Evolutionary Origins of the Blood Vascular System in Metazoans – A Microbial Perspective

François Papale, Louis-Patrick Haraoui 

This opinion piece posits two intertwined major evolutionary transformations – the advent of the circulatory system in animals and the subsequent emergence of sterile organismal compartments it enabled – as promoted by microbial communities. These transformations should be considered significant in that they shaped the ability of downstream multicellular organisms to diverge and attain new levels of specialization. We rely on evolutionary, metabolic, developmental and biophysical considerations to argue for the essential roles played by microbial communities in the emergence of vascular systems in animals. We also briefly allude to similar phenomena occurring independently in plants2,3, suggesting a form of parallel evolution. In developing our arguments, we highlight issues with the uses of the sterile vs. non-sterile dichotomy in scientific disciplines focusing on animal-microbial interactions, demonstrate how adopting this distinction has promoted inaccurate frameworks about how to conceptualize these interactions, and offer important correctives to better understand the role of microbes in shaping animal evolution and development.

a We use the term “sterile” to refer to tissues, organs or compartments whose cells and fluids have no direct physical contact with free-living microbes 1. Endosymbiotic bacteria are not free-living and can therefore be found in “sterile” sites.