Morphology, ultrastructure, and molecular phylogeny of the ciliate Sonderia vorax with insights into the systematics of order Plagiopylida

BMC Microbiology

Giulio Petroni²  Franco Verni²  Giovanna Rosati²  Filippo Ferrantini²  Ilaria Andreoli²  Vittorio Boscaro²  Sergei I Fokin¹  Letizia Modeo² 

[1] Department of Invertebrate Zoology, St. Petersburg State University, Universitetskaya emb. 7/9, St. Petersburg, 199034, Russia;Unit of Protistology-Zoology, Department of Biology, University of Pisa, via A. Volta 4/6, Pisa 56126, Italy

关键词: Ultrastructure;    Sulphide fauna;    SSU rRNA;    Silver-nitrate staining;    Phylogeny;    Plagiopylida;    Oxygen deficient environment;    Hydrogenosomes-endosymbionts assemblages;    FISH;    Ectosymbionts;   

Others  :  1144416
DOI  :  10.1186/1471-2180-13-40

 received in 2012-11-28, accepted in 2013-02-08,  发布年份 2013

【 摘 要 】

Background

Ciliates of the family Sonderiidae are common members of the eukaryotic communities in various anoxic environments. They host both ecto- and endosymbiotic prokaryotes (the latter associated with hydrogenosomes) and possess peculiar morpho-ultrastructural features, whose functions and homologies are not known. Their phylogenetic relationships with other ciliates are not completely resolved and the available literature, especially concerning electron microscopy and molecular studies, is quite scarce.

Results

Sonderia vorax Kahl, 1928 is redescribed from an oxygen-deficient, brackish-water pond along the Ligurian Sea coastlines of Italy. Data on morphology, morphometry, and ultrastructure are reported. S. vorax is ovoid-ellipsoid in shape, dorsoventrally flattened, 130 x 69 μm (mean in vivo); it shows an almost spherical macronucleus, and one relatively large micronucleus. The ventral kinetom has a “secant system” including fronto-ventral and fronto-lateral kineties. A distinctive layer of bacteria laying between kineties covers the ciliate surface. Two types of extrusomes and hydrogenosomes-endosymbiotic bacteria assemblages are present in the cytoplasm. The phylogeny based on 18S rRNA gene sequences places S. vorax among Plagiopylida; Sonderiidae clusters with Plagiopylidae, although lower-level relationships remain uncertain. The studied population is fixed as neotype and the ciliate is established as type species of the genus, currently lacking.

Conclusions

This is the first description of a representative of Sonderiidae performed with both morphological and molecular data. To sum up, many previous hypotheses on this interesting, poorly known taxon are confirmed but confusion and contradictory data are as well highlighted.

【 授权许可】

   
2013 Modeo et al.; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

Figure 2.

Figure 3.

Figure 4.

Figure 5.

Figure 6.

Figure 7.

Figure 8.

Figure 9.

Figure 10.

