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Evolution of microRNAs in Amoebozoa and implications for the origin of multicellularity
Bart Edelbroek1, Jonas Kjellin1, Inna Biryukova2
1Department of Cell and Molecular Biology, Uppsala Biomedical Centre, Uppsala University, 75124 Uppsala, Sweden.
Abstract:
MicroRNAs (miRNAs) are important and ubiquitous regulators of gene expression in both plants and animals. They are thought to have evolved convergently in these lineages and hypothesized to have played a role in the evolution of multicellularity. In line with this hypothesis, miRNAs have so far only been described in few unicellular eukaryotes. Here, we investigate the presence and evolution of miRNAs in Amoebozoa, focusing on species belonging to Acanthamoeba, Physarum and dictyostelid taxonomic groups, representing a range of unicellular and multicellular lifestyles. miRNAs that adhere to both the stringent plant and animal miRNA criteria were identified in all examined amoebae, expanding the total number of protists harbouring miRNAs from 7 to 15. We found conserved miRNAs between closely related species, but the majority of species feature only unique miRNAs. This shows rapid gain and/or loss of miRNAs in Amoebozoa, further illustrated by a detailed comparison between two evolutionary closely related dictyostelids. Additionally, loss of miRNAs in the Dictyostelium discoideum drnB mutant did not seem to affect multicellular development and, hence, demonstrates that the presence of miRNAs does not appear to be a strict requirement for the transition from uni- to multicellular life.
Insights
MicroRNAs (miRNAs) are present in diverse amoebae, suggesting their ancient origins. Their rapid evolution and non-essential role in multicellular development challenge previous hypotheses.
Area of Science:
- Evolutionary biology
- Molecular biology
- Genomics
Background:
- MicroRNAs (miRNAs) are key gene regulators in plants and animals, potentially influencing multicellularity.
- Previous research identified miRNAs in limited unicellular eukaryotes, leaving their evolutionary history in other lineages unexplored.
Purpose of the Study:
- To investigate the presence and evolutionary patterns of miRNAs in diverse Amoebozoa species.
- To assess the role of miRNAs in the transition from unicellular to multicellular life.
Main Methods:
- Bioinformatic analysis of small RNA sequencing data from Acanthamoeba, Physarum, and dictyostelids.
- Comparative genomics to identify conserved and unique miRNAs across species.
- Phenotypic analysis of miRNA-deficient mutants in Dictyostelium discoideum.
Main Results:
- Identified miRNAs adhering to plant and animal criteria in all examined amoebae, increasing known miRNA-harboring protists from 7 to 15.
- Observed rapid gain and/or loss of miRNAs within Amoebozoa, with mostly unique miRNAs per species.
- Demonstrated that miRNA loss in Dictyostelium discoideum mutants did not impede multicellular development.
Conclusions:
- miRNAs are widespread in Amoebozoa, indicating an ancient evolutionary origin.
- The rapid turnover of miRNAs in Amoebozoa suggests high evolutionary plasticity.
- The presence of miRNAs is not a strict prerequisite for the evolution of multicellularity in these organisms.
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