Initial Symbiont Contact Orchestrates Host-Organ-wide Transcriptional Changes that Prime Tissue Colonization

Kremer, Natacha; Philipp, Eva; Carpentier, Marie-Christine; Brennan, Caitlin A.; Kraemer, Lars; Altura, Melissa A.; Augustin, René; Häsler, Robert; Heath‐Heckman, Elizabeth A. C.; Peyer, Suzanne M.; Schwartzman, Julia; Rader, Bethany A.; Ruby, Edward G.; Rosenstiel, Philip; McFall‐Ngai, Margaret J.

doi:10.1016/j.chom.2013.07.006

Cited by 132 publications

(204 citation statements)

References 47 publications

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“…1D). Collectively, the data are consistent with a model wherein chitin particles within host hemocytes are released into the crypts and become accessible to extracellular hydrolysis by both host and symbiont chitinases (21,24,36).…”

Section: Resultssupporting

confidence: 74%

“…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). Chitin is synthesized by several types of squid tissue, including macrophage-like immune cells called hemocytes (22) (Fig.…”

Section: Significancementioning

confidence: 99%

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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.

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113

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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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Section: Resultssupporting

confidence: 74%

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.

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113

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“…For experimental inoculation of E. scolopes bacterial concentrations of 10 3 -10 6 cfu/mL are typically used (14,15). It was demonstrated that higher inoculum concentrations led to a greater diversity of strains within the light organ, so we used an inoculum of 2 × 10 5 cfu/mL (16,17).…”

Section: Resultsmentioning

confidence: 99%

Global discovery of colonization determinants in the squid symbiontVibrio fischeri

Brooks

Gyllborg

Cronin

et al. 2014

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

102

120

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Animal epithelial tissue becomes reproducibly colonized by specific environmental bacteria. The bacteria (microbiota) perform critical functions for the host's tissue development, immune system development, and nutrition; yet the processes by which bacterial diversity in the environment is selected to assemble the correct communities in the host are unclear. To understand the molecular determinants of microbiota selection, we examined colonization of a simplified model in which the light organ of Euprymna scolopes squid is colonized exclusively by Vibrio fischeri bacteria. We applied highthroughput insertion sequencing to identify which bacterial genes are required during host colonization. A library of over 41,000 unique transposon insertions was analyzed before and after colonization of 1,500 squid hatchlings. Mutants that were reproducibly depleted following squid colonization represented 380 genes, including 37 that encode known colonization factors. Validation of select mutants in defined competitions against the wild-type strain identified nine mutants that exhibited a reproducible colonization defect. Some of the colonization factors identified included genes predicted to influence copper regulation and secretion. Other mutants exhibited defects in biofilm development, which is required for aggregation in host mucus and initiation of colonization. Biofilm formation in culture and in vivo was abolished in a strain lacking the cytoplasmic chaperone DnaJ, suggesting an important role for protein quality control during the elaboration of bacterial biofilm in the context of an intact host immune system. Overall these data suggest that cellular stress responses and biofilm regulation are critical processes underlying the reproducible colonization of animal hosts by specific microbial symbionts.H umans and other animals are often sterile before birth, from which point they immediately proceed to acquire environmental bacteria (1). The bacteria that reproducibly colonize animal hosts are critical for host tissue development, immune system development, and nutrient acquisition. The selection process by which the functional symbionts take residence in the animal from among the great diversity of environmental microbes is poorly understood, so model systems have been especially valuable to examine how specific patterns of colonization are shaped by the genetic makeup of the bacteria and the host environment (2).The light organ of the Hawaiian bobtail squid, Euprymna scolopes, is colonized exclusively by the Gram-negative luminous bacterium Vibrio fischeri. The host inhabits seawater containing 10 6 bacteria per milliliter, with V. fischeri comprising at most 0.02% of the environmental population (3). E. scolopes hatch without symbionts, but then rapidly acquire environmental bacteria and proceed to select for V. fischeri in a "winnowing" process that ensures colonization by only the specific symbiont (4). The squid-Vibrio system thus presents an opportunity to investigate the processes that underlie acquisition of s...

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“…While the authors tested T6SS1-deficient mutants in vitro, no such data were presented under in vivo conditions. It is well established that chitin-degradation products play a key role in the establishment of the V. fischeri-squid symbiosis (16). As chitin-degradation products induce the T6SS in V. cholerae (12,13), it is conceivable that the same holds true for the T6SS1 of V. fischeri.…”

mentioning

confidence: 86%

Bacterial type VI secretion system facilitates niche domination

Dörr

Blokesch

2018

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

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Initial Symbiont Contact Orchestrates Host-Organ-wide Transcriptional Changes that Prime Tissue Colonization

Cited by 132 publications

References 47 publications

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

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

Global discovery of colonization determinants in the squid symbiontVibrio fischeri

Bacterial type VI secretion system facilitates niche domination

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