NO means 'yes' in the squid-vibrio symbiosis: nitric oxide (NO) during the initial stages of a beneficial association

Abstract

SummaryDuring 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. NADPHdiaphorase 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.

Transcriptional patterns in both host and bacterium underlie a daily rhythm of anatomical and metabolic change in a beneficial symbiosis

“…A number of pathogens, including V. cholerae, also apparently respire nitrate/nitrite when hostassociated, and this metabolism plays a critical, but as yet uncharacterized, role in their virulence (27)(28)(29). The source of nitrate/nitrite in these associations is not known; however, in the squid host it may come from a spontaneous oxidation of NO produced by the light-organ epithelium (30). At night, a down-regulation of anaerobic-respiration genes occurs concomitantly with an up-regulation of the expression of genes associated with the fermentative catabolism of chitin (Fig.…”

H-NOX–mediated nitric oxide sensing modulates symbiotic colonization by Vibrio fischeri

“…One such molecule, nitric oxide (NO), plays a key role in both cellular defense and signaling. When produced at high concentrations by activated macrophages and tissues, it is a powerful antimicrobial (2,3). In contrast, when produced at low concentrations, NO can serve as a signaling molecule; for instance, in eukaryotic endothelial cells, it regulates activities such as vasodilation, and in bacteria that contain specific NO sensors, it facilitates responses to environmental conditions (4,5).…”

“…During this transit, the migrating V. fischeri are exposed to host-derived NO produced both by vesicles embedded in the secreted mucus and later, by the epithelium lining of the ducts (2), where reactive oxygen species are also produced (14). Given its antimicrobial and signaling properties, the generation of this host-derived NO has been proposed to be involved in the early stages of the association not only as a specificity determinant but also as a symbiotic signal (2,12).…”

Selective recruitment of bacteria during embryogenesis of an earthworm

“…Vibrio fischeri are selectively collected from the mixed bacterial population in the sea water and accumulate by binding specifically to the mucus of the symbiotic organ with a few contaminant cells (Nyholm et al, 2000;Nyholm and McFall-Ngai, 2003). After a waiting period (2-3 h), V. fischeri migrate into the nascent light organ through ciliated ducts that possess an oxidatively stressful environment to exclude other bacterial types (Small and McFall-Ngai, 1999;Davidson et al, 2004). Motility and resistance to oxidative stress are required for this migration (Graf et al, 1994;Visick and Ruby, 1998).…”