Bacterial origin of a key innovation in the evolution of the vertebrate eye

Abstract

The vertebrate eye was described by Charles Darwin as one of the greatest potential challenges to a theory of natural selection by stepwise evolutionary processes. While numerous evolutionary transitions that led to the vertebrate eye have been explained, some aspects appear to be vertebrate specific with no obvious metazoan precursor. One critical difference between vertebrate and invertebrate vision hinges on interphotoreceptor retinoid-binding protein (IRBP, also known as retinol-binding protein, RBP3), which enables the physical separation and specialization of cells in the vertebrate visual cycle by promoting retinoid shuttling between cell types. While IRBP has been functionally described, its evolutionary origin has remained elusive. Here, we show that IRBP arose via acquisition of novel genetic material from bacteria by interdomain horizontal gene transfer (iHGT). We demonstrate that a gene encoding a bacterial peptidase was acquired prior to the radiation of extant vertebrates >500 Mya and underwent subsequent domain duplication and neofunctionalization to give rise to vertebrate IRBP. Our phylogenomic analyses on >900 high-quality genomes across the tree of life provided the resolution to distinguish contamination in genome assemblies from true instances of horizontal acquisition of IRBP and led us to discover additional independent transfers of the same bacterial peptidase gene family into distinct eukaryotic lineages. Importantly, this work illustrates the evolutionary basis of a key transition that led to the vertebrate visual cycle and highlights the striking impact that acquisition of bacterial genes has had on vertebrate evolution.

Horizontal transfer of vertebrate vision gene IRBP into the chordate ancestor

“…Interphotoreceptor retinoid-binding protein (IRBP) plays a key role in vertebrate vision by transporting retinoids between photoreceptor and retinal pigment epithelium cells in the eye. Kalluraya et al ( 1 ) report that vertebrate IRBP arose via horizontal gene transfer (HGT) of a bacterial S41 peptidase into the vertebrate ancestor, followed by domain duplications and neofunctionalization. These events likely occurred >500 ma, concomitant with the emergence of the vertebrate eye ( 1 ), exemplifying functionally coopted HGT in animals.…”

“…Kalluraya et al ( 1 ) report that vertebrate IRBP arose via horizontal gene transfer (HGT) of a bacterial S41 peptidase into the vertebrate ancestor, followed by domain duplications and neofunctionalization. These events likely occurred >500 ma, concomitant with the emergence of the vertebrate eye ( 1 ), exemplifying functionally coopted HGT in animals.…”

“…Kalluraya et al ( 1 ) propose independent HGTs into amphioxus and vertebrates, despite their close relationship within Chordata. However, they also noted difficulty in identifying the closest relatives to vertebrate IRBP and acknowledge that shared HGT is “difficult to completely rule out” ( 1 ).…”

“…Kalluraya et al ( 1 ) propose independent HGTs into amphioxus and vertebrates, despite their close relationship within Chordata. However, they also noted difficulty in identifying the closest relatives to vertebrate IRBP and acknowledge that shared HGT is “difficult to completely rule out” ( 1 ). We performed new phylogenetic analyses of Kalluraya et al’s full-length IRBP sequence alignment and their domain-based alignment using better-fitting site-heterogeneous models that can reduce phylogenetic error ( Fig.…”

Diversification of Ubiquinone Biosynthesis via Gene Duplications, Transfers, Losses, and Parallel Evolution

“…The enormous diversity of the natural products they synthesize is the result of a multitude of enzymes which have diversified over time ( Crits-Christoph et al 2018 ; Paoli et al 2022 ). The evolution of individual enzymes and functional innovation among homologous protein families have been extensively studied, sometimes providing an atomic level of details of a family functional diversification, along with the documentation of the evolutionary events leading to such diversification ( Zou et al 2015 ; Kalluraya et al 2023 ). The role of several phenomena, including enzymatic promiscuity, gene transfers, and gene duplications, has been extensively discussed and reviewed ( Baier et al 2016 ; Glasner et al 2020 ; Jayaraman et al 2022 ).…”