Contribution of Rapid Evolution of theluxR-luxIIntergenic Region to the Diverse Bioluminescence Outputs ofVibrio fischeriStrains Isolated from Different Environments

Bose, Jeffrey L.; Wollenberg, Michael S.; Colton, Deanna M.; Mandel, Mark J.; Septer, Alecia N.; Dunn, Anne K.; Stabb, Eric V.

doi:10.1128/aem.02643-10

Cited by 34 publications

(38 citation statements)

References 70 publications

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“…Other researchers have made great strides in dissecting the structure and function of LuxN, and we believe that comparative analyses including AinR will be enlightening. Similarly, we are intrigued by the divergence of AinR between V. fischeri isolates from different environments (43), and further investigation could elucidate selective pressures on AinS/ AinR for V. fischeri in different hosts. Finally, we are interested in the regulatory control of AinS/AinR expression, and our results have opened new research avenues, particularly with respect to our discovery of LuxR-mediated regulation and the potential for posttranscriptional control.…”

Section: Figmentioning

confidence: 99%

Substrate Specificity and Function of the Pheromone Receptor AinR in Vibrio fischeri ES114

Kimbrough

Stabb

2013

J Bacteriol

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Two distinct but interrelated pheromone-signaling systems, LuxI/LuxR and AinS/AinR, positively control bioluminescence in Vibrio fischeri. Although each system generates an acyl-homoserine lactone (AHL) signal, the protein sequences of LuxI/LuxR and AinS/AinR are unrelated. AinS and LuxI generate the pheromones N-octanoyl-AHL (C 8 -AHL) and N-3-oxo-hexanoyl-AHL (3OC 6 -AHL), respectively. LuxR is a transcriptional activator that responds to 3OC 6 -AHL, and to a lesser extent to C 8 -AHL. AinR is hypothesized to respond to C 8 -AHL and, based on homology to Vibrio harveyi LuxN, to mediate the repression of a Qrr regulatory RNA. However, a ⌬ainR mutation decreased luminescence, which was not predicted based on V. harveyi LuxN, raising the possibility of a distinct regulatory mechanism for AinR. Here we show that ainR can complement a luxN mutant, suggesting functional similarity. Moreover, in V. fischeri, we observed ainR-dependent repression of a P qrr -lacZ transcriptional reporter in the presence of C 8 -AHL, consistent with its hypothesized regulatory role. The system appears quite sensitive, with a half-maximal effect on a P qrr reporter at 140 pM C 8 -AHL. Several other AHLs with substituted and unsubstituted acyl chains between 6 and 10 carbons also displayed an AinR-dependent effect on P qrr -lacZ; however, AHLs with acyl chains of four carbons or 12 or more carbons lacked activity. Interestingly, 3OC 6 -AHL also affected expression from the qrr promoter, but this effect was largely luxR dependent, indicating a previously unknown connection between these systems. Finally, we propose a preliminary explanation for the unexpected luminescence phenotype of the ⌬ainR mutant.

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Section: Figmentioning

confidence: 99%

Substrate Specificity and Function of the Pheromone Receptor AinR in Vibrio fischeri ES114

Kimbrough

Stabb

2013

J Bacteriol

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“…Interestingly, one clade, referred to as group A strains, exhibits competitive dominance when competed against non-group A strains in colonization experiments with juvenile squid (17). Among V. fischeri strains, the luxIR intergenic region was also shown to be hypervariable and to contribute to the bioluminescence profile of each strain, suggesting that bioluminescence and its regulation are under selection (18,19). How such V. fischeri strain diversity develops within the squid light organ is unclear.…”

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confidence: 99%

Intraspecific Competition Impacts Vibrio fischeri Strain Diversity during Initial Colonization of the Squid Light Organ

