Present address: Department of Civil and Environmental Engineering, Box 352700, University of Washington, Seattle, WA 98195, USA; ‡Department of Medical Microbiology and Immunology, University of Wisconsin, Madison, WI 53706, USA.
NO means ‘yes’ in the squid-vibrio symbiosis: nitric oxide (NO) during the initial stages of a beneficial association
Article first published online: 9 AUG 2004
Volume 6, Issue 12, pages 1139–1151, December 2004
How to Cite
Davidson, S. K., Koropatnick, T. A., Kossmehl, R., Sycuro, L. and McFall-Ngai, M. J. (2004), NO means ‘yes’ in the squid-vibrio symbiosis: nitric oxide (NO) during the initial stages of a beneficial association. Cellular Microbiology, 6: 1139–1151. doi: 10.1111/j.1462-5822.2004.00429.x
- Issue published online: 9 AUG 2004
- Article first published online: 9 AUG 2004
- Received 30 March, 2004; revised 11 May, 2004; accepted 12 May, 2004.
During colonization of the Euprymna scolopes light organ, symbiotic Vibrio fischeri cells aggregate in mucus secreted by a superficial ciliated host epithelium near the sites of eventual inoculation. Once aggregated, symbiont cells migrate through ducts into epithelium-lined crypts, where they form a persistent association with the host. In this study, we provide evidence that nitric oxide synthase (NOS) and its product nitric oxide (NO) are active during the colonization of host tissues by V. fischeri. NADPH-diaphorase staining and immunocytochemistry detected NOS, and the fluorochrome diaminofluorescein (DAF) detected its product NO in high concentrations in the epithelia of the superficial ciliated fields, ducts, and crypt antechambers. In addition, both NOS and NO were detected in vesicles within the secreted mucus where the symbionts aggregate. In the presence of NO scavengers, cells of a non-symbiotic Vibrio species formed unusually large aggregates outside of the light organ, but these bacteria did not colonize host tissues. In contrast, V. fischeri effectively colonized the crypts and irreversibly attenuated the NOS and NO signals in the ducts and crypt antechambers. These data provide evidence that NO production, a defense response of animal cells to bacterial pathogens, plays a role in the interactions between a host and its beneficial bacterial partner during the initiation of symbiotic colonization.