Bioluminescence in the symbiotic squid Euprymna scolopes is controlled by a daily biological rhythm

Boettcher, Katherine J.; Ruby, Edward G.; McFall‐Ngai, Margaret J.

doi:10.1007/bf00193435

Cited by 101 publications

(100 citation statements)

References 24 publications

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“…4D). 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).…”

Section: Discussionmentioning

confidence: 99%

“…The remaining symbiont cells repopulate the light organ within hours, by growing on substrates including amino acids and glycerophospholipids (23,24), eventually providing the squid's nocturnal bioluminescence. Light emission, which requires oxygen (32), is highest during the night (33). In the fully developed light organ, where the symbionts are oxygen limited (24,33), the diel bioluminescent rhythm is potentiated by an acidic crypt environment, which creates a Bohr effect that releases oxygen from the carrier protein, hemocyanin (34).…”

Section: Significancementioning

confidence: 99%

“…Light emission, which requires oxygen (32), is highest during the night (33). In the fully developed light organ, where the symbionts are oxygen limited (24,33), the diel bioluminescent rhythm is potentiated by an acidic crypt environment, which creates a Bohr effect that releases oxygen from the carrier protein, hemocyanin (34). Here, we demonstrate that, in this mature state of light-organ development, the cyclic provision of COS to symbionts, combined with their fermentation of this glycan, leads to the nightly acidification of the symbiont-containing extracellular crypts.…”

Section: Significancementioning

confidence: 99%

See 2 more Smart Citations

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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Section: Discussionmentioning

confidence: 99%

Section: Significancementioning

confidence: 99%

Section: Significancementioning

confidence: 99%

See 1 more Smart Citation

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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“…1A). Bioluminescence produced by the symbiont is used in the host's nocturnal behaviors, and varies in intensity over the day largely due to oxygen limitation in the organ, with the lowest levels occurring from just before dawn through early afternoon, and the highest during the night (10). Superimposed on this rhythm of light production is the diel expulsion of most of the bacterial population each dawn, followed by a period of regrowth by the remaining symbionts (Fig.…”

mentioning

confidence: 99%

Transcriptional patterns in both host and bacterium underlie a daily rhythm of anatomical and metabolic change in a beneficial symbiosis

Wier¹,

Nyholm

Mandel³

et al. 2010

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

152

221

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Mechanisms for controlling symbiont populations are critical for maintaining the associations that exist between a host and its microbial partners. We describe here the transcriptional, metabolic, and ultrastructural characteristics of a diel rhythm that occurs in the symbiosis between the squid Euprymna scolopes and the luminous bacterium Vibrio fischeri. The rhythm is driven by the host's expulsion from its light-emitting organ of most of the symbiont population each day at dawn. The transcriptomes of both the host epithelium that supports the symbionts and the symbiont population itself were characterized and compared at four times over this daily cycle. The greatest fluctuation in gene expression of both partners occurred as the day began. Most notable was an up-regulation in the host of >50 cytoskeleton-related genes just before dawn and their subsequent down-regulation within 6 h. Examination of the epithelium by TEM revealed a corresponding restructuring, characterized by effacement and blebbing of its apical surface. After the dawn expulsion, the epithelium reestablished its polarity, and the residual symbionts began growing, repopulating the light organ. Analysis of the symbiont transcriptome suggested that the bacteria respond to the effacement by up-regulating genes associated with anaerobic respiration of glycerol; supporting this finding, lipid analysis of the symbionts' membranes indicated a direct incorporation of host-derived fatty acids. After 12 h, the metabolic signature of the symbiont population shifted to one characteristic of chitin fermentation, which continued until the following dawn. Thus, the persistent maintenance of the squid-vibrio symbiosis is tied to a dynamic diel rhythm that involves both partners.Euprymna scolopes | microarray | mutualism | Vibrio fischeri | cytoskeleton

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“…Squid hosts use the Vibrio ‐produced light to reduce their silhouette during the evening, which enhances their survivability and predation success (McFall‐Ngai, Heath‐Heckman, Gillette, Peyer & Harvie, 2012). After each nightly foraging session, approximately 95% of the Vibrio bacteria are vented out into the surrounding seawater, seeding the local area with symbiotically viable Vibrios (Boettcher, Ruby & McFall‐Ngai, 1996). Local cycling of symbiotic V. fischeri exposes these bacteria to a wide range of abiotic and biotic factors outside the host that can affect their fitness and ability to infect new hosts.…”

Section: Introductionmentioning

confidence: 99%

Phylogeographic patterns in the Philippine archipelago influence symbiont diversity in the bobtail squid–Vibrio mutualism

Coryell

Turnham

Ayson

et al. 2018

Ecology and Evolution

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Marine microbes encounter a myriad of biotic and abiotic factors that can impact fitness by limiting their range and capacity to move between habitats. This is especially true for environmentally transmitted bacteria that cycle between their hosts and the surrounding habitat. As geologic history, biogeography, and other factors such as water temperature, salinity, and physical barriers can inhibit bacterial movement to novel environments, we chose to examine the genetic architecture of Euprymna albatrossae (Mollusca: Cephalopoda) and their Vibrio fischeri symbionts in the Philippine archipelago using a combined phylogeographic approach. Eleven separate sites in the Philippine islands were examined using haplotype estimates that were examined via nested clade analysis to determine the relationship between E. albatrossae and V. fischeri populations and their geographic location. Identical analyses of molecular variance (AMOVA) were used to estimate variation within and between populations for host and symbiont genetic data. Host animals demonstrated a significant amount of variation within island groups, while symbiont variation was found within individual populations. Nested clade phylogenetic analysis revealed that hosts and symbionts may have colonized this area at different times, with a sudden change in habitat. Additionally, host data indicate restricted gene flow, whereas symbionts show range expansion, followed by periodic restriction to genetic flow. These differences between host and symbiont networks indicate that factors “outside the squid” influence distribution of Philippine V. fischeri. Our results shed light on how geography and changing environmental factors can impact marine symbiotic associations at both local and global scales.

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Bioluminescence in the symbiotic squid Euprymna scolopes is controlled by a daily biological rhythm

Cited by 101 publications

References 24 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

Transcriptional patterns in both host and bacterium underlie a daily rhythm of anatomical and metabolic change in a beneficial symbiosis

Phylogeographic patterns in the Philippine archipelago influence symbiont diversity in the bobtail squid–Vibrio mutualism

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