Sun

LaSota

Cecere

et al. 2016

Appl Environ Microbiol

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Animal development and physiology depend on beneficial interactions with microbial symbionts. In many cases, the microbial symbionts are horizontally transmitted among hosts, thereby making the acquisition of these microbes from the environment an important event within the life history of each host. The light organ symbiosis established between the Hawaiian squid Euprymna scolopes and the bioluminescent bacterium Vibrio fischeri is a model system for examining how hosts acquire horizontally transmitted microbial symbionts. Recent studies have revealed that the light organ of wild-caught E. scolopes squid contains polyclonal populations of V. fischeri bacteria; however, the function and development of such strain diversity in the symbiosis are unknown. Here, we report our phenotypic and phylogenetic characterizations of FQ-A001, which is a V. fischeri strain isolated directly from the light organ of an E. scolopes individual. Relative to the type strain ES114, FQ-A001 exhibits similar growth in rich medium but displays increased bioluminescence and decreased motility in soft agar. FQ-A001 outcompetes ES114 in colonizing the crypt spaces of the light organs. Remarkably, we find that animals cocolonized with FQ-A001 and ES114 harbor singly colonized crypts, in contrast to the cocolonized crypts observed from competition experiments involving single genotypes. The results with our two-strain system suggest that strain diversity within the squid light organ is a consequence of diversity in the single-strain colonization of individual crypt spaces. IMPORTANCEThe developmental programs and overall physiologies of most animals depend on diverse microbial symbionts that are acquired from the environment. However, the basic principles underlying how microbes colonize their hosts remain poorly understood. Here, we report our findings of bacterial strain competition within the coevolved animal-microbe symbiosis composed of the Hawaiian squid and bioluminescent bacterium Vibrio fischeri. Using fluorescent proteins to differentially label two distinct V. fischeri strains, we find that the strains are unable to coexist in the same niche within the host. Our results suggest that strain competition for distinct colonization sites dictates the strain diversity associated with the host. Our study provides a platform for studying how strain diversity develops within a host. Microbes directly contribute to the physiology, development, and evolution of metazoans (1). Many metazoan-microbe symbioses are established through horizontal transmission, i.e., animals acquire microbial symbionts from their environment (2). Coevolution of host-microbe pairs can result in genetic factors that promote remarkably high specificity between the partners, thereby assisting in the acquisition of symbionts from typically unpredictable environments (3). An important but understudied topic in coevolved metazoan-microbe symbioses is how strain diversity impacts the establishment of these associations.A particularly powerful model system to explo...

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“…3, 4, and 5). The intergenic lux region has diverged significantly between ES114, MJ-1, and other V. fischeri strains, and while a putative CRP binding site is evident in the same location in a variety of strains, the exact sequence of the site does vary (53). The sequence revealed in CRP footprinting analyses of V. fischeri ATCC 7744 DNA by Shadel et al (26) aligns with the ES114 sequence used in our binding studies (Fig.…”

Section: Discussionmentioning

confidence: 68%

“…The sequence revealed in CRP footprinting analyses of V. fischeri ATCC 7744 DNA by Shadel et al (26) aligns with the ES114 sequence used in our binding studies (Fig. 5), although there are several differences in the sequences, particularly in the variable central region of the binding site (53). In addition to demonstrating binding, using a transgenic E. coli system we found that the effect of CRP on luxR requires only the CRP-activating region I, consistent with this effect being mediated by a class I-type promoter interaction.…”

Section: Discussionmentioning

confidence: 99%

Cyclic AMP Receptor Protein Regulates Pheromone-Mediated Bioluminescence at Multiple Levels in Vibrio fischeri ES114

et al. 2013

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Bioluminescence in Vibrio fischeri ES114 is activated by autoinducer pheromones, and this regulation serves as a model for bacterial cell-cell signaling. As in other bacteria, pheromone concentration increases with cell density; however, pheromone synthesis and perception are also modulated in response to environmental stimuli. Previous studies suggested that expression of the pheromone-dependent bioluminescence activator LuxR is regulated in response to glucose by cyclic AMP (cAMP) receptor protein ( . Consistent with this model, we found that bioluminescence in V. fischeri ES114 is modulated by glucose and stimulated by cAMP. In addition, a ⌬crp mutant was ϳ100-fold dimmer than ES114 and did not increase luminescence in response to added cAMP, even though cells lacking crp were still metabolically capable of producing luminescence. We further discovered that CRP regulates not only luxR but also the alternative pheromone synthase gene ainS. We found that His-tagged V. fischeri CRP could bind sequences upstream of both luxR and ainS, supporting bioinformatic predictions of direct regulation at both promoters. Luminescence increased in response to cAMP if either the ainS or luxR system was under native regulation, suggesting cAMP-CRP significantly increases luminescence through both systems. Finally, using transcriptional reporters in transgenic Escherichia coli, we elucidated two additional regulatory connections. First, LuxR-independent basal transcription of the luxI promoter was enhanced by CRP. Second, the effect of CRP on the ainS promoter depended on whether the V. fischeri regulatory gene litR was also introduced. These results suggest an integral role for CRP in pheromone signaling that goes beyond sensing cell density.

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Contribution of Rapid Evolution of theluxR-luxIIntergenic Region to the Diverse Bioluminescence Outputs ofVibrio fischeriStrains Isolated from Different Environments

Cited by 34 publications

References 70 publications

Substrate Specificity and Function of the Pheromone Receptor AinR in Vibrio fischeri ES114

Substrate Specificity and Function of the Pheromone Receptor AinR in Vibrio fischeri ES114

Intraspecific Competition Impacts Vibrio fischeri Strain Diversity during Initial Colonization of the Squid Light Organ

Cyclic AMP Receptor Protein Regulates Pheromone-Mediated Bioluminescence at Multiple Levels in Vibrio fischeri ES114

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