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

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 specifi...

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Autores principales: Kalluraya, Chinmay A., Weitzel, Alexander J., Tsu, Brian V., Daugherty, Matthew D.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: National Academy of Sciences 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10120077/
https://www.ncbi.nlm.nih.gov/pubmed/37036996
http://dx.doi.org/10.1073/pnas.2214815120
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author Kalluraya, Chinmay A.
Weitzel, Alexander J.
Tsu, Brian V.
Daugherty, Matthew D.
author_facet Kalluraya, Chinmay A.
Weitzel, Alexander J.
Tsu, Brian V.
Daugherty, Matthew D.
author_sort Kalluraya, Chinmay A.
collection PubMed
description 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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spelling pubmed-101200772023-04-22 Bacterial origin of a key innovation in the evolution of the vertebrate eye Kalluraya, Chinmay A. Weitzel, Alexander J. Tsu, Brian V. Daugherty, Matthew D. Proc Natl Acad Sci U S A Biological Sciences 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. National Academy of Sciences 2023-04-10 2023-04-18 /pmc/articles/PMC10120077/ /pubmed/37036996 http://dx.doi.org/10.1073/pnas.2214815120 Text en Copyright © 2023 the Author(s). Published by PNAS. https://creativecommons.org/licenses/by-nc-nd/4.0/This open access article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND) (https://creativecommons.org/licenses/by-nc-nd/4.0/) .
spellingShingle Biological Sciences
Kalluraya, Chinmay A.
Weitzel, Alexander J.
Tsu, Brian V.
Daugherty, Matthew D.
Bacterial origin of a key innovation in the evolution of the vertebrate eye
title Bacterial origin of a key innovation in the evolution of the vertebrate eye
title_full Bacterial origin of a key innovation in the evolution of the vertebrate eye
title_fullStr Bacterial origin of a key innovation in the evolution of the vertebrate eye
title_full_unstemmed Bacterial origin of a key innovation in the evolution of the vertebrate eye
title_short Bacterial origin of a key innovation in the evolution of the vertebrate eye
title_sort bacterial origin of a key innovation in the evolution of the vertebrate eye
topic Biological Sciences
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10120077/
https://www.ncbi.nlm.nih.gov/pubmed/37036996
http://dx.doi.org/10.1073/pnas.2214815120
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