Phenotypic plasticity segregates antagonistic species but undermines their coexistence
Abstract
Environmental change often induces novel phenotypes in multiple cohabiting species, yet how such common-cue-induced plasticity shapes their coexistence is largely unknown. Testing this link requires disentangling inducing-environment effects from induced-phenotype effects, which remains elusive. We address this gap using two mutually antagonistic bacterial species, Staphylococcus aureus (Sa) and Pseudomonas aeruginosa (Pa). In habitual salinity, where both bacteria show unicellularity, Pa severely diminished Sa. In contrast, high salinity induced macroscopic cell clustering that spatially segregated Sa and Pa (Sa: bottom-dwelling vertical filament; Pa: top-dwelling horizontal mat), and led to >10-fold higher coexistence than habitual salinity. Counterintuitively, physically inhibiting cell clustering (abolishing segregation) in high salinity led to a further >100-fold higher coexistence (Sa:Pa::~1:1). This was because salinity-induced clustering was adaptive for Pa, but not for Sa: such adaptive plasticity enabled killer Pa to proliferate by monopolizing oxygen, which diminished Sa in a correlated manner, thereby weakening coexistence (mechanistically explained by diffusion-based killing). Hence, although the inducing environment promoted overall coexistence, the induced phenotype undermined it. Community-wide genomics revealed that the high level of coexistence achieved by abolishing segregation in high salinity allowed rapid coculture-specific evolution. Taken together, we uncover how plasticity can appear to promote antagonistic coexistence despite causally undermining it.
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