Skip to main content
PMC home page
Applied and Environmental Microbiology logoLink to Applied and Environmental Microbiology
. 1995 Jun;61(6):2346–2350. doi: 10.1128/aem.61.6.2346-2350.1995

Characterization of chemoautotrophic bacterial symbionts in a gutless marine worm Oligochaeta, Annelida) by phylogenetic 16S rRNA sequence analysis and in situ hybridization.

N Dubilier 1, O Giere 1, D L Distel 1, C M Cavanaugh 1
PMCID: PMC167506  PMID: 7793955

Abstract

The phylogenetic relationships of chemoautotrophic endosymbionts in the gutless marine oligochaete Inanidrilus leukodermatus to chemoautotrophic ecto- and endosymbionts from other host phyla and to free-living bacteria were determined by comparative 16S rRNA sequence analysis. Fluorescent in situ hybridization confirmed that the 16S rRNA sequence obtained from these worms originated from the symbionts. The symbiont sequence is unique to I. leukodermatus. In phylogenetic trees inferred by both distance and parsimony methods, the oligochaete symbiont is peripherally associated with one of two clusters of chemoautotrophic symbionts that belong to the gamma subdivision of the Proteobacteria. The endosymbionts of this oligochaete form a monophyletic group with chemoautotrophic ectosymbionts of a marine nematode. The oligochaete and nematode symbionts are very closely related, although their hosts belong to separate, unrelated animal phyla. Thus, cospeciation between the nematode and oligochaete hosts and their symbionts could not have occurred. Instead, the similar geographic locations and habitats of the hosts may have influenced the establishment of these symbioses.

Full Text

The Full Text of this article is available as a PDF (970.4 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Altschul S. F., Gish W., Miller W., Myers E. W., Lipman D. J. Basic local alignment search tool. J Mol Biol. 1990 Oct 5;215(3):403–410. doi: 10.1016/S0022-2836(05)80360-2. [DOI] [PubMed] [Google Scholar]
  2. Amann R. I., Krumholz L., Stahl D. A. Fluorescent-oligonucleotide probing of whole cells for determinative, phylogenetic, and environmental studies in microbiology. J Bacteriol. 1990 Feb;172(2):762–770. doi: 10.1128/jb.172.2.762-770.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bandi C., Damiani G., Magrassi L., Grigolo A., Fani R., Sacchi L. Flavobacteria as intracellular symbionts in cockroaches. Proc Biol Sci. 1994 Jul 22;257(1348):43–48. doi: 10.1098/rspb.1994.0092. [DOI] [PubMed] [Google Scholar]
  4. Cavanaugh C. M., Gardiner S. L., Jones M. L., Jannasch H. W., Waterbury J. B. Prokaryotic Cells in the Hydrothermal Vent Tube Worm Riftia pachyptila Jones: Possible Chemoautotrophic Symbionts. Science. 1981 Jul 17;213(4505):340–342. doi: 10.1126/science.213.4505.340. [DOI] [PubMed] [Google Scholar]
  5. Distel D. L., Lane D. J., Olsen G. J., Giovannoni S. J., Pace B., Pace N. R., Stahl D. A., Felbeck H. Sulfur-oxidizing bacterial endosymbionts: analysis of phylogeny and specificity by 16S rRNA sequences. J Bacteriol. 1988 Jun;170(6):2506–2510. doi: 10.1128/jb.170.6.2506-2510.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Kojima S., Hashimoto T., Hasegawa M., Murata S., Ohta S., Seki H., Okada N. Close phylogenetic relationship between Vestimentifera (tube worms) and Annelida revealed by the amino acid sequence of elongation factor-1 alpha. J Mol Evol. 1993 Jul;37(1):66–70. doi: 10.1007/BF00170463. [DOI] [PubMed] [Google Scholar]
  7. Maidak B. L., Larsen N., McCaughey M. J., Overbeek R., Olsen G. J., Fogel K., Blandy J., Woese C. R. The Ribosomal Database Project. Nucleic Acids Res. 1994 Sep;22(17):3485–3487. doi: 10.1093/nar/22.17.3485. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. McDowell E. M., Trump B. F. Histologic fixatives suitable for diagnostic light and electron microscopy. Arch Pathol Lab Med. 1976 Aug;100(8):405–414. [PubMed] [Google Scholar]
  9. Ochman H., Wilson A. C. Evolution in bacteria: evidence for a universal substitution rate in cellular genomes. J Mol Evol. 1987;26(1-2):74–86. doi: 10.1007/BF02111283. [DOI] [PubMed] [Google Scholar]
  10. Pinkel D., Landegent J., Collins C., Fuscoe J., Segraves R., Lucas J., Gray J. Fluorescence in situ hybridization with human chromosome-specific libraries: detection of trisomy 21 and translocations of chromosome 4. Proc Natl Acad Sci U S A. 1988 Dec;85(23):9138–9142. doi: 10.1073/pnas.85.23.9138. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Polz M. F., Distel D. L., Zarda B., Amann R., Felbeck H., Ott J. A., Cavanaugh C. M. Phylogenetic analysis of a highly specific association between ectosymbiotic, sulfur-oxidizing bacteria and a marine nematode. Appl Environ Microbiol. 1994 Dec;60(12):4461–4467. doi: 10.1128/aem.60.12.4461-4467.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Spurr A. R. A low-viscosity epoxy resin embedding medium for electron microscopy. J Ultrastruct Res. 1969 Jan;26(1):31–43. doi: 10.1016/s0022-5320(69)90033-1. [DOI] [PubMed] [Google Scholar]
  13. Woese C. R. Bacterial evolution. Microbiol Rev. 1987 Jun;51(2):221–271. doi: 10.1128/mr.51.2.221-271.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Zharkikh A., Li W. H. Statistical properties of bootstrap estimation of phylogenetic variability from nucleotide sequences. I. Four taxa with a molecular clock. Mol Biol Evol. 1992 Nov;9(6):1119–1147. doi: 10.1093/oxfordjournals.molbev.a040782. [DOI] [PubMed] [Google Scholar]

Articles from Applied and Environmental Microbiology are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES