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Published on: June 6, 2025
Zygomycetes, microsporidia, and the evolutionary ancestry of sex determination
Tina Koestler1, Ingo Ebersberger
1Center for Integrative Bioinformatics Vienna, University of Vienna, Medical University of Vienna, University of Veterinary Medicine Vienna, Vienna, Austria.
Abstract:
Zygomycetes and their alleged sister taxon, the microsporidia, exclusively share the presence of a cluster of three genes encoding a sugar transporter, a high mobility group (HMG)-type transcription factor, and an RNA helicase. In zygomycetes, the HMG-type transcription factor acts as the sole sex determinant. This intimately ties the evolutionary history of this gene cluster to the evolution of sex determination. Here, we have unraveled the relationships of the two gene clusters by vicariously analyzing the sugar transporters and the RNA helicases. We show that if the two gene clusters share a common ancestry, it dates back to the early days of eukaryotic evolution. As a consequence, the zygomycete MAT locus would be old enough to represent the archetype of fungal and animal sex determination. However, the evolutionary scenario that has to be invoked is complex. An independent assembly of the two clusters deserves therefore consideration. In either case, shared ancestry or convergent evolution, the presence of the gene cluster in microsporidia and in zygomycetes represents at best a plesiomorphy. Hence, it is not phylogenetically informative. A further genome-wide reanalysis of gene order conservation reveals that gene order is not significantly more similar between microsporidia and zygomycetes than between microsporidia and any other fungal taxon or even humans. Consequently, the phylogenetic placement of microsporidia as sister to the zygomycetes needs to be reconsidered.
Insights
The shared gene cluster in zygomycetes and microsporidia, linked to sex determination, may not be phylogenetically informative. Its presence is likely an ancient trait, suggesting current placement of microsporidia needs reevaluation.
Area of Science:
- Evolutionary biology
- Genomics
- Mycology
Background:
- Zygomycetes and microsporidia share a unique gene cluster: sugar transporter, high mobility group (HMG)-type transcription factor, and RNA helicase.
- In zygomycetes, the HMG-type transcription factor is the sole sex determinant, linking this gene cluster's evolution to sex determination evolution.
- The phylogenetic placement of microsporidia as sister to zygomycetes is based partly on this shared gene cluster.
Purpose of the Study:
- To investigate the evolutionary relationship between the gene clusters found in zygomycetes and microsporidia.
- To determine if the shared gene cluster provides phylogenetic information for the placement of microsporidia.
- To re-evaluate the sister-taxon relationship between microsporidia and zygomycetes.
Main Methods:
- Comparative analysis of sugar transporter and RNA helicase genes to infer the evolutionary history of the gene cluster.
- Genome-wide reanalysis of gene order conservation between microsporidia, zygomycetes, other fungi, and humans.
Main Results:
- If the gene clusters share common ancestry, it dates back to early eukaryotic evolution, potentially making the zygomycete sex determination locus ancient.
- An alternative hypothesis of independent gene cluster assembly (convergent evolution) is also considered.
- Gene order conservation is not significantly higher between microsporidia and zygomycetes compared to other fungal taxa or humans.
- The presence of the gene cluster in both groups is likely a plesiomorphy (ancient shared trait), rendering it phylogenetically uninformative.
Conclusions:
- The shared gene cluster is not phylogenetically informative for the relationship between microsporidia and zygomycetes.
- The sister-taxon status of microsporidia to zygomycetes requires reconsideration based on the lack of significant gene order conservation.
- The evolutionary history of sex determination in fungi and animals may be more complex than previously assumed.
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