A Case Study of Eukaryogenesis: The Evolution of Photoreception by Photolyase/Cryptochrome Proteins

Abstract

Eukaryogenesis, the origin of the eukaryotes, is still poorly understood. Herein, we show how a detailed all-kingdom phylogenetic analysis overlaid with a map of key biochemical features can provide valuable clues. The photolyase/cryptochrome family of proteins are well known to repair DNA in response to potentially harmful effects of sunlight and to entrain circadian rhythms. Phylogenetic analysis of photolyase/cryptochrome protein sequences from a wide range of prokaryotes and eukaryotes points to a number of horizontal gene transfer events between ancestral bacteria and ancestral eukaryotes. Previous experimental research has characterised patterns of tryptophan residues in these proteins that are important for photoreception, specifically a tryptophan dyad, a canonical tryptophan triad, an alternative tryptophan triad, a tryptophan tetrad and an alternative tetrad. Our results suggest that the spread of the different triad and tetrad motifs across the kingdoms of life accompanied the putative horizontal gene transfers and is consistent with multiple bacterial contributions to eukaryogenesis.

The Gain and Loss of Cryptochrome/Photolyase Family Members during Evolution

“…For this reason, we emphasize that this study only reflects the current state of knowledge, especially of annotated protein sequences until February 2022. Nonetheless, the high agreement of our results with the available literature reinforces our findings [ 19 , 20 , 43 , 44 ]. Furthermore, the additional protein motif analyses performed corroborate the accuracy of the individual CRY/PL members and their assignment to the subfamilies.…”

“…Photolyases are ancient DNA repair enzymes thought to have evolved before atmospheric oxygenation and the formation of the ozone layer [ 19 , 20 , 45 , 46 ]. They were crucial at those times as intense UV radiation could reach the surface of the Earth without attenuation by the ozone layer [ 45 , 47 ].…”

“…The light-insensitive MCRYs, first discovered in the mouse M. musculus [ 18 ] overtook the function of Drosophila TIM and work as transcriptional repressors, inhibiting their own transcription ( Figure 1 E). Due to their high similarity, especially in terms of protein sequences, DCRYs and MCRYs are often grouped together as animal CRYs [ 19 , 20 , 21 ].…”

“…(3) What circumstances favor the presence of certain CRY/PL family members? Several studies have already examined the phylogenetic relationships between various CRY/PL members [ 19 , 20 , 38 ]. Other studies have additionally investigated the specific roles of CRY/PL members in particular species [ 29 , 30 , 39 , 40 ].…”

A bifunctional CPD/(6-4)- photolyase from the cyanobacteria Synechococcus sp. PCC 7335 constitutes an UV-B inducible operon: new insights into photolyases phylogenetic evolution

“…Several ancestors for the CPF family have been proposed (Mei and Dvornyk, 2015; Miles et al, 2020; Vechtomova et al, 2020). After analyzing three different phylogenetic tree topologies, we found that positioning of SPL proteins as root retrieves the tree with lesser functional changes during evolution.…”