【 参考文献 】

• [1]Kahl A: Die Infusorien (Ciliata) der Oldesloer Salzwasserstellen. Arch Hydrobiol 1928, 19:50-123.
• [2]Borror AC: Tidal marsh ciliates (Protozoa: morphology, ecology and systematics). Acta Protozool 1972, 10:29-71.
• [3]Czapik A, Jordan A: Les ciliés psammophiles de la mer Baltique aux environs de Gdánsk. Partie I. Acta Protozool 1976, 15:423-446.
• [4]Dragesco J, Dragesco-Kernéis A: Cilies libres de l’Afrique intertropicale. Faune Tropicale 1986, 26:1-559.
• [5]Fauré-Fremiet E, Tuffrau M: Sonderia labiata, n. sp., cilié trichostome psammobie. Hydrobiologia 1955, 7:210-218.
• [6]Fenchel T: The ecology of marine microbenthos. IV. Structure and function of the benthic ecosystem, its chemical and physical factors and the microfauna communities with special reference to the ciliated protozoa. Ophelia 1969, 6:1-182.
• [7]Kirby H: Some ciliates from salt marshes in California. Arch Protistenkd 1934, 82:114-133.
• [8]Modeo L, Fokin SI, Ferrantini F, Rosati G, Verni F: Morphological and ultrastructural study on the plagiopylid ciliate Sonderia sp. Kahl, 1928. J Eukaryot Microbiol 2007, 54:76a.
• [9]Sola A, Guinea A, Longás JF, Fernández-Galiano D: Quelques observations sur le cilie Sonderia sinuata Kahl, 1931 (Ciliophora, Trichostomatida). Arch Protistenkd 1989, 137:1-8.
• [10]Corliss JO: The ciliated protozoa. Characterization, classification, and guide to the literature. 2nd edition. Oxford, New York, Toronto, Sydney, Paris, Frankfurt: Pergamon Press; 1979.
• [11]Kahl A: Urtiere oder Protozoa. 1: Wimpertiere oder Ciliata (Infusoria). 2. Holotricha außer den im 1. Teil behandeiten Prostomata. Tierwelt Dtl 1931, 21:181-398.
• [12]Lynn DH: The ciliated protozoa. Characterization, classification, and guide to the literature. 3rd edition. Germany: Springer; 2008.
• [13]Lynn DH, Small EB: Phylum Ciliophora. In An illustrated guide to the Protozoa. 2nd edition. Edited by Lee JJ, Hutner SH, Bovee EC. Lawrence (KS), USA: Allen Press; 2000:371-655.
• [14]Fauré-Fremiet E: Le genre Parasonderia n. g. C R Acad Sci 1973, 276:2011-2014.
• [15]Jankowski AW: Phylum Ciliophora Doflein, 1901. In Handbook on Zoology, Part 2. Protista. Edited by Alimov AF. St. Petersburg: Zoological Institute Press, Russian Academy of Sciences; 2007:415-993. In Russian with English summary
• [16]Xu Y, Shao C, Miao M, Song W: Redescription of Parasonderia vestita (Kahl, 1928) comb. nov. (Ciliophora, Plagiopylida), with notes on its phylogeny based on SSU rRNA gene. Eur J Protistolin press
• [17]Aescht E: Catalogue of the generic names of ciliates (Protozoa, Ciliophora). Denisia 2001, 1:1-350.
• [18]Foissner W, Wenzel F: Life and legacy of an outstanding ciliate taxonomist, Alfred Kahl (1877–1946), including a facsimile of his forgotten monograph from 1943. Acta Protozool 2004, 43(Suppl):3-69.
• [19]Embley TM, Finlay BJ, Dyal PL, Hirt RP, Wilkinson M, Williams AG: Multiple origins of anaerobic ciliates with hydrogenosomes within the radiation of aerobic ciliates. Proc R Soc Lond B Biol Sci 1995, 262:87-93.
• [20]Zhang Q, Simpson A, Song W: Insights into the phylogeny of the systematically controversial haptorian ciliates (Ciliophora, Litostomatea) based on multigene analyses. Proc R Soc Lond B Biol Sci 2012, 279:2625-2635.
• [21]Lynn DH, Strüder-Kypke M: Phylogenetic position of Licnophora, Lechriopyla, and Schizocaryum, three unusual ciliates (Phylum Ciliophora) endosymbiotic in echinoderms (Phylum Echinodermata). J Eukaryot Microbiol 2002, 49:460-468.
