of Science ®Google Scholar
• Maciejewska, A. (2007). Relationships of new sibling species of Paramecium jenningsi based on sequences of the histone H4 gene fragment. European Journal of Protistology, 43, 125–130. doi: 10.1016/j.ejop.2006.12.005
   PubMed Web of Science ®Google Scholar
• Messing, J. (1983). New M13 vectors for cloning. Methods in Enzymology, 101, 20–78.
   PubMed Web of Science ®Google Scholar
• Page, R. D. M. (1996). TreeView: An application to display phylogenetic tress on personal computers. Bioinformatics, 12, 357–358. doi: 10.1093/bioinformatics/12.4.357
   Google Scholar
• Paiva, T. S., Borges, B. N., Harada, M. L., & Silva-Neto, I. D. (2016). Description and molecular phylogeny of Paramecium grohmannae sp. nov. (Ciliophora, Peniculida) from a wastewater treatment plant in Brazil. Revista Brasileira de Zoociencias, 17, 7–19.
   Google Scholar
• Pawlowski, J. (2015). Protist metabarcoding and its applications. VII European Congress of Protistology in partnership with the International Society of Protitologists, 5–10 September 2015, Seville, Spain. Abstracts, p. 60.
   Google Scholar
• Pawlowski, J., Audic, S., Adl, S., Bass, D., Belbahri, L., Berney, C., … de Vargas, C. (2012). CBOL Protist working group: Barcoding eukaryotic richness beyond the animal, plant, and fungal kingdoms. Public Library of Science Biology, 10, e1001419. doi: 10.1371/journal.pbio.1001419
   Google Scholar
• Pawlowski, J., Kelly-Quinn, M., Altermatt, F., Apothéloz-Perret-Gentil, L., Beja, P., Boggero, A., … Kahlert, M. (2018). The future of biotic indices in the ecogenomic era: Integrating (e)DNA metabarcoding in biological assessment of aquatic ecosystems. Science of the Total Environment, 637-638, 1295–1310. doi: 10.1016/j.scitotenv.2018.05.002
   PubMed Web of Science ®Google Scholar
• Porter, T. M., & Hajibabaei, M. (2018a). Automated high throughput animal COI metabarcode classification. Scientific Reports, 8, 4226. doi: 10.1038/s41598-018-22505-4
   PubMed Web of Science ®Google Scholar
• Porter, T. M., & Hajibabaei, M. (2018b). Over 2.5 million COI sequences in GenBank and growing. Public Library of Science One, 13, e0200177. doi: 10.1371/journal.pone.0200177
   Google Scholar
• Przyboś, E. (1975). Genetic studies of Paramecium jenningsi strains (Diller and Earl, 1958). Folia Biologica (Kraków), 23, 425–471.
   PubMedGoogle Scholar
• Przyboś, E. (1986). Chromosomes in Paramecium jenningsi (Diller and Earl. 1958): A serial section study. Folia Biologica (Kraków), 34, 133–160.
   Web of Science ®Google Scholar
• Przyboś, E., & Tarcz, S. (2013). Three-locus analysis in conjunction with strain crosses confirms the existence of reproductively isolated populations in Paramecium jenningsi (Diller and Earl 1958). Systematics and Biodiversity, 11, 507–523. doi: 10.1080/14772000.2013.865680
   Web of Science ®Google Scholar
• Przyboś, E., & Tarcz, S. (2016). Paramecium jenningsi complex: Existence of three cryptic species confirmed by multi-locus analysis and strain crosses. Systematics and Biodiversity, 14, 140–154. doi: 10.1080/14772000.2015.1134701
   Web of Science ®Google Scholar
• Przyboś, E., Fokin, S., Stoeck, T., & Schmidt, H. J. (1999). Occurrence and ecology of Paramecium jenningsi. Folia Biologica (Kraków), 47, 53–59.
   Web of Science ®Google Scholar
• Przyboś, E., Kalavati, C., Fokin, S. I., & Tarcz, S. (2017). Paramecium jenningsi species complex (Ciliophora, Protista) in India: The first description of new stands of P. bijenningsi and P. trijenningsi. Folia Biologica, 65, 55–61. doi: 10.3409/fb65_1.55
   Web of Science ®Google Scholar
• Przyboś, E., Skotarczak, B., & Wodecka, B. (2003). Phylogenetic ralationships of Paramecium jenningsi strains (classical analysis and RAPD studies). Folia Biologica (Kraków), 51, 85–95.
