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Applied and Environmental Microbiology, March 2007, p. 1984-1991, Vol. 73, No. 6
0099-2240/07/$08.00+0     doi:10.1128/AEM.01833-06
Copyright © 2007, American Society for Microbiology. All Rights Reserved.

Spatial and Temporal Population Dynamics of a Naturally Occurring Two-Species Microbial Community inside the Digestive Tract of the Medicinal Leech{triangledown}

Yoshitomo Kikuchi1,2 and Joerg Graf1*

Department of Molecular and Cell Biology, University of Connecticut, Storrs, Connecticut 06269,1 Institute for Biological Resources and Functions, National Institute of Advanced Industrial Science and Technology (AIST), Tsukuba 305-8566, Japan2

Received 2 August 2006/ Accepted 21 January 2007

The medicinal leech, Hirudo verbana, is one of the simplest naturally occurring models for digestive-tract symbioses, where only two bacterial species, Aeromonas veronii bv. sobria ({gamma}-Proteobacteria) and a Rikenella-like bacterium (Bacteroidetes), colonize the crop, the largest compartment of the leech digestive tract. In this study, we investigated spatial and temporal changes of the localization and microcolony structure of the native symbionts in the crop, after ingestion of a sterile blood meal, by fluorescence in situ hybridization. The population dynamics differed between the two symbiotic bacteria. A. veronii was detected mainly as individual cells inside the intraluminal fluid (ILF) during 14 days after feeding (daf) unless it was found in association with Rikenella microcolonies. The Rikenella-like bacteria were observed not only inside the ILF but also in association with the luminal surface of the crop epithelium. The sizes of Rikenella microcolonies changed dynamically through the 14-day period. From 3 daf onward, mixed microcolonies containing both species were frequently observed, with cells of both species tightly associating with each other. The sizes of the mixed microcolonies were consistently larger than the size of either single-species microcolony, suggesting a synergistic interaction of the symbionts. Lectin staining with succinylated wheat germ agglutinin revealed that the planktonic microcolonies present in the ILF were embedded in a polysaccharide matrix containing N-acetylglucosamine. The simplicity, symbiont-symbiont interaction, and mixed microcolonies of this naturally occurring, digestive-tract symbiosis lay the foundation for understanding the more complex communities residing in most animals.

* Corresponding author. Mailing address: Department of Molecular and Cell Biology, University of Connecticut, 91 N. Eagleville Rd., Unit 3125, Storrs, CT 06269. Phone: (860) 486-9284. Fax: (860) 486-4331. E-mail: joerg.graf{at}uconn.edu.

{triangledown} Published ahead of print on 2 February 2007.

Applied and Environmental Microbiology, March 2007, p. 1984-1991, Vol. 73, No. 6
0099-2240/07/$08.00+0     doi:10.1128/AEM.01833-06
Copyright © 2007, American Society for Microbiology. All Rights Reserved.



This article has been cited by other articles:

  • Rio, R. V. M., Maltz, M., McCormick, B., Reiss, A., Graf, J. (2009). Symbiont Succession during Embryonic Development of the European Medicinal Leech, Hirudo verbana. Appl. Environ. Microbiol. 75: 6890-6895 [Abstract] [Full Text]  
  • Laufer, A. S., Siddall, M. E., Graf, J. (2008). Characterization of the Digestive-Tract Microbiota of Hirudo orientalis, a European Medicinal Leech. Appl. Environ. Microbiol. 74: 6151-6154 [Abstract] [Full Text]  
  • Silver, A. C., Rabinowitz, N. M., Kuffer, S., Graf, J. (2007). Identification of Aeromonas veronii Genes Required for Colonization of the Medicinal Leech, Hirudo verbana. J. Bacteriol. 189: 6763-6772 [Abstract] [Full Text]  
  • Rio, R. V. M., Anderegg, M., Graf, J. (2007). Characterization of a catalase gene from Aeromonas veronii, the digestive-tract symbiont of the medicinal leech. Microbiology 153: 1897-1906 [Abstract] [Full Text]  
  • Silver, A. C., Kikuchi, Y., Fadl, A. A., Sha, J., Chopra, A. K., Graf, J. (2007). Interaction between innate immune cells and a bacterial type III secretion system in mutualistic and pathogenic associations. Proc. Natl. Acad. Sci. USA 104: 9481-9486 [Abstract] [Full Text]  


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