Fibrillarin evolution through the Tree of Life: Comparative genomics and microsynteny network analyses provide new insights into the evolutionary history of Fibrillarin

Fibrillarin (FIB), a methyltransferase essential for life in the vast majority of eukaryotes, is involved in methylation of rRNA required for proper ribosome assembly, as well as methylation of histone H2A of promoter regions of rRNA genes. RNA viral progression that affects both plants and animals requires FIB proteins. Despite the importance and high conservation of fibrillarins, there little is known about the evolutionary dynamics of this small gene family. We applied a phylogenomic microsynteny-network approach to elucidate the evolutionary history of FIB proteins across the Tree of Life. We identified 1063 non-redundant FIB sequences across 1049 completely sequenced genomes from Viruses, Bacteria, Archaea, and Eukarya. FIB is a highly conserved single-copy gene through Archaea and Eukarya lineages, except for plants, which have a gene family expansion due to paleopolyploidy and tandem duplications. We found a high conservation of the FIB genomic context during plant evolution. Surprisingly, FIB in mammals duplicated after the Eutheria split (e.g., ruminants, felines, primates) from therian mammals (e.g., marsupials) to form two main groups of sequences, the FIB and FIB-like groups. The FIB-like group transposed to another genomic context and remained syntenic in all the eutherian mammals. This transposition correlates with differences in the expression patterns of FIB-like proteins and with elevated Ks values potentially due to reduced evolutionary constraints of the duplicated copy. Our results point to a unique evolutionary event in mammals, between FIB and FIB-like genes, that led to non-redundant roles of the vital processes in which this protein is involved. Author summary Fibrillarins are a small group of proteins known to be essential for eukaryotic life as they are involved in several process in the cell. Changes in the amount of fibrillarins in cells can lead to incorrect translation of proteins, and is associated with various types of cancer as well as bacterial and viral responses. To date, no formal analysis of the evolution of fibrillarins through different groups of organisms such as prokaryotes, fungi, plants, and animals exists. Next-generation sequencing enhances the accessibility of great number of genome sequences from different organisms. The aim of this work is to detect the sequence stability of the fibrillarin gene copies on distant related organisms, and whether it could be associated to the changes on the organization of their genome structures. We applied a novel methodology to detect rearrangements on genomes and found evidence of evolutionary forces on plants that keep the genome region where fibrillarin is located conserved. Also, we observed that a duplication of fibrillarin occurred in mammals which led to novel or specific functions of fibrillarin duplicates.