A Transient Exposure to Symbiosis-Competent Bacteria Induces Light Organ Morphogenesis in the Host Squid

Doino, Judith; McFall‐Ngai, Margaret J.

doi:10.2307/1542152

Cited by 91 publications

(85 citation statements)

References 27 publications

(18 reference statements)

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“…Thus, the ϳ100-fold increase in net PG monomer release by the ampG mutant in We next examined whether the ampG mutation could trigger morphogenesis in a strain that could not colonize the light-organ crypts. Nonmotile V. fischeri strains do not enter the light-organ crypts and do not induce regression (15), although they are able to induce mucus production from the ciliated fields and can form aggregates outside the pores of the light organ (53). We therefore tested whether a nonmotile strain generating large amounts of extracellular PG monomer might be able to induce regression without colonizing the lightorgan crypt, by constructing a flaJ ampG double mutant.…”

Section: Resultsmentioning

confidence: 99%

“…The latter filter set was used in conjunction with a Nikon Coolpix 5000 camera to obtain the epifluorescence images shown of animals stained with Cell Tracker. Regression stage (stages 0 to 4) was scored blindly, as set forth by Doino and McFall-Ngai (15). The E. scolopes light organ is bilobed, and each of the two lobes was scored separately, although we never observed an animal with lobes at different stages of regression.…”

Section: Continued On Following Pagementioning

confidence: 99%

“…E. scolopes hatchlings contain ciliated appendages that increase water flow across the light organ and help facilitate infection (40,41,48). During initial colonization, V. fischeri triggers regression of these ciliated fields (15,47), and this can be mimicked by adding PG monomers to the seawater (31). In this study, we constructed and analyzed mutants to determine the contributions of lytic transglycosylases and AmpG to PG monomer release in V. fischeri.…”

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Mutations in ampG and Lytic Transglycosylase Genes Affect the Net Release of Peptidoglycan Monomers from Vibrio fischeri

et al. 2009

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The light-organ symbiont Vibrio fischeri releases N-acetylglucosaminyl-1,6-anhydro-N-acetylmuramylalanyl-␥-glutamyldiaminopimelylalanine, a disaccharide-tetrapeptide component of peptidoglycan that is referred to here as "PG monomer." In contrast, most gram-negative bacteria recycle PG monomer efficiently, and it does not accumulate extracellularly. PG monomer can stimulate normal light-organ morphogenesis in the host squid Euprymna scolopes, resulting in regression of ciliated appendages similar to that triggered by infection with V. fischeri. We examined whether the net release of PG monomers by V. fischeri resulted from lytic transglycosylase activity or from defects in AmpG, the permease through which PG monomers enter the cytoplasm for recycling. An ampG mutant displayed a 100-fold increase in net PG monomer release, indicating that AmpG is functional. The ampG mutation also conferred the uncharacteristic ability to induce light-organ morphogenesis even when placed in a nonmotile flaJ mutant that cannot infect the light-organ crypts. We targeted five potential lytic transglycosylase genes singly and in specific combinations to assess their role in PG monomer release. Combinations of mutations in ltgA, ltgD, and ltgY decreased net PG monomer release, and a triple mutant lacking all three of these genes had little to no accumulation of PG monomers in culture supernatants. This mutant colonized the host as well as the wild type did; however, the mutant-infected squid were more prone to later superinfection by a second V. fischeri strain. We propose that the lack of PG monomer release by this mutant results in less regression of the infection-promoting ciliated appendages, leading to this propensity for superinfection.Microbe-associated molecular patterns (MAMPs) are recognized by hosts in a variety of pathogenic and symbiotic relationships. MAMP is an umbrella term for a variety of semiconserved bacterial molecules, including lipopolysaccharide, lipoproteins, flagella, and peptidoglycan (PG), that are sensed by conserved host surveillance mechanisms (e.g., the innate immune system), triggering context-dependent reactions to bacterial colonization. Mounting evidence shows that PG-derived MAMPs play important and previously underappreciated roles in host-bacterium interactions (11).The PG layer of gram-negative bacteria is a rigid network in the periplasm that protects against osmotic lysis and helps to determine cell size and shape while still allowing diffusion of molecules into the cell (14). In PG, repeated subunits of Nacetylglucosamine and N-acetylmuramic acid are connected to a short pentapeptide side chain of L-alanyl-D-␥-glutamyl-mesodiaminopimelyl-D-alanyl-D-alanine (Ala-Glu-DAP-Ala-Ala). Adjacent peptides are cross-linked through Ala-DAP or DAP-DAP peptide bonds, and side chains are converted to tetra-, tri-, and dipeptides through the action of carboxypeptidases in the periplasm (19,49).Despite its mechanical stability, PG is a dynamic structure that undergoes remodeling and recycling. Murein hydrola...

