This Article
Right arrow Full Text
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrowReprints and Permissions
Right arrow Copyright Information
Right arrow Books from ASM Press
Right arrow MicrobeWorld
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Suzuki, Y.
Right arrow Articles by Horikoshi, K.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Suzuki, Y.
Right arrow Articles by Horikoshi, K.
Agricola
Right arrow Articles by Suzuki, Y.
Right arrow Articles by Horikoshi, K.

 Previous Article  |  Next Article 

Applied and Environmental Microbiology, September 2005, p. 5440-5450, Vol. 71, No. 9
0099-2240/05/$08.00+0     doi:10.1128/AEM.71.9.5440-5450.2005
Copyright © 2005, American Society for Microbiology. All Rights Reserved.

Novel Chemoautotrophic Endosymbiosis between a Member of the Epsilonproteobacteria and the Hydrothermal-Vent Gastropod Alviniconcha aff. hessleri (Gastropoda: Provannidae) from the Indian Ocean{dagger}

Yohey Suzuki,1* Takenori Sasaki,2 Masae Suzuki,1 Yuichi Nogi,1 Tetsuya Miwa,1 Ken Takai,1 Kenneth H. Nealson,1,3 and Koki Horikoshi1

Frontier Research System for Extremophiles, Japan Agency for Marine-Earth Science and Technology, 2-15 Natsushima-cho, Yokosuka 237-0061, Japan,1 Department of Historical Geology and Paleontology, The University Museum, The University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo 113-0033, Japan,2 Department of Earth Sciences, University of Southern California, 3651 Trousdale Parkway, Los Angeles, California 90089-07403

Received 8 December 2004/ Accepted 21 March 2005

The hydrothermal-vent gastropod Alviniconcha aff. hessleri from the Kairei hydrothermal field on the Central Indian Ridge houses bacterium-like cells internally in its greatly enlarged gill. A single 16S rRNA gene sequence was obtained from the DNA extract of the gill, and phylogenetic analysis placed the source organism within a lineage of the epsilon subdivision of the Proteobacteria. Fluorescence in situ hybridization analysis with an oligonucleotide probe targeting the specific epsilonproteobacterial subgroup showed the bacterium densely colonizing the gill filaments. Carbon isotopic homogeneity among the gastropod tissue parts, regardless of the abundance of the endosymbiont cells, suggests that the carbon isotopic composition of the endosymbiont biomass is approximately the same as that of the gastropod. Compound-specific carbon isotopic analysis revealed that fatty acids from the gastropod tissues are all 13C enriched relative to the gastropod biomass and that the monounsaturated C16 fatty acid that originates from the endosymbiont is as 13C enriched relative to the gastropod biomass as that of the epsilonproteobacterial cultures grown under chemoautotrophic conditions. This fractionation pattern is most likely due to chemoautotrophy based on the reductive tricarboxylic-acid (rTCA) cycle and subsequent fatty acid biosynthesis from 13C-enriched acetyl coenzyme A. Enzymatic characterization revealed evident activity of several key enzymes of the rTCA cycle, as well as the absence of ribulose-1,5-bisphosphate carboxylase/oxygenase activity in the gill tissue. The results from anatomic, molecular phylogenetic, bulk and compound-specific carbon isotopic, and enzymatic analyses all support the inference that a novel nutritional strategy relying on chemoautotrophy in the epsilonproteobacterial endosymbiont is utilized by the hydrothermal-vent gastropod from the Indian Ocean. The discrepancies between the data of the present study and those of previous ones for Alviniconcha gastropods from the Pacific Ocean imply that at least two lineages of chemoautotrophic bacteria, phylogenetically distinct at the subdivision level, occur as the primary endosymbiont in one host animal type.

* Corresponding author. Mailing address: Frontier Research System for Extremophiles, Japan Agency for Marine-Earth Science and Technology, 2-15 Natsushima-cho, Yokosuka 237-0061, Japan. Phone: 81-468-67-9710. Fax: 81-468-67-9715. E-mail: yohey{at}jamstec.go.jp.

