Prokaryotic Cells in the Hydrothermal Vent Tube Worm
            <i>Riftia pachyptila</i>
            Jones: Possible Chemoautotrophic Symbionts

Cavanaugh, Colleen M.; Gardiner, Stephen L.; Jones, Meredith L.; Jannasch, Holger W.; Waterbury, John

doi:10.1126/science.213.4505.340

Cited by 628 publications

(324 citation statements)

References 26 publications

Supporting

Mentioning

313

Contrasting

Unclassified

Order By: Relevance

“…Since the first discovery of a dense, unique and diverse ecosystem in deep-sea hydrothermal vents in 1977 (Corliss et al, 1979), many studies have shown that deep-sea vent invertebrates such as tubeworms and Bathymodiolus mussels are sustained nutritionally by intracellular symbiotic bacteria (endosymbionts) as primary producers (Cavanaugh et al, 1981(Cavanaugh et al, , 1987Felbeck, 1981;Childress et al, 1986). In addition, several species of deep-sea vent invertebrates harbour bacteria (epibionts) that colonize the surfaces of specialized tissues such as the dorsal setae of the polychaete Alvinella pompejana, the gill chambers of the shrimp Rimicaris exoculata and the setae of the galatheid crabs Shinkaia crosnieri, Kiwa hirsuta and K. puravida (Polz and Cavanaugh, 1995;Cary et al, 1997;Goffredi et al, 2008;Watsuji et al, 2010;Thurber et al, 2011).…”

Section: Introductionmentioning

confidence: 99%

Molecular evidence of digestion and absorption of epibiotic bacterial community by deep-sea crab Shinkaia crosnieri

et al. 2014

View full text Add to dashboard Cite

The hydrothermal vent crab Shinkaia crosnieri is considered to obtain nutrition from the epibiotic bacteria found on the setae, but previous studies have not shown how nutrients can be transferred from the epibionts to the host. In this study, microscopic observations of S. crosnieri intestinal components detected autofluorescent setae fragments and pigmentation derived from the digestion of epibionts in a dye-stained epibiont tracer experiment. An in vitro digestion experiment with epibiotic populations using an intestinal extract demonstrated the degradation of epibiotic cells by digestive enzymes. A phylogenetic analysis showed that many of the bacterial 16S ribosomal RNA gene sequences obtained from the intestine were closely related to the sequences of the epibionts, thus they were probably derived from the epibionts. A stable isotope tracer experiment also indicated that 13 C assimilated by the epibionts provided a carbon (nutrition) source for the host. Both activity measurements and isotope studies showed that chemosynthetic metabolism by the gut microbial components were inactive. Together with the feeding behaviour of living S. crosnieri, these results indicate that S. crosnieri ingests the epibionts using maxillipeds and assimilates them via its digestive organs as a nutrient source. The results of this study elucidate the mechanism of nutritional transfer in ectosymbiosis between chemosynthetic bacteria and deep-sea invertebrates.

show abstract

Section: Introductionmentioning

confidence: 99%

Molecular evidence of digestion and absorption of epibiotic bacterial community by deep-sea crab Shinkaia crosnieri

et al. 2014

View full text Add to dashboard Cite

show abstract

“…Substrates for bacterial chemosynthesis, that is, oxygen, sulfide and carbon dioxide, are taken up from the diffuse flow fluids through the worm's plume and delivered to the symbionts, which are enclosed in specialized host cells (bacteriocytes) in an organ termed trophosome (Hand, 1987;Bright and Sorgo, 2003). Bacterial sulfide oxidation provides the energy that fuels CO 2 fixation into organic matter (Cavanaugh et al, 1981;Felbeck, 1981;Felbeck and Somero, 1982;Fisher and Childress, 1984;Childress et al, 1991;Girguis and Childress, 2006). With the publication of its metagenome (Robidart et al, 2008), the name Candidatus Endoriftia persephone was proposed for the Riftia symbiont.…”

Section: Introductionmentioning

confidence: 99%

Physiological homogeneity among the endosymbionts of Riftia pachyptila and Tevnia jerichonana revealed by proteogenomics

et al. 2011

View full text Add to dashboard Cite

The two closely related deep-sea tubeworms Riftia pachyptila and Tevnia jerichonana both rely exclusively on a single species of sulfide-oxidizing endosymbiotic bacteria for their nutrition. They do, however, thrive in markedly different geochemical conditions. A detailed proteogenomic comparison of the endosymbionts coupled with an in situ characterization of the geochemical environment was performed to investigate their roles and expression profiles in the two respective hosts. The metagenomes indicated that the endosymbionts are genotypically highly homogeneous. Gene sequences coding for enzymes of selected key metabolic functions were found to be 99.9% identical. On the proteomic level, the symbionts showed very consistent metabolic profiles, despite distinctly different geochemical conditions at the plume level of the respective hosts. Only a few minor variations were observed in the expression of symbiont enzymes involved in sulfur metabolism, carbon fixation and in the response to oxidative stress. Although these changes correspond to the prevailing environmental situation experienced by each host, our data strongly suggest that the two tubeworm species are able to effectively attenuate differences in habitat conditions, and thus to provide their symbionts with similar micro-environments.

show abstract

“…Attempts to detect tube worm symbionts in host eggs and larvae by the use of microscopy and PCR have been unsuccessful (4)(5)(6)12), suggesting that transmission does not occur vertically. Furthermore, most vent vestimentiferan species host symbionts that share identical 16S rRNA sequences, which is also consistent with the hypothesis of environmental transmission (14,22).…”

mentioning

confidence: 99%

Free-Living Tube Worm Endosymbionts Found at Deep-Sea Vents

Harmer

Rotjan

Nussbaumer

et al. 2008

Appl Environ Microbiol

Self Cite

View full text Add to dashboard Cite

Recent evidence suggests that deep-sea vestimentiferan tube worms acquire their endosymbiotic bacteria from the environment each generation; thus, free-living symbionts should exist. Here, free-living tube worm symbiont phylotypes were detected in vent seawater and in biofilms at multiple deep-sea vent habitats by PCR amplification, DNA sequence analysis, and fluorescence in situ hybridization. These findings support environmental transmission as a means of symbiont acquisition for deep-sea tube worms.

show abstract

Prokaryotic Cells in the Hydrothermal Vent Tube Worm Riftia pachyptila Jones: Possible Chemoautotrophic Symbionts

Abstract: The existence of a symbiotic association between vestimentiferan tube worms from deep-sea hydrothermal vents and chemoautotrophic sulfur-oxidizing prokaryotes, based on histological and enzymatic evidence, is suggested.

Cited by 628 publications

References 26 publications

Molecular evidence of digestion and absorption of epibiotic bacterial community by deep-sea crab Shinkaia crosnieri

Molecular evidence of digestion and absorption of epibiotic bacterial community by deep-sea crab Shinkaia crosnieri

Physiological homogeneity among the endosymbionts of Riftia pachyptila and Tevnia jerichonana revealed by proteogenomics

Free-Living Tube Worm Endosymbionts Found at Deep-Sea Vents

Contact Info

Product

Resources

About