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

Sun, Yan; LaSota, Elijah; Cecere, Andrew G.; LaPenna, Kyle B.; Larios-Valencia, Jessie; Wollenberg, Michael S.; Miyashiro, Tim

doi:10.1128/aem.04143-15

Cited by 36 publications

(49 citation statements)

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“…CysB promotes growth of V. fischeri on various sulfur sources V. fischeri grows in defined minimal medium containing sulfate as the sole sulfur source (Sun et al, 2015), which shows that V. fischeri has the ability to assimilate sulfate. To determine whether V. fischeri grows on other sulfur sources, we measured the growth yield of the wild-type, symbiotic V. fischeri strain ES114 (Ruby et al, 2005) in sulfur-free medium supplemented with sulfate, thiosulfate, cysteine, cystine or glutathione, which are sulfur sources commonly used by other γ-proteobacteria (Kredich, 1996).…”

Section: Resultsmentioning

confidence: 97%

“…Shortly after juvenile squid hatch from their eggs, they acquire V. fischeri cells from the seawater environment, which quickly colonize three epithelium-lined crypt spaces located on either side of the host's light organ. V. fischeri is a genetically tractable microbe, and the juvenile light organ is amenable to light microscopy, which has led to the use of fluorescent proteins as markers of cell position and gene expression in vivo (Dunn et al, 2006;Sun et al, 2015). The populations resulting from the rapid proliferation of the founder cells that initially colonize the crypt spaces produce bioluminescence that the host uses as a form of camouflage (Jones and Nishiguchi, 2004).…”

Section: Introductionmentioning

confidence: 99%

“…While chitin fermentation appears to fuel the growth of V. fischeri in the mature symbiosis, the mechanisms that support bacterial growth within the juvenile light organ are less clear. The expression of genes necessary for metabolizing chitin byproducts are repressed by NagC (Sun et al, 2015), suggesting that nutrients other than chitin are accessed by the corresponding V. fischeri populations at this early stage of symbiosis. The current model is that host proteins are degraded into peptides and amino acids that promote V. fischeri growth, which was initially proposed from the successful colonization of juvenile animals by mutants that exhibit auxotrophy for various amino acids (Graf and Ruby, 1998).…”

Section: Introductionmentioning

confidence: 99%

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Sulfur availability for Vibrio fischeri growth during symbiosis establishment depends on biogeography within the squid light organ

Wasilko

Larios-Valencia

Steingard

et al. 2019

Molecular Microbiology

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Summary The fitness of host‐associated microbes depends on their ability to access nutrients in vivo. Identifying these mechanisms is significant for understanding how microbes have evolved to fill specific ecological niches within a host. Vibrio fischeri is a bioluminescent bacterium that colonizes and proliferates within the light organ of the Hawaiian bobtail squid, which provides an opportunity to study how bacteria grow in vivo. Here, the transcription factor CysB is shown to be necessary for V. fischeri both to grow on several sulfur sources in vitro and to establish symbiosis with juvenile squid. CysB is also found to regulate several genes involved in sulfate assimilation and to contribute to the growth of V. fischeri on cystine, which is the oxidized form of cysteine. A mutant that grows on cystine but not sulfate could establish symbiosis, suggesting that V. fischeri acquires nutrients related to this compound within the host. Finally, CysB‐regulated genes are shown to be differentially expressed among the V. fischeri populations occupying the various colonization sites found within the light organ. Together, these results suggest the biogeography of V. fischeri populations within the squid light organ impacts the physiology of this symbiotic bacterium in vivo through CysB‐dependent gene regulation.

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Section: Resultsmentioning

confidence: 97%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Sulfur availability for Vibrio fischeri growth during symbiosis establishment depends on biogeography within the squid light organ

Wasilko

Larios-Valencia

Steingard

et al. 2019

Molecular Microbiology

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“…Past experiments designed to directly compare the abilities of two V. fischeri strains to colonize juvenile squid used different fluorescent proteins to distinguish strain types within the light organ (26,29,30). In the colonization experiments described here, isogenic plasmids pSCV37 and pSCV38 were used to differentially label strains with CFP and YFP, respectively.…”

Section: Resultsmentioning

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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“…After a series of additional in vitro experiments to better understand the compatibility of strains isolated from the same or different animals, the authors tested whether T6SS2-mediated interstrain competition was required for the crypt monocolonization phenotype (15). To address this question, animals were inoculated with a mixture of bacterial strains that were distinguishable through their production of two different fluorescent proteins.…”

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confidence: 99%

Bacterial type VI secretion system facilitates niche domination

Dörr

Blokesch

2018

Proc. Natl. Acad. Sci. U.S.A.

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

Cited by 36 publications

References 46 publications

Sulfur availability for Vibrio fischeri growth during symbiosis establishment depends on biogeography within the squid light organ

Sulfur availability for Vibrio fischeri growth during symbiosis establishment depends on biogeography within the squid light organ

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

Bacterial type VI secretion system facilitates niche domination

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