TY  - JOUR
A1  - Birikmen, Mehmet
A1  - Bohnsack, Katherine E.
A1  - Tran, Vinh Ngoc
A1  - Somayaji, Sharvari
A1  - Bohnsack, Markus
A1  - Ebersberger, Ingo
T1  - Tracing eukaryotic ribosome biogenesis factors into the archaeal momain sheds light on the evolution of functional complexity
T2  - Frontiers in microbiology
N2  - 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.
KW  - domain architecture evolution
KW  - asgard group
KW  - phylogenetic profiles
KW  - orthology assignment
KW  - evolutionary traceability
KW  - pathway complexity
KW  - large subunit maturation
Y1  - 2021
UR  - http://publikationen.ub.uni-frankfurt.de/frontdoor/index/index/docId/62661
UR  - https://nbn-resolving.org/urn:nbn:de:hebis:30:3-626613
SN  - 1664-302X
N1  - This work was supported by the Research Funding Program Landes-Offensive zur Entwicklung Wissenschaftlich-ökonomischer Exzellenz (LOEWE) of the State of Hessen, Research Center for Translational Biodiversity Genomics (TBG) to IE, the Deutsche Forschungsgemeinschaft (SFB1190 to MTB, SFB860 to KB, and EB-285-2/2 to IE), and the University Medical Centre Göttingen (to MTB and KB).
VL  - 12
IS  - art. 739000
SP  - 1
EP  - 18
PB  - Frontiers Media
CY  - Lausanne
ER  -