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Heliorhodopsin evolution is driven by photosensory promiscuity in monoderms
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modified on 2021-11-18, 17:28 Rhodopsins are light-activated proteins displaying an enormous versatility
of function as cation/anion pumps or sensing environmental stimuli and are widely distributed
across all domains of life. Even with wide sequence divergence and uncertain
evolutionary linkages between microbial (type 1) and animal (type 2) rhodopsins, the
membrane orientation of the core structural scaffold of both was presumed universal.
This was recently amended through the discovery of heliorhodopsins (HeRs; type 3),
that, in contrast to known rhodopsins, display an inverted membrane topology and yet
retain similarities in sequence, structure, and the light-activated response. While no ionpumping
activity has been demonstrated for HeRs and multiple crystal structures are
available, fundamental questions regarding their cellular and ecological function or
even their taxonomic distribution remain unresolved. Here, we investigated HeR function
and distribution using genomic/metagenomic data with protein domain fusions,
contextual genomic information, and gene coexpression analysis with strand-specific
metatranscriptomics. We bring to resolution the debated monoderm/diderm occurrence
patterns and show that HeRs are restricted to monoderms. Moreover, we provide
compelling evidence that HeRs are a novel type of sensory rhodopsins linked to histidine
kinases and other two-component system genes across phyla. In addition, we also
describe two novel putative signal-transducing domains fused to some HeRs. We posit
that HeRs likely function as generalized light-dependent switches involved in the mitigation
of light-induced oxidative stress and metabolic circuitry regulation. Their role as
sensory rhodopsins is corroborated by their photocycle dynamics and their presence/
function in monoderms is likely connected to the higher sensitivity of these organisms
to light-induced damage.