Abstract

African trypanosomes are devastating human and animal pathogens that cause significant human mortality and limit economic development in sub-Saharan Africa. Studies of trypanosome biology generally consider these protozoan parasites as individual cells in suspension cultures or in animal models of infection. Here we report that the procyclic form of the African trypanosome Trypanosoma brucei engages in social behavior when cultivated on semisolid agarose surfaces. This behavior is characterized by trypanosomes assembling into multicellular communities that engage in polarized migrations across the agarose surface and cooperate to divert their movements in response to external signals. These cooperative movements are flagellum-mediated, since they do not occur in trypanin knockdown parasites that lack normal flagellum motility. We term this behavior social motility based on features shared with social motility and other types of surface-induced social behavior in bacteria. Social motility represents a novel and unexpected aspect of trypanosome biology and offers new paradigms for considering host-parasite interactions.

Highlights

  • Studying microbial life under conditions that promote a singlecell lifestyle has proven very effective for uncovering important aspects of microbial physiology

  • Social interactions among individuals lead to development of multicellular communities with specialized and advantageous capabilities versus single cells

  • The concept of bacteria acting as groups of cells communicating and cooperating with one another has had a major impact on our understanding of bacterial physiology and pathogenesis, but this paradigm has not been applied to parasitic protozoa

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Summary

Introduction

Studying microbial life under conditions that promote a singlecell lifestyle has proven very effective for uncovering important aspects of microbial physiology. Social interactions among cells in a population effectively give rise to multicellular communities having specialized functionalities and offering advantages over a unicellular lifestyle. Some of these advantages include increased protection from external antagonists, such as desiccation or host defenses, access to nutrients, exchange of genetic information and enhanced ability to colonize, penetrate and migrate on surfaces [1,2,11]. In bacterial and fungal pathogens, social interactions have major influences on microbial physiology and disease pathogenesis and considering multicellularity as a general property of bacteria has profoundly changed our understanding of microbiology [1,2,3,6]

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