1887

Abstract

This paper reports the identification of bacterial endosymbionts that inhabit the cytoplasm of the marine ciliated protozoon . Ultrastructural and full-cycle rRNA approaches were used to reveal the identity of these bacteria. Based on analysis of 16S rRNA gene sequences, evolutionary trees were constructed; these placed the endosymbiont in the genus in the -. The validity of this finding was also shown by fluorescence hybridization with a -specific oligonucleotide probe. Differences at the 16S rRNA gene level (which allowed the construction of a species-specific oligonucleotide probe) and the peculiar habitat indicate that the endosymbiont represents a novel species. As its cultivation has not been successful to date, the provisional name ‘ Devosia euplotis' is proposed. The species- and group-specific probes designed in this study could represent convenient tools for the detection of ‘ Devosia euplotis' and -like bacteria in the environment.

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2004-07-01
2021-04-11
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References

  1. Amann R., Schleifer K.-H. 2001; Nucleic acid probes and their application in environmental microbiology. In Bergey's Manual of Systematic Bacteriology , 2nd edn. pp  67–82 Edited by Boone D. R., Castenholz R. W., Garrity G. M. New York: Springer;
    [Google Scholar]
  2. Amann R. I., Krumholz L., Stahl D. A. 1990; Fluorescent-oligonucleotide probing of whole cells for determinative, phylogenetic, and environmental studies in microbiology. J Bacteriol 172:762–770
    [Google Scholar]
  3. Amann R., Springer N., Ludwig W., Görtz H.-D., Schleifer K.-H. 1991; Identification in situ and phylogeny of uncultured bacterial endosymbionts. Nature 351:161–164 [CrossRef]
    [Google Scholar]
  4. Amann R. I., Ludwig W., Schleifer K. H. 1995; Phylogenetic identification and in situ detection of individual microbial cells without cultivation. Microbiol Rev 59:143–169
    [Google Scholar]
  5. Beier C. L., Horn M., Michel R., Schweikert M., Görtz H.-D., Wagner M. 2002; The genus Caedibacter comprises endosymbionts of Paramecium spp. related to the Rickettsiales ( Alphaproteobacteria ) and to Francisella tularensis ( Gammaproteobacteria ). Appl Environ Microbiol 68:6043–6050 [CrossRef]
    [Google Scholar]
  6. Dini F., Nyberg D. 1994; Adolescence and the reversibility of maturity in Euplotes crassus . J Eukaryot Microbiol 41:373–380 [CrossRef]
    [Google Scholar]
  7. Don R. H., Cox P. T., Wainwright B. J., Baker K., Mattick J. S. 1991; ‘Touchdown’ PCR to circumvent spurious priming during gene amplification. Nucleic Acids Res 19:4008 [CrossRef]
    [Google Scholar]
  8. Gromov B. V., Ossipov D. V. 1981; Holospora ( ex Hafkine 1890) nom. rev., a genus of bacteria inhabiting the nuclei of paramecia. Int J Syst Bacteriol 31:348–352 [CrossRef]
    [Google Scholar]
  9. Görtz H.-D. 2002; Symbiotic associations between ciliates and prokaryotes. In The Prokaryotes: an Evolving Electronic Resource for the Microbiological Community , 3rd edn. http://141.150.157.117:8080/prokPUB/chaprender/jsp/showchap.jsp?chapnum=355
    [Google Scholar]
  10. Heckmann K., Schmidt H. J. 1987; Polynucleobacter necessarius gen. nov., sp. nov., an obligately endosymbiotic bacterium living in the cytoplasm of Euplotes aediculatus . Int J Syst Bacteriol 37:456–457 [CrossRef]
