Microbes as part of ancestral neuronal circuits: Bacterial produced signals affect neurons controlling eating behavior inHydra

Abstract

Although recent studies indicate the impact of microbes on the central nervous systems and behavior, it remains unclear how the relationship between the functionality of the nervous system, behavior and the microbiota arise. We studied the eating behavior of Hydra, a host that has a simple nervous system and a low-complexity microbiota. To identify the neuronal subpopulations involved, we used a subpopulation specific cell ablation system and calcium imaging. The role of the microbiota was uncovered by reducing the diversity of the natural microbiota. Here, we demonstrate that different neuronal subpopulations are functioning together to control the eating behavior. The microbiota participates in control of the eating behavior since germ-free or mono-colonized animals have drastic difficulties in mouth opening. This was restored by adding a full complement of the microbiota. In summary, we provide a mechanistic explanation of how the eating behavior is controlled in Hydra and how microbes can affect the neuronal circuit.

The internal metabolic state controls behavior inHydrathrough an interplay of enteric and central nervous system-like neuron populations

“…As Hydra would not have been able to catch prey due to MTZ-treatment, we decided to use artificial food (here glass beads) for testing its ability to swallow the prey. Consistent with previously published data 16 , all N4 ablated animals could open their mouth. Surprisingly, however, they cannot swallow the glass beads and transport them into the gastric cavity ( Fig.…”

“…1 B, Fig. 3C ) 16–18 . First, we examined the N1 neuronal network - previously named contraction burst (CB) - which was correlated with body contractions 17 .…”

“…5A-B ). The endodermal N4 population is distributed along the whole-body axis except for the tentacles with an increase in density in the hypostome area ( Fig 3 C ) 16 . Within the body, the population forms a network composed of ganglion neurons whereas in the head it forms a spiderweb-like structure with ganglion and sensory neurons which extend into the gastrovascular cavity ( Fig.…”

“…3D and G ), and the altered mouth opening duration. To accomplish this, we investigated the neuronal activity during mouth opening with a previously established calcium imaging setup 16 . We observed that the endodermal N4 and the ectodermal N3 neuronal population responded significantly different compared to the starved control ( Fig.…”

“…4E ). N3 has also been proposed to have an inhibitory impact on the eating behavior and the mouth opening 16 . Therefore, we next tested, if the absence of N3 neurons affects the response time or the mouth opening duration in animals 4 hours post feeding.…”