Vibrio fischeri lux Genes Play an Important Role in Colonization and Development of the Host Light Organ

Abstract

The bioluminescent bacterium Vibrio fischeri and juveniles of the squid Euprymna scolopes specifically recognize and respond to one another during the formation of a persistent colonization within the host's nascent light-emitting organ. The resulting fully developed light organ contains brightly luminescing bacteria and has undergone a bacterium-induced program of tissue differentiation, one component of which is a swelling of the epithelial cells that line the symbiont-containing crypts. While the luminescence (lux) genes of symbiotic V. fischeri have been shown to be highly induced within the crypts, the role of these genes in the initiation and persistence of the symbiosis has not been rigorously examined. We have constructed and examined three mutants (luxA, luxI, and luxR), defective in either luciferase enzymatic or regulatory proteins. All three are unable to induce normal luminescence levels in the host and, 2 days after initiating the association, had a three-to fourfold defect in the extent of colonization. Surprisingly, these lux mutants also were unable to induce swelling in the crypt epithelial cells. Complementing, in trans, the defect in light emission restored both normal colonization capability and induction of swelling. We hypothesize that a diminished level of oxygen consumption by a luciferase-deficient symbiotic population is responsible for the reduced fitness of lux mutants in the light organ crypts. This study is the first to show that the capacity for bioluminescence is critical for normal cell-cell interactions between a bacterium and its animal host and presents the first examples of V. fischeri genes that affect normal host tissue development.

Symbiont recognition of mutualistic bacteria by Acromyrmex leaf-cutting ants

“…Sachs et al, 2004) or as a preferential choice of one symbiont over another irrespective of symbiont degree of cooperation (for example, Bot et al, 2001;Mueller et al, 2004). Partner choice can take place during the initiation of an association, for example, the colonization of the bobtail squid light organ by Vibrio fischeri symbionts (McFall-Ngai and Ruby, 1991;Visick et al, 2000;Nishiguchi, 2002), or as a means of avoiding cheating symbiont strains (for example, in the yucca-yucca moth symbiosis: Pellmyr and Huth, 1994;Huth and Pellmyr, 2000; in the squid-Vibrio symbiosis: Visick et al, 2000; and in the legume-Rhizobium symbiosis: Simms and Taylor, 2002;West et al, 2002). Our experiments do not evaluate if ant symbiont choice is a response to the degree of cooperation of the Pseudonocardia strains.…”

What can microbial genetics teach sociobiology?

“…All mutants showed little bioluminescence; however, no clone could cheat. This is because the expression of lux genes is also required for efficient colonization [58,59]. Analogous to the case of dimA, this seems to be a system in which pleiotropic constraints go hand-in-hand with coercion.…”

Exploring host–microbiota interactions in animal models and humans

“…This potential metabolic advantage for nonluminescent bacteria could undermine the function of the light organ if these microbes chronically colonized the squid. However, several studies have demonstrated that the quorum-sensing mutants are unable to initiate the normal light organ developmental program and are significantly less capable of persistent colonization (Visick et al 2000;Lupp et al 2003;Bose et al 2008;Chun et al 2008). How the squid monitors bacterial luminesce is not as well understood, but the light organ does share some similarities to the eye.…”