Architecture and Evolution of Prokaryotic Multicellularity: Common Patterns and Diversity

ABSTRACT

Prokaryotes form multicellular structures under both natural and experimental conditions, through developmental processes that sometimes echo those known from eukaryotes. Recent research has increasingly focused on the mechanisms underlying bacterial multicellular organization and its evolutionary origins. In this review, we first consider the modes of group formation, that is, clonal or aggregative, and show how mixed strategies in prokaryotic systems complicate this division. We then survey bacterial and, where known, archaeal multicellular structures, focusing on common patterns and differences in developmental dynamics across species, and highlighting the “soft” similarities with eukaryotic tissues and organismal organization. Next, we discuss the molecular and cellular mechanisms underlying the canonical hallmarks of multicellularity in prokaryotes. Finally, we discuss recent research on the evolution of prokaryotic multicellularity, drawing on experimental, computational, and comparative approaches. Studying the specific forms of prokaryotic multicellularity, beyond simplified descriptions (aggregative vs. clonal), is necessary for understanding its complexity, and its consequences for microbial ecology, biogeochemical cycles and the evolution of bacteria per se. The prevalence of multicellularity in bacteria and emerging evidence from archaea raise the possibility that LUCA already possessed multicellular traits, suggesting that multicellularity may be an ancestral feature of life. The emerging picture is that bacterial multicellularity only partly matches eukaryotic models, instead reflecting multiple independent evolutionary origins and a striking capacity to regenerate and diversify developmental programs.