Individual proteins can dynamically encode environmental information through intramolecular competition between sensory domains, as demonstrated by BcLOV4 and its homologues, which generate light- and temperature-conditioned activity pulses through competitive interactions between a light-sensing LOV domain and a modular temperature-sensing domain that regulate clustering and membrane translocation. This dynamic response mechanism has been conserved across over 300 million years of fungal evolution, with characteristic thermal switch points adapted to match the ecological niches of host organisms ranging from Antarctic to thermophilic environments, revealing fundamental principles for time-varying protein activation and suggesting functional importance for environmentally-conditioned protein dynamics.

Proteins are information processors, but their computations are typically considered at steady state. Here we find that individual proteins can dynamically encode information about their environment and that such response dynamics have been conserved throughout evolution. The fungal protein BcLOV4 exhibits pulsatory light responses shaped by the magnitude of environmental light and temperature. Response adaptation resulted from competitive interactions between domains that sensed either light or temperature. Temperature-sensing was encoded in a modular domain and could be tuned by mutations within co-evolved loops. Photo-thermal response dynamics were conserved in homologues from fungi that diverged >300 million years ago, and the characteristic temperature of pulsatory responses had adapted to match the ecological niche of the hosts, ranging from Antarctica to thermal ponds. These findings uncover a class of dynamic proteins, determine molecular principles of time-varying protein activation, and suggest functional importance for light- and temperature-conditioned protein activity pulses.

Individual proteins can dynamically encode information through interactions between their component domains, revealing principles for complex signal processing in natural and engineered proteins.