Heliorhodopsin evolution is driven by photosensory promiscuity in monoderms

Abstract

The ability to harness Sun’s electromagnetic radiation by channeling it into high-energy phosphate bonds empowered microorganisms to tap into a cheap and inexhaustible source of energy. Life’s billion-years history of metabolic innovations led to the emergence of only two biological complexes capable of harvesting light: one based on rhodopsins and the other on (bacterio)chlorophyll. Rhodopsins encompass the most diverse and abundant photoactive proteins on Earth and were until recently canonically split between type-1 (microbial rhodopsins) and type-2 (animal rhodopsins) families. Unexpectedly, the long-lived type-1/type-2 dichotomy was recently amended through the discovery of heliorhodopsins (HeRs) (Pushkarev et al. 2018), a novel and exotic family of rhodopsins (i.e. type-3) that evaded recognition in our current homology-driven scrutiny of life’s genomic milieu. Here, we bring to resolution the debated monoderm/diderm occurrence patterns by conclusively showing that HeR distribution is restricted to monoderms. Furthermore, through investigating protein domain fusions, contextual genomic information, and gene co-expression data we show that HeRs likely function as generalised light-dependent switches involved in the mitigation of light-induced oxidative stress and metabolic circuitry regulation. We reason that HeR’s ability to function as sensory rhodopsins is corroborated by their photocycle dynamics (Pushkarev et al. 2018) and that their presence and function in monoderms is likely connected to the increased sensitivity to light-induced damage of these organisms (Maclean et al. 2009).