   PubMed Web of Science ®Google Scholar
• Przyboś, E., & Tarcz, S. (2018). New stands of the Paramecium aurelia spp. complex (Protista, Oligohymenophorea) in Ethiopia, Madagascar, Taiwan, and Romania. Folia Biologica, 66, 111–119. doi: 10.3409/fb_66-3.12
   Web of Science ®Google Scholar
• Przyboś, E., Tarcz, S., & Dusi, E. (2013). New Paramecium quadecaurelia strains (P. aurelia spp. complex, Ciliophora) identified by molecular markers (rDNA and mtDNA). European Journal of Protistology, 49, 477–486. doi: 10.1016/j.ejop.2012.11.001
   PubMed Web of Science ®Google Scholar
• Przyboś, E., Tarcz, S., Rautian, M., & Lebedeva, N. (2014). The first European stand of Paramecium sonneborni (P. aurelia complex), a species known only from the Northern America (USA, Texas). Insights from molecular, genetic, and cytological studies. European Journal of Protistology, 50, 236–247. doi: 10.1016/j.ejop.2014.03.001
   PubMed Web of Science ®Google Scholar
• Przyboś, E., Tarcz, S., Rautian, M., & Sawka, N. (2015). Delimiting species boundaries within a paraphyletic species complex: Insights from morphological, genetic, and molecular data on Paramecium sonneborni (Paramecium aurelia species complex, Ciliphora, Protozoa). Protist, 166, 438–456. doi: 10.1016/j.protis.2015.07.001
   PubMed Web of Science ®Google Scholar
• Ratnasingham, S., & Hebert, P. D. N. (2007). bold: The Barcode of Life Data System. Molecular Ecology Notes, 7, 355–364. doi: 10.1111/j.1471-8286.2007.01678.x. Retrieved from http://www.barcodinglife.org (accessed 30 July 2019).
   PubMed Web of Science ®Google Scholar
• Ronquist, F., & Huelsenbeck, J. P. (2003). MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics, 19, 1572–1574. doi: 10.1093/bioinformatics/btg180
   PubMed Web of Science ®Google Scholar
• Rossi, A., Boscaro, V., Carducci, D., Serra, V., Modeo, L., Verni, F., … Petroni, G. (2016). Ciliate communities and hidden biodiversity in freshwater biotopes of the Pistoia province (Tuscany, Italy). European Journal of Protistology, 53, 11–19. doi: 10.1016/j.ejop.2015.12.005
   PubMed Web of Science ®Google Scholar
• Serra, V., Fokin, S. I., Castelli, M., Basuri, C. K., Nitla, V., Verni, F., … Petroni, G. (2016). “Candidatus Gortzia Shahrazadis”, a novel endosymbiont of Paramecium multimicronucleatum and a revision of the biogeographical distribution of Holospora–like bacteria. Frontiers in Microbiology, 7, 1704. doi: 10.3389/fmicb.2016.01704
   PubMed Web of Science ®Google Scholar
• Shakoori, F. R., Tasneem, F., Al-Ghanim, K., Mahboob, S., Al-Misned, F., Jahan, N., & Shakoori, A. R. (2014). Variability in secondary structure of 18S ribosomal RNA as topological marker for identification of Paramecium species. Journal of Cellular Biochemistry, 115, 2077–2088. doi: 10.1002/jcb.24885
   PubMed Web of Science ®Google Scholar
• Sogin, M. L., Morrison, H. G., Huber, J. A., Welch, D. M., Huse, S. M., Neal, P. R., … Herndl, G. J. (2006). Microbial diversity in the deep sea and the underexplored “rare biosphere”. Proceedings of the National Academy of Sciences of the United States of America, 103, 12115–12120. doi: 10.1073/pnas.0605127103
   PubMed Web of Science ®Google Scholar
• Sonneborn, T. M. (1950). Methods in the general biology and genetics of Paramecium. Journal of Experimental Zoology, 113, 87–148. doi: 10.1002/jez.1401130106
   Google Scholar
• Sonneborn, T. M. (1970). Methods in Paramecium research. In D. M. Prescott (Ed.), Methods of cell physiology, vol. 4 (pp. 241–339). New York and London: Academic Press.
