Vibrio fisheri: Squid Symbiosis

Stabb, Eric V.; Visick, Karen L.

doi:10.1007/978-3-642-30194-0_22

Cited by 36 publications

(11 citation statements)

References 204 publications

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“…We predict that host provision of chitin sugars to symbionts will both decrease respiratory activity and promote luminescence ( Fig. 5 ), thereby supporting the functional basis of the squid-vibrio mutualism ( 11 ).…”

Section: Discussionsupporting

confidence: 59%

“…Vibrio fischeri can exist both free-living in seawater and as the specific symbiont of the squid, Euprymna scolopes ( 10 ). In the latter, V. fischeri colonizes epithelium-lined crypt spaces in the squid’s light-emitting organ, a structure anatomically designed to use bacterium-produced luminescence during the host’s nocturnal activities ( 11 ). Each newly hatched squid must obtain an inoculum of V. fischeri from the ambient seawater; these bacteria quickly proliferate in the crypts, where the symbiont population reaches a high density, and luminescence is induced by quorum signaling ( 12 ).…”

Section: Introductionmentioning

confidence: 99%

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A Single Host-Derived Glycan Impacts Key Regulatory Nodes of Symbiont Metabolism in a Coevolved Mutualism

Pan

Schwartzman

Dunn

et al. 2015

mBio

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Most animal-microbe mutualistic associations are characterized by nutrient exchange between the partners. When the host provides the nutrients, it can gain the capacity to shape its microbial community, control the stability of the interaction, and promote its health and fitness. Using the bioluminescent squid-vibrio model, we demonstrate how a single host-derived glycan, chitin, regulates the metabolism of Vibrio fischeri at key points in the development and maintenance of the symbiosis. We first characterized the pathways for catabolism of chitin sugars by V. fischeri, demonstrating that the Ccr-dependent phosphoenolpyruvate-pyruvate phosphotransferase system (PTS) prioritizes transport of these sugars in V. fischeri by blocking the uptake of non-PTS carbohydrates, such as glycerol. Next, we found that PTS transport of chitin sugars into the bacterium shifted acetate homeostasis toward a net excretion of acetate and was sufficient to override an activation of the acetate switch by AinS-dependent quorum sensing. Finally, we showed that catabolism of chitin sugars decreases the rate of cell-specific oxygen consumption. Collectively, these three metabolic functions define a physiological shift that favors fermentative growth on chitin sugars and may support optimal symbiont luminescence, the functional basis of the squid-vibrio mutualism.

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Section: Discussionsupporting

confidence: 59%

Section: Introductionmentioning

confidence: 99%

A Single Host-Derived Glycan Impacts Key Regulatory Nodes of Symbiont Metabolism in a Coevolved Mutualism

Pan

Schwartzman

Dunn

et al. 2015

mBio

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“…Previous work has shown that an acidic crypt pH potentiates the release of oxygen from hemocyanin (34) at the time when the symbiont's nocturnal light production increases (33). Thus, the host's cyclic provision of chitin, coupled with the symbionts' physiological responses to this rhythm, regulates the output of bioluminescence, the central product of the association (17). To acidify the light-organ crypts to their nighttime pH of ∼5.5 (34) would require an amount of acetate released by catabolism of 11 μg of COS; we estimate that this amount of substrate could be transported into the crypts by ∼2,000 hemocytes or 5% of the total circulating population (SI Calculations) (35,44).…”

Section: Discussionmentioning

confidence: 99%

“…The squid-vibrio symbiosis occurs within the light-emitting organ of E. scolopes and is based on the bacterium's production of bioluminescence (17), which the host uses in its nocturnal behaviors, such as foraging and camouflage. The symbionts are obtained through horizontal transmission from the ambient seawater by each generation of juvenile squid (18) and are cultured in the epithelium-lined crypts of the light organ (Fig.…”

mentioning

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.

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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“…Recent reviews(63; 83) on the biology of symbiont, Vibrio fischeri, provide a detailed up-to-date summary of what is known about V. fischeri as a species, both in symbiosis as well as in other ecological niches. Here, I will focus my efforts on a review of what is known about the development of the symbiosis, the interplay between partners that mediates this developmental program, and the near and far horizons of the system.…”

Section: Introduction – It’s a New Day For Developmental Biologymentioning

confidence: 99%

The Importance of Microbes in Animal Development: Lessons from the Squid-Vibrio Symbiosis

McFall‐Ngai

2014

Annu. Rev. Microbiol.

221

231

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Developmental biology is among the many sub-disciplines of the life sciences being transformed by our increasing awareness of the role of coevolved microbial symbionts in health and disease. Most symbioses are horizontally acquired, i.e., begin anew each generation. In such associations, the embryonic period prepares the animal to engage with the coevolved partner(s) with fidelity following birth or hatching into the environment. Once interactions are underway, the microbial partners drive maturation of tissues that are either directly associated with or distant from the symbiont populations. Animal alliances often involve complex microbial communities, such as those in the vertebrate gastrointestinal tract. A series of simpler model systems is providing insight into the basic ‘rules’ and principles that govern the establishment and maintenance of stable animal-microbe partnerships. This review focuses upon what biologists have learned about the developmental trajectory of horizontally acquired symbioses through the study of the binary squid-vibrio model.

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Vibrio fisheri: Squid Symbiosis

Cited by 36 publications

References 204 publications

A Single Host-Derived Glycan Impacts Key Regulatory Nodes of Symbiont Metabolism in a Coevolved Mutualism

A Single Host-Derived Glycan Impacts Key Regulatory Nodes of Symbiont Metabolism in a Coevolved Mutualism

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

The Importance of Microbes in Animal Development: Lessons from the Squid-Vibrio Symbiosis

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