The role of the immune system in the initiation and persistence of the Euprymna scolopes–Vibrio fischeri symbiosis

McFall‐Ngai, Margaret J.; Nyholm, Spencer V.; Castillo, Maria G.

doi:10.1016/j.smim.2009.11.003

Cited by 91 publications

(97 citation statements)

References 39 publications

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“…Because, over time, the host can sanction specific members of the symbiont population (Koch et al, 2014); it is critical to include the role of the host in the dynamics of the symbiont population (McFall-Ngai et al, 2010;Palmer et al, 2010). In any case, tracking the population dynamics of artificially constructed combinations of symbionts during the approximately 9-month lifetime of the squid may reveal whether the D-or S-type strain behaviors described here increase stability in the symbiosis or, in contrast, lead to undesirable outcomes for the association.…”

Section: Discussionmentioning

confidence: 99%

A genomic comparison of 13 symbiotic Vibrio fischeri isolates from the perspective of their host source and colonization behavior

et al. 2016

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Newly hatched Euprymna scolopes squid obtain their specific light-organ symbionts from an array of Vibrio (Allivibrio) fischeri strains present in their environment. Two genetically distinct populations of this squid species have been identified, one in Kaneohe Bay (KB), and another in Maunaloa Bay (MB), Oahu. We asked whether symbionts isolated from squid in each of these populations outcompete isolates from the other population in mixed-infection experiments. No relationship was found between a strain's host source (KB or MB) and its ability to competitively colonize KB or MB juveniles in a mixed inoculum. Instead, two colonization behaviors were identified among the 11 KB and MB strains tested: a 'dominant' outcome, in which one strain outcompetes the other for colonization, and a 'sharing' outcome, in which two strains co-colonize the squid. A genome-level comparison of these and other V. fischeri strains suggested that the core genomic structure of this species is both syntenous and highly conserved over time and geographical distance. We also identified~250 Kb of sequence, encoding 194 dispersed orfs, that was specific to those strains that expressed the dominant colonization behavior. Taken together, the results indicate a link between the genome content of V. fischeri strains and their colonization behavior when initiating a light-organ symbiosis.

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Section: Discussionmentioning

confidence: 99%

A genomic comparison of 13 symbiotic Vibrio fischeri isolates from the perspective of their host source and colonization behavior

et al. 2016

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“…Several phenotypes associated with light organ morphogenesis are induced by the synergic activity of PG fragments and LPS (8,30). These two classes of MAMPs have different effects in symbiont-induced morphogenesis: the phosphorylated lipid A of LPS triggers early stage apoptosis, while PG fragments, like tracheal cytotoxin (TCT), activate both hemocyte trafficking and late-stage apoptosis (8).…”

Section: Discussionmentioning

confidence: 99%

Rotation of Vibrio fischeri Flagella Produces Outer Membrane Vesicles That Induce Host Development

et al. 2016

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Using the squid-vibrio association, we aimed to characterize the mechanism through which Vibrio fischeri cells signal morphogenesis of the symbiotic light-emitting organ. The symbiont releases two cell envelope molecules, peptidoglycan (PG) and lipopolysaccharide (LPS) that, within 12 h of light organ colonization, act in synergy to trigger normal tissue development. Recent work has shown that outer membrane vesicles (OMVs) produced by V. fischeri are sufficient to induce PG-dependent morphogenesis; however, the mechanism(s) of OMV release by these bacteria has not been described. Like several genera of both beneficial and pathogenic bacteria, V. fischeri cells elaborate polar flagella that are enclosed by an extension of the outer membrane, whose function remains unclear. Here, we present evidence that along with the well-recognized phenomenon of blebbing from the cell's surface, rotation of this sheathed flagellum also results in the release of OMVs. In addition, we demonstrate that most of the development-inducing LPS is associated with these OMVs and that the presence of the outer membrane protein OmpU but not the LPS O antigen on these OMVs is important in triggering normal host development. These results also present insights into a possible new mechanism of LPS release by pathogens with sheathed flagella. IMPORTANCEDetermining the function(s) of sheathed flagella in bacteria has been challenging, because no known mutation results only in the loss of this outer membrane-derived casing. Nevertheless, the presence of a sheathed flagellum in such host-associated genera as Vibrio, Helicobacter, and Brucella has led to several proposed functions, including physical protection of the flagella and masking of their immunogenic flagellins. Using the squid-vibrio light organ symbiosis, we demonstrate another role, that of V. fischeri cells require rotating flagella to induce apoptotic cell death within surface epithelium, which is a normal step in the organ's development. Further, we present evidence that this rotation releases apoptosis-triggering lipopolysaccharide in the form of outer membrane vesicles. Such release may also occur by pathogens but with different outcomes for the host.

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“…The stark differences in epithelial tissues in the ANG suggest that unique microenvironments exist between tubules. In the light organ, hemocytes, representing the sole cellular component of the host's innate immune system, have been implicated in establishing and maintaining specificity (22,31,36,37). Hemocytes were also observed to infiltrate the lumina of the ANG tubules and were found to come in direct contact with the bacterial consortium (Fig.…”

Section: Discussionmentioning

confidence: 99%

Diversity and Partitioning of Bacterial Populations within the Accessory Nidamental Gland of the Squid Euprymna scolopes

Collins

LaBarre

Won

et al. 2012

Appl Environ Microbiol

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ABSTRACTMicrobial consortia confer important benefits to animal and plant hosts, and model associations are necessary to examine these types of host/microbe interactions. The accessory nidamental gland (ANG) is a female reproductive organ found among cephalopod mollusks that contains a consortium of bacteria, the exact function of which is unknown. To begin to understand the role of this organ, the bacterial consortium was characterized in the Hawaiian bobtail squid,Euprymna scolopes, a well-studied model organism for symbiosis research. Transmission electron microscopy (TEM) analysis of the ANG revealed dense bacterial assemblages of rod- and coccus-shaped cells segregated by morphology into separate, epithelium-lined tubules. The host epithelium was morphologically heterogeneous, containing ciliated and nonciliated cells with various brush border thicknesses. Hemocytes of the host's innate immune system were also found in close proximity to the bacteria within the tubules. A census of 16S rRNA genes suggested thatRhodobacterales, Rhizobiales, andVerrucomicrobiabacteria were prevalent, with members of the genusPhaeobacterdominating the consortium. Analysis of 454-shotgun sequencing data confirmed the presence of members of these taxa and revealed members of a fourth,Flavobacteriaof theBacteroidetesphylum. 16S rRNA fluorescentin situhybridization (FISH) revealed that many ANG tubules were dominated by members of specific taxa, namely,Rhodobacterales,Verrucomicrobia, orCytophaga-Flavobacteria-Bacteroidetes, suggesting symbiont partitioning to specific host tubules. In addition, FISH revealed that bacteria, includingPhaeobacterspecies from the ANG, are likely deposited into the jelly coat of freshly laid eggs. This report establishes the ANG of the invertebrateE. scolopesas a model to examine interactions between a bacterial consortium and its host.

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The role of the immune system in the initiation and persistence of the Euprymna scolopes–Vibrio fischeri symbiosis

Cited by 91 publications

References 39 publications

A genomic comparison of 13 symbiotic Vibrio fischeri isolates from the perspective of their host source and colonization behavior

A genomic comparison of 13 symbiotic Vibrio fischeri isolates from the perspective of their host source and colonization behavior

Rotation of Vibrio fischeri Flagella Produces Outer Membrane Vesicles That Induce Host Development

Diversity and Partitioning of Bacterial Populations within the Accessory Nidamental Gland of the Squid Euprymna scolopes

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