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

Abstract

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

PF4 Promotes Platelet Production and Lung Cancer Growth

“…This research has discovered that growing tumors can continuously recruit new hematopoietic cells from the circulation by releasing signals that amplify the production of hematopoietic progenitors in remote hematopoietic organs. Long-range tumor-associated signals include osteopontin, a tumor-secreted endocrine factor that activates bone marrow cells (McAllister et al, 2008); G-CSF, a tumor-derived factor that promotes bone marrow myelopoiesis (Casbon et al, 2015) and Angiotensin-II, a peptide hormone that instigates extramedullary monocytopoiesis (Cortez-Retamozo et al, 2013). However, while local immune-neoplastic interactions in the microenvironment are well studied, several aspects of systemically activated tumor-associated immune components remain unclear.…”

The Role of Hemocytes in the Hawaiian Bobtail Squid, Euprymna scolopes: A Model Organism for Studying Beneficial Host–Microbe Interactions

“…In addition to their role in distinguishing between symbiotic and non-symbiotic bacteria, hemocytes have recently been demonstrated to act as a nutrient source for V. fischeri in adult hosts (Schwartzman et al, 2015). Hemocytes have been observed in light organ crypt spaces (Nyholm and McFall-Ngai, 1998) where they increase in numbers during the evening when the symbiont population is greatest (Schwartzman et al, 2015).…”

“…Hemocytes have been observed in light organ crypt spaces (Nyholm and McFall-Ngai, 1998) where they increase in numbers during the evening when the symbiont population is greatest (Schwartzman et al, 2015). Like many other invertebrate hemocytes, blood cells from E. scolopes are rich in chitin (Heath-Heckman and McFall-Ngai, 2011).…”

“…Like many other invertebrate hemocytes, blood cells from E. scolopes are rich in chitin (Heath-Heckman and McFall-Ngai, 2011). This chitin is localized in acidic compartments, presumably lysosomes, and delivered to the symbiotic population of the light organ at night after cell membrane blebbing and lysis of a subset of hemocytes ( Figure 1E ; Schwartzman et al, 2015). Diel transcriptional changes in both host and symbiont revealed an increase in expression of chitinases by the symbiont and chitotriosidase by the host at night (Wier et al, 2010).…”

Ready or Not: Microbial Adaptive Responses in Dynamic Symbiosis Environments

“…In the meantime, the colonization of symbionts causes host hemocyte migration into the crypts of the light organ, where they lyse and release chitin for chitin catabolism among the bacterial symbionts (23). Chitin metabolism acidifies the host tissue and further induces bacterial acid tolerance response and intensifies the bacterial luminescence production right after dusk, facilitating the host nocturnal predation (24). The symbiont microbe-associated molecular patterns (MAMPs) and luminescence also ensure the expression of host cryptochrome protein in the light organ, which is proposed to regulate host circadian behavior (25).…”