Spontaneous body contractions are modulated by the microbiome of Hydra

Abstract

Spontaneous contractile activity, such as gut peristalsis, is ubiquitous in animals and is driven by pacemaker cells. In humans, disruption of the contraction pattern leads to gastrointestinal conditions, which are also associated with gut microbiota dysbiosis. Spontaneous contractile activity is also present in animals lacking gastrointestinal tract. Here we show that spontaneous body contractions in Hydra are modulated by symbiotic bacteria. Germ-free animals display strongly reduced and less regular contraction frequencies. These effects are partially restored by reconstituting the natural microbiota. Moreover, soluble molecule(s) produced by symbiotic bacteria may be involved in contraction frequency modulation. As the absence of bacteria does not impair the contractile ability itself, a microbial effect on the pacemakers seems plausible. Our findings indicate that the influence of bacteria on spontaneous contractile activity is present in the early-branching cnidarian hydra as well as in Bilateria, and thus suggest an evolutionary ancient origin of interaction between bacteria and metazoans, opening a window into investigating the roots of human motility disorders.

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

“…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.…”

“…[17]). The combination of diverse in vitro techniques, such as in situ hybridization, [20] immunofluorescence, [12] and electrophysiological measurements, [21,22] and recently developed in vivo imaging [23] and behavioral recordings, [24] promises deep insights into the molecular architecture and function of the nervous system in Hydra (for review see ref. [18,19] In addition to this conventional role in coordinating motor activities, the nervous system in Hydra appears to be orchestrating other organismal functions, such as development, tissue homeostasis, and immune function.…”

“…Key observations providing evidence for the intricate dialogue between the nervous system in Hydra and its commensal microbiota. [24] Copyright 2017, the authors, published by Springer Nature. Some neurons reach the surface of epithelium, where they secrete antimicrobial peptides and contribute to production of the glycocalyx.…”

“…[24] Germ-free animals display strongly reduced and less regular spontaneous body contraction frequencies ( Figure 3H-J). Recently, we showed that symbiotic bacteria modulate the nervous system activity and behavior in Hydra.…”

“…[51][52][53][54] Remarkably, in both cases sensory neurons directly bind the inducer and trigger metamorphosis by secreting a GLW-family neuropeptide. [24] [41,43,57,58] We propose that a systems biology approach based on deep transcriptomic and metabolomic analysis of microbes associated with Hydra, combined with a survey of existing complete genomic sequences of all major colonizers of Hydra (Fraune and Bosch, unpublished), may lead to identification of the bacteria-derived neuroactive molecules.…”