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

Abstract

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

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

“…1A), and has also been implicated, along with amino acids (23), as a nutrient provided to the symbiont population. Specifically, transcription of V. fischeri genes associated with the fermentation of chitin oligosaccharides (COS) is elevated during the nocturnal, bioluminescent phase of the symbiosis (24) (Fig. 1A).…”

“…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.…”

“…1A). 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).…”

Exploring host–microbiota interactions in animal models and humans

“…Interestingly, the squid and V. fischeri symbiosis follows a diel rhythm, temporal pattern, where each dawn, the squid expel the majority of bacteria from their light organ, allowing the remaining V. fischeri to regrow during the day. Both the squid and the symbiont undergo profound changes throughout this diel cycle (Wier et al 2010), but perhaps the most obvious difference is the increased microbial luminescence that occurs at night and during the squid's active period. These observations raise curiosity about how day-night cycle changes in light, temperature, and nutrient availability impact animal-microbe symbioses.…”

Ready or Not: Microbial Adaptive Responses in Dynamic Symbiosis Environments

“…At dawn, the adult squid expels the contents of the light organ, including the bulk of the symbiont population (19), and the light organ epithelium undergoes morphological changes that alter local environment (20,21). Such host environmental changes are synchronized with symbiotic bacterial transcription profiles to express glycerol metabolism genes that support symbiont growth on host-derived glycerol substrates during the day (22). Based on transcriptomic and other data, it appears that bacterial growth in turn initiates a chemical dialog between host and microbe that allows each to adapt in anticipation of nightfall.…”