Phylogeny and fitness of <i>Vibrio fischeri</i> from the light organs of <i>Euprymna scolopes</i> in two Oahu, Hawaii populations

Wollenberg, Michael S.; Ruby, Edward G.

doi:10.1038/ismej.2011.92

Cited by 54 publications

(70 citation statements)

References 46 publications

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“…To explore the evolutionary relationship of FQ-A001 to other V. fischeri strains, we conducted a phylogenetic analysis. This phylogenetic analysis used a previously described methodology of constructing a phylogenetic hypothesis using concatenated partial sequences of four housekeeping loci (recA, mdh, katA, and pyrC) in V. fischeri and several closely related Vibrio species (17). Our phylogenetic analysis strongly supported a very close evolutionary relationship of FQ-A001 and MB14A3 (Fig.…”

Section: Resultssupporting

confidence: 54%

“…Previous studies have revealed significant phenotypic, genetic, and phylogenetic diversity among symbiotic V. fischeri strains (16,17). To explore the evolutionary relationship of FQ-A001 to other V. fischeri strains, we conducted a phylogenetic analysis.…”

Section: Resultsmentioning

confidence: 99%

“…In this study, we examined whether the initial stages of colonization could contribute to the previously reported V. fischeri strain diversity associated with the light organs of wild-caught squid (16,17). Microbiological assays and phylogenetic analyses demonstrated that the strain FQ-A001, which was isolated directly from an adult light organ, is physiologically and genetically distinct from the V. fischeri type strain ES114.…”

Section: Discussionmentioning

confidence: 99%

“…Phylogenetic analyses created from concatenated housekeeping genes have revealed that several well-supported clades of strains exist within the greater V. fischeri clade. 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).…”

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confidence: 99%

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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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Section: Resultssupporting

confidence: 54%

Section: Resultsmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

mentioning

confidence: 99%

See 2 more Smart Citations

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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“…Numerous studies of squid-Vibrio symbiosis have used the CFU-based competition assay to highlight the individual contributions of signaling pathways (18,35), cell-envelope monomers (36), motility factors (37), and even strain phylogeny (38) to light organ colonization. The approach presented here can also be used to examine the spatial organization of these strains, thereby facilitating better understanding of the link between the bacterium-associated factors and the developmental stages of the light organ crypts.…”

Section: Discussionmentioning

confidence: 99%

Niche-Specific Impact of a Symbiotic Function on the Persistence of Microbial Symbionts within a Natural Host

Verma

Miyashiro

2016

Appl Environ Microbiol

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How the function of microbial symbionts is affected by their population/consortium structure within a host remains poorly understood. The symbiosis established between Euprymna scolopes and Vibrio fischeri is a well-characterized host-microbe association in which the function and structure of V. fischeri populations within the host are known: V. fischeri populations produce bioluminescence from distinct crypt spaces within a dedicated host structure called the light organ. Previous studies have revealed that luminescence is required for V. fischeri populations to persist within the light organ and that deletion of the lux gene locus, which is responsible for luminescence in V. fischeri, leads to a persistence defect. In this study, we investigated the impact of bioluminescence on V. fischeri population structure within the light organ. We report that the persistence defect is specific to crypt I, which is the most developmentally mature crypt space within the nascent light organ. This result provides insight into the structure/function relationship that will be useful for future mechanistic studies of squid-Vibrio symbiosis. In addition, our report highlights the potential impact of the host developmental program on the spatiotemporal dynamics of host-microbe interactions. IMPORTANCEMetazoan development and physiology depend on microbes. The relationship between the symbiotic function of microbes and their spatial structure within the host environment remains poorly understood. Here we demonstrate, using a binary symbiosis, that the host requirement for the symbiotic function of the microbial symbiont is restricted to a specific host environment. Our results also suggest a link between microbial function and host development that may be a fundamental aspect of the more complex host-microbe interactions. Microbes are a dominant form of life on Earth, and their associations with humans and other animals directly impact host development, physiology, and evolution (1-3). In many cases, the acquisition of microbes from the environment represents a key moment in the life history of the host. Studies of mammalian gut microbiota have suggested that the spatial distribution of these microbes within the host, i.e., their biogeography, is an important factor in the assemblage and maintenance of such associations (see reference 4 for a recent review). For instance, when microbial communities isolated from diverse habitats are transplanted into gnotobiotic mice, the resulting composition closely resembles that normally found in the mouse cecum (5). Body part-specific microbiota have also been observed in nonmammalian systems, such as that of the jellyfish Aurelia aurita, which shows significant differences in microbial composition between the gastric cavity and exumbrellar mucus (6). These studies suggest that hosts select certain biogeographical landscapes for their associated microbiota. However, examining how biogeography impacts the symbiotic function of microbes remains challenging for most associations, due in ...

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Rethinking “mutualism” in diverse host‐symbiont communities

Mushegian

Ebert

2015

BioEssays

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While examples of bacteria benefiting eukaryotes are increasingly documented, studies examining effects of eukaryote hosts on microbial fitness are rare. Beneficial bacteria are often called "mutualistic" even if mutual reciprocity of benefits has not been demonstrated and despite the plausibility of other explanations for these microbes' beneficial effects on host fitness. Furthermore, beneficial bacteria often occur in diverse communities, making mutualism both empirically and conceptually difficult to demonstrate. We suggest reserving the terms "mutualism" and "parasitism" for pairwise interactions where the relationship is largely independent of other species and can be verified by measuring the fitness effect experienced by both partners. In hosts with diverse microbial communities, we propose re-formulating some of the essential questions of symbiosis research - e.g. concerning specificity, transmission mode, and common evolutionary fates - as questions of community ecology and ecosystem function, allowing important biological interactions to be investigated without making assumptions about reciprocity. Understanding the fitness of host-associated bacteria is a crucial component of investigations into the role of microbes in eukaryote evolution.

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Phylogeny and fitness of Vibrio fischeri from the light organs of Euprymna scolopes in two Oahu, Hawaii populations

Cited by 54 publications

References 46 publications

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

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

Niche-Specific Impact of a Symbiotic Function on the Persistence of Microbial Symbionts within a Natural Host

Rethinking “mutualism” in diverse host‐symbiont communities

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