Omics of an enigmatic marine amoeba uncovers unprecedented giant viruses gene trafficking and provides insights into its complex life cycle

Abstract

Amoebozoa include lineages of diverse ecology, behavior and morphology. They are assumed to encompass members with the largest genome sizes of all living things, yet genomic studies in the group are limited. Trichosphaerium, a polymorphic, multinucleate, marine amoeba with a complicated life cycle has puzzled experts in the field for over a century. In an effort to explore the genomic diversity, and investigate extraordinary behavior observed among the Amoebozoa, we used integrated omics approaches to study this enigmatic marine amoeba. Omics data, including single-cell transcriptomics and cytological data, demonstrate that Trichosphaerium sp. possesses the complete meiosis toolkit genes. These genes are expressed in life stages of the amoeba including medium and large cells. The life cycle of Trichosphaerium sp. involves asexual processes via binary fission and multiple fragmentation of giant cells, and sexual-like processes involving genes implicated in sexual reproduction and polyploidization. These findings are in stark contrast to a life cycle previously reported for this amoeba. Despite the extreme morphological plasticity observed in Trichosphaerium, our genomic data showed populations maintain a species-level intragenomic variation. A draft genome of Trichosphaerium indicates elevated lateral gene transfer (LGT) from bacteria and giant viruses. Gene trafficking in Trichosphaerium is the highest within Amoebozoa, and among the highest in microbial eukaryotes. Significance statementAmoebozoa include various genome complexities and life cycles, however, the genomes of the vast diversity of amoebozoans remains unexplored. In this study an integrated omics approach is used to investigate the genome and life cycle of Trichophaerium, an enigmatic polymorphic marine amoeba. We uncovered elevated gene trafficking from giant viruses and presence of the complete meiosis gene toolkit. Despite the observed large morphological plasticity, the population of Trichophaerium maintains intragenomic variation of a species level.