Amoebozoans are Secretly but Ancestrally Sexual: Evidence for Sex Genes and Potential Novel Crossover Pathways in Diverse Groups of Amoebae

Abstract

Sex is beneficial in eukaryotes as it can increase genetic diversity, reshuffle their genomes, and purge deleterious mutations. Yet, its evolution remains a mystery. The eukaryotic clade supergroup Amoebozoa encompasses diverse lineages of polymorphic amoeboid forms, including both free-living and parasitic lineages. The group is generally believed to be asexual, though recent studies show that some of its members are implicated in cryptic forms of sexual cycles. In this study, we conduct a comprehensive inventory and analysis of genes involved in meiosis and related processes, in order to investigate the evolutionary history of sex in the clade. We analyzed genomic and transcriptomic data of 39 amoebozoans representing all major subclades of Amoebozoa. Our results show that Amoebozoa possess most of the genes exclusive to meiosis but lack genes encoding synaptonemal complex (SC). The absence of SC genes is discussed in the context of earlier studies that reported ultrastructural evidence of SC in some amoebae. We also find interclade and intrageneric variation in sex gene distribution, indicating diversity in sexual pathways in the group. Particularly, members of Mycetozoa engage in a novel sexual pathway independent of the universally conserved meiosis initiator gene, SPO11. Our findings strongly suggest that not only do amoebozoans possess sex genes in their genomes, but also, based on the transcriptome evidence, the present sex genes are functional. We conclude that Amoebozoa is ancestrally sexual, contrary to the long held belief that most of its members are asexual. Thus, asexuality in Amoebozoa, if confirmed to be present, is a derived-trait that appeared later in their evolution.

Three New Freshwater Cochliopodium Species (Himatismenida, Amoebozoa) from the Southeastern United States

“…Furthermore, this sexual behavior is supported with genetic evidence that reported nearly complete recombination gene repertoire in some members of this genus (Tekle et al. ; Wood et al. ).…”

Microbial Diversity in the Eukaryotic SAR Clade: Illuminating the Darkness Between Morphology and Molecular Data

“…The use of an integrative taxonomic approach can provide a better understanding of species distributions including taking into account cryptic species, phenotypic plasticity, population‐level variation, etc . Recent studies have shown that the use of single cell “omics” allows acquisition of data from the dark area particularly for uncultivable species . Hence, combining community and single cell approaches will help to increase our knowledge of this highly diverse clade.…”

Sexual Processes in Microbial Eukaryotes

“…Amoebozoan species include a variety of lineages of polymorphic amoeboid forms that until recently were considered to be asexual. A recent study, however revealed that amoebozoans representing all major subclades possess most of the genes that function specifically in meiosis, as well as many of the genes involved in meiotic recombinational repair [61]. It was concluded that Amoebozoa is ancestrally sexual.…”