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PMID:10913092

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Citation

Visick, KL, Foster, J, Doino, J, McFall-Ngai, M and Ruby, EG (2000) Vibrio fischeri lux genes play an important role in colonization and development of the host light organ. J. Bacteriol. 182:4578-86

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.

Links

PubMed PMC94630

Keywords

Animals; Bacterial Proteins/genetics; Decapodiformes/microbiology; Electric Organ/microbiology; Epithelial Cells/cytology; Epithelial Cells/microbiology; Luciferases/genetics; Luminescent Measurements; Mutagenesis; Operon; Plasmids; Recombination, Genetic; Repressor Proteins/genetics; Symbiosis; Trans-Activators/genetics; Vibrio/enzymology; Vibrio/genetics; Vibrio/physiology

Significance

Annotations

Gene product Qualifier GO Term Evidence Code with/from Aspect Extension Notes Status

ALIFS:LUXI

GO:1905087: positive regulation of bioluminescence

ECO:0000315:

P

Table 1 shows that when autoinducers are introduced to the LuxI mutant then the bacteria will bioluminesce. Fig 2 signifies that when the luxI is not present the bioluminescence is significantly decreased in the colonized juvenile squid.

complete
CACAO 11359

ALIFS:LUXI

GO:0052043: modification by symbiont of host cellular component

ECO:0000315:

P

Figure 5 shows the different cytoplasmic volumes of the mutants and uninfected vs the wild type.

complete
CACAO 11680

ALIFS:LUXR

GO:1905087: positive regulation of bioluminescence

ECO:0000315:

P

Table 1 displays results of autoinducing molecules that can trigger the LuxR mutant into bioluminescing. Fig 2 signifies that when the luxR is not present the bioluminescence is significantly decreased in the colonized juvenile squids.

complete
CACAO 11360

ALIFS:LUXR

GO:0052043: modification by symbiont of host cellular component

ECO:0000315:

P

The table in Figure 5 shows the decreased levels of cytoplasm in the LuxR mutant vs the uninfected squids and wild type infected squids.

complete
CACAO 11681

ALIFS:LUXA

involved_in

GO:0008218: bioluminescence

ECO:0000315: mutant phenotype evidence used in manual assertion

P

Seeded From UniProt

complete

ALIFS:LUXA

GO:0008218: bioluminescence

ECO:0000315:

P

Table 1 shows that the LuxA gene is necessary for bioluminescence (not a regulator). Figure 2 also shows that biolumiscence is low in the LuxA mutants of the colonized juvenile squids in the experiment.

complete
CACAO 11612

ALIFS:LUXA

GO:0052043: modification by symbiont of host cellular component

ECO:0000315:

P

Figure 5 shows TEMs of the narrow columnar cells of the LuxA mutant infected squids vs the enlarged columnar cells of the wild type infected squids. The graph also depicts the decreased cytoplasmic volume between the two.

complete
CACAO 11683

See also

References

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