• [22]Baumgartner M, Stetter KO, Foissner W: Morphological, small subunit rRNA, and physiological characterization of Trimyema minutum Kahl, 1931, an anaerobic ciliate from submarine hydrothermal vents growing from 28°C to 52°C. J Eukaryot Microbiol 2002, 49:227-238.
• [23]Shinzato N, Watanabe I, Meng XY, Sekiguchi Y, Tamaki H, Matsui T, Kamagata Y: Phylogenetic analysis and fluorescence in situ hybridization detection of archaeal and bacterial endosymbionts in the anaerobic ciliate Trimyema compressum. Microb Ecol 2007, 54:627-636.
• [24]Cho BC, Park JS, Xu K, Choi JK: Morphology and molecular phylogeny of Trimyema koreanum n. sp., a ciliate from the hypersaline water of a solar saltern. J Eukaryot Microbiol 2008, 55:417-426.
• [25]Stoeck T, Foissner W, Lynn DH: Small-subunit rRNA phylogenies suggest that Epalxella antiquorum (Penard, 1922) Corliss, 1960 (Ciliophora, Odontostomatida) is a member of the Plagiopylea. J Eukaryot Microbiol 2007, 54:436-442.
• [26]Skovorodkin IN: A device for immobilization of small biological objects during light microscopical observation. Tsitologiia 1990, 32:87-91. In Russian with English summary
• [27]Foissner W: Colpodea (Ciliophora). Stuttgart, Jena, New York: Gustav Fisher Verlag; 1993.
• [28]Corliss JO: Silver impregnation of ciliated protozoa by the Chatton-Lwoff technique. Stain Technol 1953, 28:97-100.
• [29]Modeo L, Rosati G, Andreoli I, Gabrielli G, Verni F, Petroni G: Molecular systematics and ultrastructural characterization of a forgotten species: Chattonidium setense (Ciliophora, Heterotrichea). Proc Jpn Acad B Phys 2006, 82:359-374.
• [30]Finlay BJ, Fenchel T: Hydrogenosomes in some anaerobic protozoa resemble mitochondria. FEMS Microbiol Lett 1989, 65:311-314.
• [31]Finlay BJ, Fenchel T: An aerobic protozoon, with symbiotic methanogens, living in municipal landfill material. FEMS Microbiol Ecol 1991, 85:169-180.
• [32]Ferrantini F, Fokin SI, Modeo L, Andreoli I, Dini F, Görtz H-D, Verni F, Petroni G: “Candidatus Cryptoprodotis polytropus”, a novel Rickettsia-like organism in the ciliated protist Pseudomicrothorax dubius (Ciliophora, Nassophorea). J Eukaryot Microbiol 2009, 56:119-129.
• [33]Amann RI, Krumholz I, Stahl DA: Fluorescent oligonucleotide probing of whole cells for determinative, phylogenetic, and environmental studies in microbiology. J Bacteriol 1990, 172:716-770.
• [34]Stahl DA, Amann R: Development and application of nucleic acid probes. In Nucleic acid techniques in bacterial systematics. Edited by Stackebrandt E, Goodfellow M. Chichester, United Kingdom: John Wiley & Sons Ltd; 1991:205-248.
• [35]Medlin L, Elwood HJ, Stickel S, Sogin ML: The characterization of enzymatically amplified 16S-like rRNA-coding regions. Gene 1988, 71:491-499.
• [36]Petroni G, Dini F, Verni F, Rosati G: A molecular approach to the tangled intrageneric relationships underlying phylogeny in Euplotes (Ciliophora, Spirotrichea). Mol Phylogenet Evol 2002, 22:118-130.
• [37]Rosati G, Modeo L, Melai M, Petroni G, Verni F: A multidisciplinary approach to describe protists: a morphological, ultrastructural, and molecular study on Peritromus kahli Villeneuve-Brachon, 1940 (Ciliophora, Heterotrichea). J Eukaryot Microbiol 2004, 51:49-59.
• [38]Pruesse E, Quast C, Knittel K, Fuchs B, Ludwig W, Peplies J, Glöckner FO: SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucleic Acids Res 2007, 35:7188-7196.