    [Google Scholar]
  11. Heckmann K., den Hagen R., Görtz H. D. 1983; Fresh-water Euplotes species with a 9 type 1 cirrus pattern depend upon endosymbionts. J Protozool 30:284–289 [CrossRef]
    [Google Scholar]
  12. Ludwig W., Strunk O. 1997 arb: a software environment for sequence data http://www.arb-home.de/
  13. Ludwig W., Klenk H.-P. 2001; Overview: a phylogenetic backbone and taxonomic framework for procaryotic systematics. In Bergey's Manual of Systematic Bacteriology , 2nd edn. pp  49–65 Edited by Boone D. R., Castenholz R. W., Garrity G. M. New York: Springer;
    [Google Scholar]
  14. Ludwig W., Amann R., Martinez-Romero E., Schönhuber W., Bauer S., Neef A., Schleifer K.-H. 1998a; rRNA based identification and detection systems for rhizobia and other bacteria. Plant Soil 204:1–19 [CrossRef]
    [Google Scholar]
  15. Ludwig W., Strunk O., Klugbauer S., Klugbauer N., Weizenegger M., Neumaier J., Bachleitner M., Schleifer K. H. 1998b; Bacterial phylogeny based on comparative sequence analysis. Electrophoresis 19:554–568 [CrossRef]
    [Google Scholar]
  16. Manz W., Amann R. I., Ludwig W., Wagner M., Schleifer K. H. 1992; Phylogenetic oligodeoxynucleotide probes for the major subclasses of proteobacteria: problems and solutions. Syst Appl Microbiol 15:593–600 [CrossRef]
    [Google Scholar]
  17. Medlin L., Elwood H. J., Stickel S., Sogin M. L. 1988; The characterization of enzymatically amplified eukaryotic 16S-like rRNA-coding regions. Gene 71:491–499 [CrossRef]
    [Google Scholar]
  18. Modeo L., Petroni G., Rosati G., Montagnes D. J. 2003; A multidisciplinary approach to describe protists: redescriptions of Novistrombidium testaceum Anigstein 1914 and Strombidium inclinatum Montagnes, Taylor, and Lynn 1990 (Ciliophora, Oligotrichia). J Eukaryot Microbiol 50:175–189 [CrossRef]
    [Google Scholar]
  19. Murray R. G. E., Schleifer K. H. 1994; Taxonomic notes: a proposal for recording the properties of putative taxa of procaryotes. Int J Syst Bacteriol 44:174–176 [CrossRef]
    [Google Scholar]
  20. Murray R. G. E., Stackebrandt E. 1995; Taxonomic note: implementation of the provisional status Candidatus for incompletely described procaryotes. Int J Syst Bacteriol 45:186–187 [CrossRef]
    [Google Scholar]
  21. Nakagawa Y., Sakane T., Yokota A. 1996; Transfer of “ Pseudomonas riboflavina ” (Foster 1944), a gram-negative, motile rod with long-chain 3-hydroxy fatty acids, to Devosia riboflavina gen. nov., sp. nov., nom. rev. Int J Syst Bacteriol 46:16–22 [CrossRef]
    [Google Scholar]
  22. Nobili R., Rosati G., Verni F. 1976 The killer trait in Euplotes crassus (Ciliata, Hypotrichida) Boll Zool 43:251–258 [CrossRef]
    [Google Scholar]
  23. Petroni G., Spring S., Schleifer K. H., Verni F., Rosati G. 2000; Defensive extrusive ectosymbionts of Euplotidium (Ciliophora) that contain microtubule-like structures are bacteria related to Verrucomicrobia . Proc Natl Acad Sci U S A 97:1813–1817 [CrossRef]
    [Google Scholar]
  24. Petroni G., Dini F., Verni F., Rosati G. 2002; A molecular approach to the tangled intrageneric relationships underlying phylogeny in Euplotes (Ciliophora, Spirotrichea). Mol Phylogenet Evol 22:118–130 [CrossRef]
    [Google Scholar]
