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Tracing Eukaryotic Ribosome Biogenesis Factors Into the Archaeal Domain Sheds Light on the Evolution of Functional Complexity

Ribosome assembly is an essential and carefully choreographed cellular process. In eukaryotes, several 100 proteins, distributed across the nucleolus, nucleus, and cytoplasm, co-ordinate the step-wise assembly of four ribosomal RNAs (rRNAs) and approximately 80 ribosomal proteins (RPs) into the matu...

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Autores principales: Birikmen, Mehmet, Bohnsack, Katherine E., Tran, Vinh, Somayaji, Sharvari, Bohnsack, Markus T., Ebersberger, Ingo
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8481954/
https://www.ncbi.nlm.nih.gov/pubmed/34603269
http://dx.doi.org/10.3389/fmicb.2021.739000
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author Birikmen, Mehmet
Bohnsack, Katherine E.
Tran, Vinh
Somayaji, Sharvari
Bohnsack, Markus T.
Ebersberger, Ingo
author_facet Birikmen, Mehmet
Bohnsack, Katherine E.
Tran, Vinh
Somayaji, Sharvari
Bohnsack, Markus T.
Ebersberger, Ingo
author_sort Birikmen, Mehmet
collection PubMed
description Ribosome assembly is an essential and carefully choreographed cellular process. In eukaryotes, several 100 proteins, distributed across the nucleolus, nucleus, and cytoplasm, co-ordinate the step-wise assembly of four ribosomal RNAs (rRNAs) and approximately 80 ribosomal proteins (RPs) into the mature ribosomal subunits. Due to the inherent complexity of the assembly process, functional studies identifying ribosome biogenesis factors and, more importantly, their precise functions and interplay are confined to a few and very well-established model organisms. Although best characterized in yeast (Saccharomyces cerevisiae), emerging links to disease and the discovery of additional layers of regulation have recently encouraged deeper analysis of the pathway in human cells. In archaea, ribosome biogenesis is less well-understood. However, their simpler sub-cellular structure should allow a less elaborated assembly procedure, potentially providing insights into the functional essentials of ribosome biogenesis that evolved long before the diversification of archaea and eukaryotes. Here, we use a comprehensive phylogenetic profiling setup, integrating targeted ortholog searches with automated scoring of protein domain architecture similarities and an assessment of when search sensitivity becomes limiting, to trace 301 curated eukaryotic ribosome biogenesis factors across 982 taxa spanning the tree of life and including 727 archaea. We show that both factor loss and lineage-specific modifications of factor function modulate ribosome biogenesis, and we highlight that limited sensitivity of the ortholog search can confound evolutionary conclusions. Projecting into the archaeal domain, we find that only few factors are consistently present across the analyzed taxa, and lineage-specific loss is common. While members of the Asgard group are not special with respect to their inventory of ribosome biogenesis factors (RBFs), they unite the highest number of orthologs to eukaryotic RBFs in one taxon. Using large ribosomal subunit maturation as an example, we demonstrate that archaea pursue a simplified version of the corresponding steps in eukaryotes. Much of the complexity of this process evolved on the eukaryotic lineage by the duplication of ribosomal proteins and their subsequent functional diversification into ribosome biogenesis factors. This highlights that studying ribosome biogenesis in archaea provides fundamental information also for understanding the process in eukaryotes.
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spelling pubmed-84819542021-10-01 Tracing Eukaryotic Ribosome Biogenesis Factors Into the Archaeal Domain Sheds Light on the Evolution of Functional Complexity Birikmen, Mehmet Bohnsack, Katherine E. Tran, Vinh Somayaji, Sharvari Bohnsack, Markus T. Ebersberger, Ingo Front Microbiol Microbiology Ribosome assembly is an essential and carefully choreographed cellular process. In eukaryotes, several 100 proteins, distributed across the nucleolus, nucleus, and cytoplasm, co-ordinate the step-wise assembly of four ribosomal RNAs (rRNAs) and approximately 80 ribosomal proteins (RPs) into the mature ribosomal subunits. Due to the inherent complexity of the assembly process, functional studies identifying ribosome biogenesis factors and, more importantly, their precise functions and interplay are confined to a few and very well-established model organisms. Although best characterized in yeast (Saccharomyces cerevisiae), emerging links to disease and the discovery of additional layers of regulation have recently encouraged deeper analysis of the pathway in human cells. In archaea, ribosome biogenesis is less well-understood. However, their simpler sub-cellular structure should allow a less elaborated assembly procedure, potentially providing insights into the functional essentials of ribosome biogenesis that evolved long before the diversification of archaea and eukaryotes. Here, we use a comprehensive phylogenetic profiling setup, integrating targeted ortholog searches with automated scoring of protein domain architecture similarities and an assessment of when search sensitivity becomes limiting, to trace 301 curated eukaryotic ribosome biogenesis factors across 982 taxa spanning the tree of life and including 727 archaea. We show that both factor loss and lineage-specific modifications of factor function modulate ribosome biogenesis, and we highlight that limited sensitivity of the ortholog search can confound evolutionary conclusions. Projecting into the archaeal domain, we find that only few factors are consistently present across the analyzed taxa, and lineage-specific loss is common. While members of the Asgard group are not special with respect to their inventory of ribosome biogenesis factors (RBFs), they unite the highest number of orthologs to eukaryotic RBFs in one taxon. Using large ribosomal subunit maturation as an example, we demonstrate that archaea pursue a simplified version of the corresponding steps in eukaryotes. Much of the complexity of this process evolved on the eukaryotic lineage by the duplication of ribosomal proteins and their subsequent functional diversification into ribosome biogenesis factors. This highlights that studying ribosome biogenesis in archaea provides fundamental information also for understanding the process in eukaryotes. Frontiers Media S.A. 2021-09-16 /pmc/articles/PMC8481954/ /pubmed/34603269 http://dx.doi.org/10.3389/fmicb.2021.739000 Text en Copyright © 2021 Birikmen, Bohnsack, Tran, Somayaji, Bohnsack and Ebersberger. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Microbiology
Birikmen, Mehmet
Bohnsack, Katherine E.
Tran, Vinh
Somayaji, Sharvari
Bohnsack, Markus T.
Ebersberger, Ingo
Tracing Eukaryotic Ribosome Biogenesis Factors Into the Archaeal Domain Sheds Light on the Evolution of Functional Complexity
title Tracing Eukaryotic Ribosome Biogenesis Factors Into the Archaeal Domain Sheds Light on the Evolution of Functional Complexity
title_full Tracing Eukaryotic Ribosome Biogenesis Factors Into the Archaeal Domain Sheds Light on the Evolution of Functional Complexity
title_fullStr Tracing Eukaryotic Ribosome Biogenesis Factors Into the Archaeal Domain Sheds Light on the Evolution of Functional Complexity
title_full_unstemmed Tracing Eukaryotic Ribosome Biogenesis Factors Into the Archaeal Domain Sheds Light on the Evolution of Functional Complexity
title_short Tracing Eukaryotic Ribosome Biogenesis Factors Into the Archaeal Domain Sheds Light on the Evolution of Functional Complexity
title_sort tracing eukaryotic ribosome biogenesis factors into the archaeal domain sheds light on the evolution of functional complexity
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8481954/
https://www.ncbi.nlm.nih.gov/pubmed/34603269
http://dx.doi.org/10.3389/fmicb.2021.739000
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