Tracing the paths of modular evolution by quantifying rearrangement events of protein domains

Abstract Background Protein evolution is central to molecular adaptation and largely characterized by modular rearrangements of domains, the evolutionary and structural building blocks of proteins. Genetic events underlying protein rearrangements are relatively rare compared to changes of amino-acid...

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Main Authors: Abdulbaki Coban, Erich Bornberg-Bauer, Carsten Kemena
Format: Article
Language:English
Published: BMC 2025-01-01
Series:BMC Ecology and Evolution
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Online Access:https://doi.org/10.1186/s12862-024-02347-7
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author Abdulbaki Coban
Erich Bornberg-Bauer
Carsten Kemena
author_facet Abdulbaki Coban
Erich Bornberg-Bauer
Carsten Kemena
author_sort Abdulbaki Coban
collection DOAJ
description Abstract Background Protein evolution is central to molecular adaptation and largely characterized by modular rearrangements of domains, the evolutionary and structural building blocks of proteins. Genetic events underlying protein rearrangements are relatively rare compared to changes of amino-acids. Therefore, these events can be used to characterize and reconstruct major events of molecular adaptation by comparing large data sets of proteomes. Results Here we determine, at unprecedented completeness, the rates of fusion, fission, emergence and loss of domains in five eukaryotic clades (monocots, eudicots, fungi, insects, vertebrates). By characterizing rearrangements that were previously considered “ambiguous” or “complex” we raise the fraction of resolved rearrangement events from previously ca. 60% to around 92%. We exemplify our method by analyzing the evolutionary histories of protein rearrangements in (i) the extracellular matrix, (ii) innate immunity across Eukaryota, Metazoa, and Vertebrata, and (iii) Toll-Like-Receptors in the innate immune system of Eukaryota. In all three cases we can find hot-spots of rearrangement events in their phylogeny which (i) can be related with major events of adaptation and (ii) which follow the emergence of new domains which become integrated into existing arrangements. Conclusion Our results demonstrate that, akin to the change at the level of amino acids, domain rearrangements follow a clock-like dynamic which can be well quantified and supports the concept of evolutionary tinkering. While many novel domain emergence events are ancient, emerged domains are quickly incorporated into a great number of proteins. In parallel, the observed rates of emergence of new domains are becoming smaller over time.
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spelling doaj-art-bdfa59374e414bfaa1b321239bbd5d4c2025-01-12T12:05:04ZengBMCBMC Ecology and Evolution2730-71822025-01-012511910.1186/s12862-024-02347-7Tracing the paths of modular evolution by quantifying rearrangement events of protein domainsAbdulbaki Coban0Erich Bornberg-Bauer1Carsten Kemena2Institute for Evolution and Biodiversity, University of MünsterInstitute for Evolution and Biodiversity, University of MünsterInstitute for Evolution and Biodiversity, University of MünsterAbstract Background Protein evolution is central to molecular adaptation and largely characterized by modular rearrangements of domains, the evolutionary and structural building blocks of proteins. Genetic events underlying protein rearrangements are relatively rare compared to changes of amino-acids. Therefore, these events can be used to characterize and reconstruct major events of molecular adaptation by comparing large data sets of proteomes. Results Here we determine, at unprecedented completeness, the rates of fusion, fission, emergence and loss of domains in five eukaryotic clades (monocots, eudicots, fungi, insects, vertebrates). By characterizing rearrangements that were previously considered “ambiguous” or “complex” we raise the fraction of resolved rearrangement events from previously ca. 60% to around 92%. We exemplify our method by analyzing the evolutionary histories of protein rearrangements in (i) the extracellular matrix, (ii) innate immunity across Eukaryota, Metazoa, and Vertebrata, and (iii) Toll-Like-Receptors in the innate immune system of Eukaryota. In all three cases we can find hot-spots of rearrangement events in their phylogeny which (i) can be related with major events of adaptation and (ii) which follow the emergence of new domains which become integrated into existing arrangements. Conclusion Our results demonstrate that, akin to the change at the level of amino acids, domain rearrangements follow a clock-like dynamic which can be well quantified and supports the concept of evolutionary tinkering. While many novel domain emergence events are ancient, emerged domains are quickly incorporated into a great number of proteins. In parallel, the observed rates of emergence of new domains are becoming smaller over time.https://doi.org/10.1186/s12862-024-02347-7Protein domainsEvolutionDomain arrangements
spellingShingle Abdulbaki Coban
Erich Bornberg-Bauer
Carsten Kemena
Tracing the paths of modular evolution by quantifying rearrangement events of protein domains
BMC Ecology and Evolution
Protein domains
Evolution
Domain arrangements
title Tracing the paths of modular evolution by quantifying rearrangement events of protein domains
title_full Tracing the paths of modular evolution by quantifying rearrangement events of protein domains
title_fullStr Tracing the paths of modular evolution by quantifying rearrangement events of protein domains
title_full_unstemmed Tracing the paths of modular evolution by quantifying rearrangement events of protein domains
title_short Tracing the paths of modular evolution by quantifying rearrangement events of protein domains
title_sort tracing the paths of modular evolution by quantifying rearrangement events of protein domains
topic Protein domains
Evolution
Domain arrangements
url https://doi.org/10.1186/s12862-024-02347-7
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AT carstenkemena tracingthepathsofmodularevolutionbyquantifyingrearrangementeventsofproteindomains