Rethinking the role of immunity and the function of the nervous system

The ability of multicellular organisms to detect and respond to microorganisms is fundamental and has ancient evolutionary origins. Our work has shown that these apparently simple animals provide us with important information in understanding the evolution of epithelial-based innate immunity.Lab_2

The work has contributed to a paradigm shift in evolutionary immunology: components of the innate immune system with its host-specific antimicrobial peptides and a rich repertoire of pattern recognition receptors appear to have evolved in early branching metazoans because of the need to control the resident beneficial microbes rather than because of invasive pathogens. This conclusion is based on studies showing that individuals from different species differ greatly in their microbiota, that specific microbial communities are maintained over long periods of time, and that species-specific antimicrobial peptides account for different bacterial communities associated with closely related species. In sum

  • The hydra immune system evolved because of the need to control resident microbiota
  • Defense against invasive pathogens is secondary to the need to regulate microbiota
  • Antimicrobial peptides have regulatory roles in host-microbe homeostasis and adaptations
  • Developmental pathways (e.g. FoxO) interact with environmental cues such as microbes

Rethinking the Role of the Nervous System

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. Animal evolution, therefore, is deeply influenced by the presence of microbes. The emergence and evolution of the nervous system must be also considered in the context of host-microbe interactions. We have demonstrated that the neuron-bacteria interactions have a deep evolutionary origin, dating back to the emergence of the nervous system itself. This thinking casts a new light on the ancestral role of the nervous system, and supports the view that it was not restricted to conventional sensory-motor coordination. The first nervous systems seem to have mediated the complex interactions between the host and its microbiota, hence maintaining the holobiont. This view indicates a shared functionality between the immune system and the nervous system, pointing to a common evolutionary origin and suggesting that the nervous system evolved as much to sense and control bacteria as to coordinate movements.