A secreted antibacterial neuropeptide shapes the microbiome of Hydra

Abstract

Colonization of body epithelial surfaces with a highly specific microbial community is a fundamental feature of all animals, yet the underlying mechanisms by which these communities are selected and maintained are not well understood. Here, we show that sensory and ganglion neurons in the ectodermal epithelium of the model organism hydra (a member of the animal phylum Cnidaria) secrete neuropeptides with antibacterial activity that may shape the microbiome on the body surface. In particular, a specific neuropeptide, which we call NDA-1, contributes to the reduction of Gram-positive bacteria during early development and thus to a spatial distribution of the main colonizer, the Gram-negative Curvibacter sp., along the body axis. Our findings warrant further research to test whether neuropeptides secreted by nerve cells contribute to the spatial structure of microbial communities in other organisms.

Rethinking the Role of the Nervous System: Lessons From the Hydra Holobiont

“…A recent study of Augustin et al provided evidence supporting the first scenario, [37] and showed that some sensory and ganglion neurons express a cationic neuropeptide called NDA-1 ( Figure 3E and F), secrete it into the mucus layer and regulate the spatial distribution of the main colonizer, the Gram-negative bacterium Curvibacter, along the Hydra trunk. The density of Curvibacter colonization is relatively low in the foot and tentacles of Hydra, where NDA-1 is strongly expressed, compared to the body Figure 1.…”

“…All multicellular animals emerged in a world that was already densely populated by microbes, and all extant animals are multiorganismal and colonized by a large number of symbiotic microbes. [43,44] Our recent studies demonstrate the existence of such communication in non-bilaterian animals as well, [24,37] and suggest a universal role of the nervous system in mediating host-microbe interactions throughout the Metazoa. [4] The emergence and evolution of the nervous system must be also considered in the context of host-microbe interactions.…”

“…While previous studies have identified few neuropeptides that have antibacterial activity, [37] these are, clearly, a minute fraction of the Hydra neuron-derived effectors that may mediate the hostmicrobiome interplay. A systematic approach to identifying peptide signalling molecules in Hydra revealed over 800 short peptides and estimated about half of them to be neuronderived.…”

“…[29,34] However, a series of experiments elegantly combining host tissue and microbiota manipulations and biochemical assays together with modern imaging techniques, behavioral recordings and gene manipulation techniques, have recently revealed previously underappreciated roles of the nervous system in host-microbiome crosstalk in Hydra. [35][36][37][38] Thus, in addition to cells of the both epithelial lineages, also distinct differentiation products of the interstitial cell lineage, such as neurons, which have an elaborate secretion system, participate in the interactions with microbes.…”

“…www.advancedsciencenews.com www.bioessays-journal.com Figure 3. [37] Copyright 2017, the authors, published by Springer Nature. A) Nerve cells are localized within both epithelial layers of Hydra, ectoderm and the endoderm.…”