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

• Published in: Proceedings of the National Academy of Sciences - PNAS 2015-01, Vol.112 (2), p.566-571
• Main Authors: Schwartzman, Julia A., Koch, Eric, Heath-Heckman, Elizabeth A. C., Zhou, Lawrence, Kremer, Natacha, McFall-Ngai, Margaret J., Ruby, Edward G.
• Format: Article
• Language: English
• Subjects: Acidification; Aliivibrio fischeri - genetics; Aliivibrio fischeri - metabolism; Amino Acid Sequence; Animals; Anoxia; Bacteriology; Base Sequence; Biochemistry, Molecular Biology; Biodiversity; Biodiversity and Ecology; Biological Sciences; Bioluminescence; Chitin; Chitin - genetics; Chitin - metabolism; Darkness; Decapodiformes - genetics; Decapodiformes - metabolism; Decapodiformes - microbiology; DNA - genetics; Ecology, environment; Environmental Sciences; Euprymna scolopes; Genes, Bacterial; Genomics; Hemocytes - metabolism; Hexosaminidases - genetics; Hexosaminidases - metabolism; Hydrogen-Ion Concentration; Life Sciences; Luminescence; Metabolism; Microbial activity; Microbiology; Microbiology and Parasitology; Molecular biology; Molecular Sequence Data; Mollusks; Mutation; Mutualism; Oligosaccharides - genetics; Oligosaccharides - metabolism; Polysaccharides - metabolism; Populations and Evolution; Scolopes; Shellfish; Symbiosis; Symbiosis - genetics; Symbiosis - physiology; Vibrio fischeri; Virology
• ISSN: 0027-8424; 1091-6490
• DOI: 10.1073/pnas.1418580112

Significance The chemical dialog through which a host promotes long-term symbioses with particular microbial partners remains largely unexplored, especially within complex consortia like the human microbiota. Natural, monospecific associations, including that between bobtail squid and Vibrio fischeri , have proved useful for discovering shared strategies, such as rhythmic microbial signaling and symbiosis-induced development, subsequently found in mammalian associations. Here, we demonstrate that symbiont metabolism is driven by a diel provision of a squid-derived glycan, resulting in tissue acidification. This event alters bacterial physiology, favoring the cyclic production of bioluminescence, the functional basis of the symbiosis. More generally, studies of this association can help reveal mechanisms by which other hosts modulate the chemistry of symbiosis to regulate microbial community function. 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 strategi