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Section: Resultsmentioning

confidence: 99%

Section: Continued On Following Pagementioning

confidence: 99%

mentioning

confidence: 99%

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Mutations in ampG and Lytic Transglycosylase Genes Affect the Net Release of Peptidoglycan Monomers from Vibrio fischeri

et al. 2009

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“…The symbiont induces postembryonic light-organ development (19), and the organ morphology reaches maturity in 4 wk (20). Host-derived chitin, a polymeric glycan of N-acetylglucosamine, is known to promote the speciesspecific colonization of the squid by V. fischeri (21).…”

Section: Significancementioning

confidence: 99%

The chemistry of negotiation: Rhythmic, glycan-driven acidification in a symbiotic conversation

Schwartzman

Koch

Heath‐Heckman

et al. 2014

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

117

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Glycans have emerged as critical determinants of immune maturation, microbial nutrition, and host health in diverse symbioses. In this study, we asked how cyclic delivery of a single host-derived glycan contributes to the dynamic stability of the mutualism between the squid Euprymna scolopes and its specific, bioluminescent symbiont, Vibrio fischeri. V. fischeri colonizes the crypts of a host organ that is used for behavioral light production. E. scolopes synthesizes the polymeric glycan chitin in macrophage-like immune cells called hemocytes. We show here that, just before dusk, hemocytes migrate from the vasculature into the symbiotic crypts, where they lyse and release particulate chitin, a behavior that is established only in the mature symbiosis. Diel transcriptional rhythms in both partners further indicate that the chitin is provided and metabolized only at night. A V. fischeri mutant defective in chitin catabolism was able to maintain a normal symbiont population level, but only until the symbiotic organ reached maturity (∼4 wk after colonization); this result provided a direct link between chitin utilization and symbiont persistence. Finally, catabolism of chitin by the symbionts was also specifically required for a periodic acidification of the adult crypts each night. This acidification, which increases the level of oxygen available to the symbionts, enhances their capacity to produce bioluminescence at night. We propose that other animal hosts may similarly regulate the activities of epithelium-associated microbial communities through the strategic provision of specific nutrients, whose catabolism modulates conditions like pH or anoxia in their symbionts' habitat.symbiosis | squid-vibrio | metabolism | chitin

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“…Specifically, the crypt epithelium, which interfaces directly with the symbionts, undergoes a reversible increase in the microvillar density of the apical sur-faces of the crypt cells (21) and an induction of edema in these cells (41). In contrast, the superficial ciliated fields, which are remote from the symbionts occupying the crypt spaces, undergo a 4-day program of regression that only requires a 12-h exposure to the symbionts (4,27). In addition to these initial events, the symbiosis is characterized by a daily rhythm (12,29).…”

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Symbiont-Induced Changes in Host Actin during the Onset of a Beneficial Animal-Bacterial Association

Kimbell

McFall‐Ngai

2004

Appl Environ Microbiol

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The influence of bacteria on the cytoskeleton of animal cells has been studied extensively only in pathogenic associations. We characterized changes in host cytoskeletal actin induced by the bacterial partner during the onset of a cooperative animal-bacteria association using the squid-vibrio model. Two-dimensional sodium dodecyl sulfate-polyacrylamide gel electrophoresis and Western blot analysis revealed that Vibrio fischeri induced a dramatic increase in actin protein abundance in the bacteria-associated host tissues during the onset of the symbiosis. Immunocytochemistry revealed that this change in actin abundance correlated with a two-to threefold increase in actin in the apical cell surface of the epithelium-lined ducts, the route of entry of symbionts into host tissues. Real-time reverse transcriptase PCR and in situ hybridization did not detect corresponding changes in actin mRNA. Temporally correlated with the bacteria-induced changes in actin levels was a two-to threefold decrease in duct circumference, a 20% loss in the average number of cells interfacing with the duct lumina, and dramatic changes in duct cell shape. When considered with previous studies of the biomechanical and biochemical characteristics of the duct, these findings suggest that the bacterial symbionts, upon colonizing the host organ, induce modifications that physically and chemically limit the opportunity for subsequent colonizers to pass through the ducts. Continued study of the squid-vibrio system will allow further comparisons of the mechanisms by which pathogenic and cooperative bacteria influence cytoskeleton dynamics in host cells.

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A Transient Exposure to Symbiosis-Competent Bacteria Induces Light Organ Morphogenesis in the Host Squid

Cited by 91 publications

References 27 publications

Mutations in ampG and Lytic Transglycosylase Genes Affect the Net Release of Peptidoglycan Monomers from Vibrio fischeri

Mutations in ampG and Lytic Transglycosylase Genes Affect the Net Release of Peptidoglycan Monomers from Vibrio fischeri

The chemistry of negotiation: Rhythmic, glycan-driven acidification in a symbiotic conversation

Symbiont-Induced Changes in Host Actin during the Onset of a Beneficial Animal-Bacterial Association

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