• [39]Ludwig W, Strunk O, Westram R, Richter L, Meier H, Yadhukumar , Buchner A, Lai T, Steppi S, Jobb G, Förster W, Brettske I, Gerber S, Ginhart AW, Gross O, Grumann S, Hermann S, Jost R, König A, Liss T, Grumann S, Hermann S, Jost R, König A, Liss T, Lüßmann R, May M, Nonhoff B, Reichel B, Strehlow R, Stamatakis A, Stuckmann N, Vilbig A, Lenke M, Ludwig T, Bode A, Schleifer KH: ARB: a software environment for sequence data. Nucleic Acids Res 2004, 32:1363-1371.
• [40]Guindon S, Gascuel O: A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 2003, 52:696-704.
• [41]Posada D: jModelTest: phylogenetic model averaging. Mol Biol Evol 2008, 25:1253-1256.
• [42]Schmidt HA, Strimmer K, Vingron M, von Haeseler A: TREE-PUZZLE: Maximum likelihood phylogenetic analysis using quartets and parallel computing. Bioinformatics 2002, 18:502-504.
• [43]Huelsenbeck JP, Ronquist F: MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 2001, 17:754-755.
• [44]Small EB, Lynn DH: An illustrated guide to the Protozoa. Edited by Lee JJ, Hutner SH, Bovee EC. Kansas, USA: Society of Protozoologists, Lawrence; 1985:393-575.
• [45]Al-Rasheid KAS: New records of interstitial ciliates (Protozoa, Ciliophora) from the Saudi coasts of the Red Sea. Trop Zool 2001, 14:133-156.
• [46]Fenchel T, Perry T, Thane A: Anaerobiosis and symbiosis with bacteria in free-living ciliates. J Protozool 1977, 24:154-163.
• [47]Berger J, Lynn DH: Somatic and oral cortical ultrastructure of the plagiopylid ciliates Lechriopyla mystax Lynch, 1930 and Plagiopyla minuta Powers, 1933. J Protozool 1984, 31:433-443.
• [48]Berger J, Lynn DH: Hydrogenosomes-methanogen assemblages in the echinoid endocommensal plagiopylid ciliates, Lechriopyla mystax Lynch, 1930 and Plagiopyla minuta Powers, 1933. J Protozool 1992, 39:4-8.
• [49]Embley TM, Finlay BJ: The use of small subunit rRNA sequences to unravel the relationships between anaerobic ciliates and their methanogen endosymbionts. Microbiology 1994, 140:225-235.
• [50]Fenchel T, Finlay BJ: The biology of free-living anaerobic ciliates. Eur J Protistol 1991, 26:201-215.
• [51]Fenchel T, Finlay BJ: Synchronous division of an endosymbiotic methanogenic bacterium in the anaerobic ciliate Plagiopyla frontata Kahl. J Protozool 1991, 38:22-28.
• [52]Goosen NK, Horemans AMC, Hillebrand SJW, Stumm CK, Vogels GD: Cultivation of the sapropelic ciliate Plagiopyla nasuta Stein and isolation of the endosymbiont Methanobacterium formicicum. Arch Microbiol 1988, 150:165-170.
• [53]de Puytorac P, Groliére JC, Detcheva R, Grain J: Observations sur l’ultrastructure du cilié Vestibulifera, Plagiopyla nasuta Stein, 1860. Ann Sci Nat Zool 1985, 7:189-198. in French with English summary
• [54]Detcheva R, de Puytorac P, Grolière CA: Some ultrastructural characteristics of the polysaprobic ciliate Trimyema compressum. Trans Am Microsc Soc 1981, 100:65-73.
• [55]Finlay BJ, Embley TM, Fenchel T: A new polymorphic methanogen, closely related to Methanocorpusculum parvum, living in stable symbiosis within the anaerobic ciliate Trimyema sp. J Gen Microbiol 1993, 139:371-378.
• [56]Rinke C, Schmitz-Esser S, Stoecker K, Nussbaumer AD, Molnár DA, Vanura K, Wagner M, Horn M, Ott JA, Bright M: “Candidatus Thiobios zoothamnicoli”, an ectosymbiotic bacterium covering the giant marine ciliate Zoothamnium niveum. Appl Environ Microbiol 2006, 72:2014-2021.
• [57]Rosati G: Epixenosomes: symbionts of the hypotrich ciliate Euplotidium itoi. Symbiosis 1999, 26:1-23.
