Shared in planta population and transcriptomic features of nonpathogenic members of endophytic phyllosphere microbiota

Plants and animals are in constant association with a variety of microbes. Although much is known about how pathogenic and symbiotic microbes interact with plants, less is known about the population dynamics, adaptive traits, and transcriptional features of the vast number of microbes that make up the bulk of the plant microbiota. The majority of microbiota taxa are either commensal, natural mutants of pathogens, or pathogens that encounter strong immune responses due to plant recognition of pathogen effectors. How these “nonpathogenic” microbes interact with plants is poorly understood, especially during long-term, steady-state interactions, which are more reflective of plant–microbiota interactions in nature. In this study, we embarked upon long-term population and in planta transcriptomic studies of commensal endophytic bacteria and compared them to nonpathogenic or effector-triggered immunity-inducing strains of the bacterial pathogen Pseudomonas syringae. Our results led to the discovery of multiplication–death equilibrium as a common basis for the shared long-term static population densities of these bacteria. A comprehensive in planta transcriptomic analysis using multiple time points after inoculation revealed a striking similarity between the transcriptomic features of nonpathogenic P. syringae to that of bacteria in stationary phase in vitro, a metabolically active physiological state in which the production of adaptive secondary metabolites and stress responses are induced. We propose that the long-term population and transcriptomic features of nonpathogenic bacteria captured in this study likely reflect the physiological steady state encountered by the bulk of endophytic microbiota—excluding virulent pathogens—in their life-long interactions with plants in nature.