https://www.pnas.org/doi/epdf/10.1073/pnas.2214815120
Significance
Since the time of Charles Darwin, explaining the stepwise
evolution of the eye has been a challenge. Here, we describe
the essential contribution of bacteria to the evolution of
the vertebrate eye, via interdomain horizontal gene transfer
(iHGT), of a bacterial gene that gave rise to the
vertebrate-specific interphotoreceptor retinoid-binding
protein (IRBP). We demonstrate that IRBP, a highly conserved
and essential retinoid shuttling protein, arose from a
bacterial gene that was acquired, duplicated, and
neofunctionalized coincident with the development of the
vertebrate-type eye >500 Mya. Importantly, our findings
provide a path by which complex structures like the vertebrate
eye can evolve: not just by tinkering with existing genetic
material, but also by acquiring and functionally integrating
foreign genes.
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.
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