{dagger} Supplemental material for this article may be found at http://aem.asm.org/.

Applied and Environmental Microbiology, September 2005, p. 5440-5450, Vol. 71, No. 9
0099-2240/05/$08.00+0     doi:10.1128/AEM.71.9.5440-5450.2005
Copyright © 2005, American Society for Microbiology. All Rights Reserved.



This article has been cited by other articles:

  • Nakagawa, S., Takaki, Y., Shimamura, S., Reysenbach, A.-L., Takai, K., Horikoshi, K. (2007). Deep-sea vent {varepsilon}-proteobacterial genomes provide insights into emergence of pathogens. Proc. Natl. Acad. Sci. USA 104: 12146-12150 [Abstract] [Full Text]  
  • Nakagawa, S., Inagaki, F., Suzuki, Y., Steinsbu, B. O., Lever, M. A., Takai, K., Engelen, B., Sako, Y., Wheat, C. G., Horikoshi, K., Integrated Ocean Drilling Program Expedition 301 S, (2006). Microbial Community in Black Rust Exposed to Hot Ridge Flank Crustal Fluids. Appl. Environ. Microbiol. 72: 6789-6799 [Abstract] [Full Text]  
  • Inagaki, F., Kuypers, M. M. M., Tsunogai, U., Ishibashi, J.-i., Nakamura, K.-i., Treude, T., Ohkubo, S., Nakaseama, M., Gena, K., Chiba, H., Hirayama, H., Nunoura, T., Takai, K., Jorgensen, B. B., Horikoshi, K., Boetius, A. (2006). From the Cover: Microbial community in a sediment-hosted CO2 lake of the southern Okinawa Trough hydrothermal system. Proc. Natl. Acad. Sci. USA 103: 14164-14169 [Abstract] [Full Text]  
  • Macalady, J. L., Lyon, E. H., Koffman, B., Albertson, L. K., Meyer, K., Galdenzi, S., Mariani, S. (2006). Dominant Microbial Populations in Limestone-Corroding Stream Biofilms, Frasassi Cave System, Italy. Appl. Environ. Microbiol. 72: 5596-5609 [Abstract] [Full Text]  
  • Takai, K., Suzuki, M., Nakagawa, S., Miyazaki, M., Suzuki, Y., Inagaki, F., Horikoshi, K. (2006). Sulfurimonas paralvinellae sp. nov., a novel mesophilic, hydrogen- and sulfur-oxidizing chemolithoautotroph within the Epsilonproteobacteria isolated from a deep-sea hydrothermal vent polychaete nest, reclassification of Thiomicrospira denitrificans as Sulfurimonas denitrificans comb. nov. and emended description of the genus Sulfurimonas.. Int. J. Syst. Evol. Microbiol. 56: 1725-1733 [Abstract] [Full Text]  
  • Suzuki, Y., Kojima, S., Sasaki, T., Suzuki, M., Utsumi, T., Watanabe, H., Urakawa, H., Tsuchida, S., Nunoura, T., Hirayama, H., Takai, K., Nealson, K. H., Horikoshi, K. (2006). Host-Symbiont Relationships in Hydrothermal Vent Gastropods of the Genus Alviniconcha from the Southwest Pacific. Appl. Environ. Microbiol. 72: 1388-1393 [Abstract] [Full Text]  
  • Takai, K., Campbell, B. J., Cary, S. C., Suzuki, M., Oida, H., Nunoura, T., Hirayama, H., Nakagawa, S., Suzuki, Y., Inagaki, F., Horikoshi, K. (2005). Enzymatic and Genetic Characterization of Carbon and Energy Metabolisms by Deep-Sea Hydrothermal Chemolithoautotrophic Isolates of Epsilonproteobacteria. Appl. Environ. Microbiol. 71: 7310-7320 [Abstract] [Full Text]  


Copyright © 2009 by the American Society for Microbiology.   For an alternate route to Journals.ASM.org, visit: http://intl-journals.asm.org | More Info»