  25. Petroni G., Rosati G., Vannini C., Modeo L., Dini F., Verni F. 2003; In situ identification by fluorescently labeled oligonucleotide probes of morphologically similar, closely related ciliate species. Microb Ecol 45:156–162 [CrossRef]
    [Google Scholar]
  26. Preer J. R. Jr, Preer L. B. 1982; Revival of names of protozoan endosymbionts and proposal of Holospora caryophila nom. nov. Int J Syst Bacteriol 32:140–141 [CrossRef]
    [Google Scholar]
  27. Preer J. R. Jr, Preer L. B., Jurand A. 1974; Kappa and other endosymbionts in Paramecium aurelia . Bacteriol Rev 38:113–163
    [Google Scholar]
  28. Quackenbush R. L. 1982; Pseudocaedibacter gen. nov. In Validation of the Publication of New Names and New Combinations Previously Effectively Published Outside the IJSB List no: 8 Int J Syst Bacteriol 32:266–268 [CrossRef]
    [Google Scholar]
  29. Rivas R., Velázquez E., Willems A., Vizcaíno N., Subba-Rao N. S., Mateos P. F., Gillis M., Dazzo F. B., Martínez-Molina E. 2002; A new species of Devosia that forms a unique nitrogen-fixing root-nodule symbiosis with the aquatic legume Neptunia natans (L.f.) Druce. Appl Environ Microbiol 68:5217–5222 [CrossRef]
    [Google Scholar]
  30. Rivas R., Willems A., Subba-Rao N. S., Mateos P. F., Dazzo F. B., Kroppenstedt R. M., Martínez-Molina E., Gillis M., Velázquez E. 2003; Description of Devosia neptuniae sp. nov. that nodulates and fixes nitrogen in symbiosis with Neptunia natans , an aquatic legume from India. Syst Appl Microbiol 26:47–53 [CrossRef]
    [Google Scholar]
  31. Rosati G., Verni F., Luporini P. 1976; Cytoplasmic bacteria-like endosymbionts in Euplotes crassus (Dujardin) (Ciliata Hypotrichida. Monit Zool Ital 10:449–460
    [Google Scholar]
  32. Rosati G., Modeo L., Melai M., Petroni G., Verni F. 2004; A multidisciplinary approach to describe protists: a morphological, ultrastructural, and molecular study on Peritromus kahli Villeneuve-Brachon, 1940 (Ciliophora, Heterotrichea). J Eukaryot Microbiol 51:49–59 [CrossRef]
    [Google Scholar]
  33. Rosselló-Mora R., Amann R. 2001; The species concept for prokaryotes. FEMS Microbiol Rev 25:39–67 [CrossRef]
    [Google Scholar]
  34. Springer N., Ludwig W., Amann R., Schmidt H. J., Görtz H.-D., Schleifer K.-H. 1993; Occurrence of fragmented 16S rRNA in an obligate bacterial endosymbiont of Paramecium caudatum . Proc Natl Acad Sci U S A 90:9892–9895 [CrossRef]
    [Google Scholar]
  35. Springer N., Amann R., Ludwig W., Schleifer K.-H., Schmidt H. 1996; Polynucleobacter necessarius , an obligate bacterial endosymbiont of the hypotrichous ciliate Euplotes aediculatus , is a member of the β -subclass of Proteobacteria. FEMS Microbiol Lett 135:333–336
    [Google Scholar]
  36. Stackebrandt E. 2000; Defining taxonomic ranks. In The Prokaryotes: an Evolving Electronic Resource for the Microbiological Community , 3rd edn. http://141.150.157.117:8080/prokPUB/chaprender/jsp/showchap.jsp?chapnum=240
    [Google Scholar]
  37. Stahl D. A., Amann R. 1991; Development and application of nucleic acid probes. In Nucleic Acid Techniques in Bacterial Systematics pp  205–248 Edited by Stackebrandt E., Goodfellow M. Chichester, UK: Wiley;
    [Google Scholar]
  38. Wisotzkey J. D., Jurtshuk P. Jr, Fox G. E. 1990; PCR amplification of 16S rDNA from lyophilized cell cultures facilitates studies in molecular systematics. Curr Microbiol 21:325–327 [CrossRef]
    [Google Scholar]
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