• [58]Modeo L, Petroni G, Lobban CS, Verni F, Vannini C: Morphological, ultrastructural, and molecular characterization of Euplotidium rosati n. sp. (Ciliophora, Euplotida) from Guam. J Eukaryot Microbiol 2013, 60:25-36.
• [59]Breglia SA, Yubuki N, Hoppenrath M, Leander BS: Ultrastructure and molecular phylogenetic position of a novel euglenozoan with extrusive epysimbiotic bacteria: Bihospites bacati n. gen. et sp. (Symbiontida). BMC Microbiol 2010, 10:145. BioMed Central Full Text
• [60]Yubuki N, Edgcomb VP, Bernhard JM, Leander BS: Ultrastructure and molecular phylogeny of Calkinsia aureus: cellular identity of a novel clade of deep-sea euglenozoans with epibiotic bacteria. BMC Microbiol 2009, 9:16. BioMed Central Full Text
• [61]Simpson AGB, van Den Hoff J, Bernard C, Burton HR, Patterson DJ: The ultrastructure and systematic position of the euglenozoon Postgaardi mariagerensis, Fenchel et al. Arch Protistenkd 1996, 147:213-225.
• [62]Fokin SI: Frequency and biodiversity of symbionts in representatives of the main classes of Ciliophora. Eur J Protistol 2012, 48:138-148.
• [63]Fokin SI, Modeo L, Andreoli I, Ferrantini F, Verni F, Petroni G: Rare ciliate species (Ciliophora, Protista) revealed from brackish water habitats with oxygen deficiency. Paris, Book of Abstracts: International Congress of Zoology; 2008:31.
• [64]Hausmann K: Extrusive organelles in Protists. Int Rev Cytol 1978, 52:197-276.
• [65]Rosati G, Modeo L: Extrusomes in ciliates: diversification, distribution, and phylogenetic implications. J Eukaryot Microbiol 2003, 50:383-402.
• [66]Broers CAM, Stumm CK, Vogels GD: Axenic cultivation of the anaerobic free-living ciliate Trimyema compressum. J Protozool 1991, 38:507-511.
• [67]Benchimol M: Hydrogenosomes under microscopy. Tissue Cell 2009, 41:151-168.
• [68]Embley TM, Martin W: Eukaryotic evolution, changes and challenges. Nature 2006, 30:623-630.
• [69]Müller M: The hydrogenosomes. J Gen Microbiol 1993, 139:2235-2241.
• [70]Van der Giezen M: Hydrogenosomes and mitosomes: conservation and evolutions of functions. J Eukaryot Microbiol 2009, 56:221-231.
• [71]Finlay BJ, Clarke KJ, Vicente E, Miracle MR: Anaerobic ciliates from a sulphide-rich solution lake in Spain. Eur J Protistol 1991, 27:148-159.
• [72]Clarke KJ, Finlay BJ, Esteban G, Guhl BE, Embley TM: Cyclidium porcatum n. sp.: a free-living anaerobic scuticociliate containing a stable complex of hydrogenosomes, eubacteria and archeobacteria. Eur J Protistol 1993, 29:262-270.
• [73]Fokin SI: Morphological diversity of the micronuclei in Paramecium. Arch Protistenkd 1997, 148:376-387.
• [74]Behnke A, Barger KJ, Bunge J, Stoeck T: Spatio-temporal variations in protistan communities along an O2/H2S gradient in the anoxic Framvaren Fjord (Norway). FEMS Microbiol Ecol 2010, 72:89-102.
• [75]Behnke A, Bunge J, Barger K, Breiner HW, Alla V, Stoeck T: Microeukaryote community patterns along an O2/H2S gradient in a supersulfidic anoxic fjord (Framvaren, Norway). Appl Environ Microbiol 2006, 72:3626-3636.
• [76]Carey PG: Marine interstitial ciliates. An illustrated key. London, New York: Chapman & Hall; 1992.
• [77]International Commission on Zoological Nomenclature (ICZN): International Code of Zoological Nomenclature. London: International Trust For Zoological Numenclature; 1999.
• [78]Foissner W: Neotypification of protists, especially ciliates (Protozoa, Ciliophora). Bull Zool Nom 2002, 59:165-169.
• [79]Finlay BJ, Corliss JO, Esteban GF, Fenchel T: Biodiversity at the microbial level: the number of free-living ciliates in the biosphere. Q Rev Biol 1996, 71:221-237.