Abstract
ABSTRACTAssociations between animals and microbes affect not only the immediate tissues where they occur, but also the entire host. Metabolomics, the study of small biomolecules generated during metabolic processes, provides a window into how mutualistic interactions shape host biochemistry. The Hawaiian bobtail squid, Euprymna scolopes, is amenable to metabolomic studies of symbiosis because the host can be reared with or without its species-specific symbiont, Vibrio fischeri. In addition, unlike many invertebrates, the host squid has a closed circulatory system. This feature allows a direct sampling of the refined collection of metabolites circulating through the body, a focused approach that has been highly successful with mammals. Here, we show that rearing E. scolopes without its natural symbiont significantly affected one-quarter of the more than 100 hemolymph metabolites defined by gas chromatography mass spectrometry analysis. Furthermore, as in mammals, which harbor complex consortia of bacterial symbionts, the metabolite signature oscillated on symbiont-driven daily rhythms and was dependent on the sex of the host. Thus, our results provide evidence that the population of even a single symbiont species can influence host hemolymph biochemistry as a function of symbiotic state, host sex and circadian rhythm.
Highlights
Mutualistic interactions between animals and their microbial symbionts are stabilized by the exchange of biomolecules throughout the lifespan of the host
The E. scolopes hemolymph metabolome is complex, and rich in amines and carbohydrates Sampling body fluids of animals and analysing them with untargeted metabolomic methods allows for discrete determination of metabolic changes over time
In this first study of the host metabolome in the squid–vibrio symbiosis, we chose to focus on the hemolymph to compare features influencing changes in blood chemistry that have been characterized in mammals, influence of symbiosis, daily rhythms and sex of the host
Summary
Mutualistic interactions between animals and their microbial symbionts are stabilized by the exchange of biomolecules throughout the lifespan of the host. The human intestinal microbiota ferments indigestible polysaccharides into short-chain fatty acids that can be used by the host, while the symbionts receive an energetic benefit from the catabolic process (Bäckhed et al, 2005). Such host–microbe interactions may occur in a particular tissue location, the molecules generated have far-reaching and lasting effects, e.g. a change in the microbes present in the mammalian gut affects metabolism in the brain and eye The diversity found within consortial associations, such as in the mammalian gut, creates a significant challenge to understanding the role of individual microbial species in the exchange of biomolecules and the chemical signature of the metabolome
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