Omics of an Enigmatic Marine Amoeba Uncovers Unprecedented Gene Trafficking from Giant Viruses 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 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, as well as 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 that 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.

Deep Learning-based structural and functional annotation of Pandoravirus hypothetical proteins

“…This suggests that they have been captured from hosts, contradicting the reduction theory of a single cellular ancestor (Fischer et al ., 2010; Koonin and Yutin, 2018; Chelkha et al ., 2020; Sun et al ., 2020; Belhaouari et al ., 2022). The phylogenetic demonstration that different giant virus genes originate in any of the three domains of life supports the occurrence of exchange of genetic material between viruses and other organisms, providing further evidence for the expansion theory (Iyer et al ., 2006; Koonin and Yutin, 2018; Brandes and Linial, 2019; Tekle et al ., 2023). Indeed, the NCLDVs as a whole undergo extremely dynamic evolution (Brandes and Linial, 2019), again consistent with the expansion theory (Koonin and Yutin, 2018).…”