   Google Scholar
• Sonneborn, T. M. (1975). The Paramecium aurelia complex of fourteen sibling species. Transactions of the American Microscopical Society, 94, 155–178. doi: 10.2307/3224977
   Google Scholar
• Stoeck, T., Bass, D., Nebel, M., Christen, R., Jones, M. D., Breiner, H. W., & Richards, T. A. (2010). Multiple marker parallel tag environmental DNA sequencing reveals a highly complex eukaryotic community in marine anoxic water. Molecular Ecology, 19, 21–31. doi: 10.1111/j.1365-294X.2009.04480.x
   PubMed Web of Science ®Google Scholar
• Stoeck, T., Przybos, E., & Dunthorn, M. (2014). The D1-D2 region of the large ribosomal DNA as barcode for ciliates. Molecular Ecology Resources, 14, 458–468. doi: 10.1111/1755-0998.12195
   PubMed Web of Science ®Google Scholar
• Strüder-Kypke, M. C., & Lynn, D. H. (2010). Comparative analysis of the mitochondrial cytochrome c oxidase subunit I (COI) gene in ciliates (Alveolata, Ciliophpra) and evaluation of its suitability as a biodiversity marker. Systematics and Biodiversity, 8, 131–148. doi: 10.1080/14772000903507744
   Web of Science ®Google Scholar
• Strüder-Kypke, M. C., Wright, A. G., Fokin, S. I., & Lynn, D. H. (2000). Phylogenetic relationships of the genus Paramecium inferred from small subunit rRNA gene sequences. Molecular Phylogenetics and Evolution, 14, 122–130. doi: 10.1006/mpev.1999.0686
   PubMed Web of Science ®Google Scholar
• Tamura, K., Stecher, G., Peterson, D., Filipski, A., & Kumar, S. (2013). MEGA6: Molecular Evolutionary Genetics Analysis Version 6.0. Molecular Biology and Evolution, 30, 2725–2729. doi: 10.1093/molbev/mst197
   PubMed Web of Science ®Google Scholar
• Tarcz, S., Potekhin, A., Rautian, M., & Przyboś, E. (2012). Variation in ribosomal and mitochondrial DNA sequences demonstrates the existence of intraspecific groups in Paramecium multimicronucleatum (Ciliophora, Oligohymenophorea). Molecular Phylogenetics and Evolution, 63, 500–509. doi: 10.1016/j.ympev.2012.01.024
   PubMed Web of Science ®Google Scholar
• Tarcz, S., Przyboś, E., & Surmacz, M. (2013). An assessment of haplotype variation in ribosomal and mitochondrial DNA fragments suggests incomplete lineage sorting in some species of the Paramecium aurelia complex (Ciliophora, Protozoa). Molecular Phylogenetics and Evolution, 67, 255–265. doi: 10.1016/j.ympev.2013.01.016
   PubMed Web of Science ®Google Scholar
• Tarcz, S., Sawka-Gądek, N., & Przyboś, E. (2018). Worldwide sampling reveals low genetic variability in populations of the freshwater ciliate Paramecium biaurelia (P. aurelia species complex, Ciliophora, Protozoa). Organisms Diversity & Evolution, 18, 39–50.
   Web of Science ®Google Scholar
• Venter, J. C., Remington, K., Heidelberg, J. F., Halpern, A. L., Rusch, D., Eisen, J. A., … Smith, H. O. (2004). Environmental genome shotgun sequencing of the Sargasso sea. Science, 304, 66–74. doi: 10.1126/science.1093857
   PubMed Web of Science ®Google Scholar
• Watts, P. C., Martin, L. E., Kimmance, S. E., Montagnes, D. J. S., & Lowe, C. D. (2011). The distribution of Oxyrrhis marina–A global wanderer or poorly characterised endemic? Journal of Plankton Research, 33, 579–589. doi: 10.1093/plankt/fbq148
   Web of Science ®Google Scholar
• White, T. J., Bruns, T., Lee, S., & Taylor, J. (1990). PCR protocols: A guide to methods and applications: Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. San Diego, CA: Academic Press.
   Google Scholar
• Wichterman, R. (1986). The biology of Paramecium. New York: Plenum Press.
   Google Scholar