The External Microbiome Communicates with the Developing Zebrafish (Danio rerio) Embryo Through the Protective Chorion and Influences Developmental Trajectory

Abstract

AbstractThe commensal microbiome plays a significant role in shaping host physiological processes including energy metabolism and neurobiology. However, current knowledge on host-microbiome interactions is limited to effects of the microbiome during post-embryonic development. Elucidating mechanisms and consequences of host-microbe communication during embryonic development, particularly in oviparous organisms is a notable gap. Protected from the chorionic fluid and considered to be sterile, embryonic development in oviparous organisms is typically considered to be independent of the influence of the microbiome. Here, we tested the hypothesis that the external microbiome influences embryonic development in oviparous organisms despite lack of physical contact. We utilized zebrafish (Danio rerio) reared germ-free (GF) and conventionalized with microbes (CV) at different times during embryonic development to examine changes in the embryonic transcriptome, proteome, and physiology during embryogenesis at 32 hours post-fertilization. Our results contrast the conventional notion that zebrafish embryos are shielded from the external microbial environment by their protective chorion until hatching. We demonstrate the external microbial community influences embryonic transcript and protein abundance associated with critical developmental processes including energy metabolism and neurodevelopment. While these pathways are previously identified to be influence by microbes duringpost-embryonic stages, here, we reveal a significant role of the surrounding aquatic microbial community in regulating these processes as early as embryogenesis. Furthermore, we demonstrate the external microbial community differentially regulates cytochrome P450 driven xenobiotic metabolism and associated bioenergetic and behavioral responses following exposure to a CYP1A activator during embryogenesis. These findings transform our interpretation and consideration of embryonic development as a function of microbial cues and genetic blueprints, enhance knowledge of fundamental processes governing vertebrate embryonic development, and expand comprehension of host-microbe communication.