Leão, Pedro

Abstract Asgard archaea were pivotal in the origin of complex cellular life. Hodarchaeales (Asgardarchaeota class Heimdallarchaeia) were recently shown to be the closest relatives of eukaryotes. However, limited sampling of these archaea constrains our understanding of their ecology and evolution 1–3 , including their anticipated role in eukaryogenesis. Here, we nearly double the number of Asgardarchaeota metagenome-assembled genomes (MAGs) to 869, including 136 new Heimdallarchaeia (49 Hodarchaeales) and several novel lineages. Examining global distribution revealed Hodarcheales are primarily found in coastal marine sediments. Detailed analysis of their metabolic capabilities revealed guilds of Heimdallarchaeia are distinct from other Asgardarchaeota. These archaea encode hallmarks of aerobic eukaryotes, including electron transport chain complexes (III and IV), biosynthesis of heme, and response to reactive oxygen species (ROS). The predicted structural architecture of Heimdallarchaeia membrane-bound hydrogenases includes additional Complex-I-like subunits potentially increasing the proton motive force and ATP synthesis. Heimdallarchaeia genomes encode CoxD, which regulates the electron transport chain (ETC) in eukaryotes. Thus, key hallmarks for aerobic respiration may have been present in the Asgard-eukaryotic ancestor. Moreover, we found that Heimdallarchaeia is present in a variety of oxic marine environments. This expanded diversity reveals these Archaea likely conferred energetic advantages during early stages of eukaryogenesis, fueling cellular complexity.

Magnetosome synthesis in magnetotactic bacteria (MTB) is regarded as a very ancient evolutionary process that dates back to deep-branching phyla. Magnetotactic bacteria belonging to one of such phyla, Nitrospirota, contain the classical genes for the magnetosome synthesis (e.g., mam, mms) and man genes, which were considered to be specific for this group. However, the recent discovery of man genes in MTB from the Thermodesulfobacteriota phylum has raised several questions about the inheritance of these genes in MTB. In this work, three new man genes containing MTB genomes affiliated with Nitrospirota and Thermodesulfobacteriota, were obtained. By applying reconciliation with these and the previously published MTB genomes, we demonstrate that the last common ancestor of all Nitrospirota was most likely not magnetotactic as assumed previously. Instead, our findings suggest that the genes for magnetosome synthesis were transmitted to the phylum Nitrospirota by horizontal gene transfer (HGT), which is the first case of the interphylum transfer of magnetosome genes detected to date. Furthermore, we provide evidence for the HGT of magnetosome genes from the Magnetobacteriaceae to the Dissulfurispiraceae family within Nitrospirota. Thus, our results imply a more significant role of HGT in the MTB evolution than deemed before and challenge the hypothesis of the ancient origin of magnetosome synthesis.

AbstractCandidatus Magnetoglobus multicellularis is an uncultured magnetotactic multicellular prokaryote composed of 17-40 Gram-negative cells that are capable of synthesizing organelles known as magnetosomes. The magnetosomes of Ca. M. multicellularis are composed of greigite and are organized in chains that are responsible for the microorganism's orientation along magnetic field lines. The characteristics of the microorganism, including its multicellular life cycle, magnetic field orientation, and swimming behavior, and the lack of viability of individual cells detached from the whole assembly, are considered strong evidence for the existence of a unique multicellular life cycle among prokaryotes. It has been proposed that the position of each cell within the aggregate is fundamental for the maintenance of its distinctive morphology and magnetic field orientation. However, the cellular organization of the whole organism has never been studied in detail. Here, we investigated the magnetosome organization within a cell, its distribution within the microorganism, and the intercellular relationships that might be responsible for maintaining the cells in the proper position within the microorganism, which is essential for determining the magnetic properties of Ca. M. multicellularis during its life cycle. The results indicate that cellular interactions are essential for the determination of individual cell shape and the magnetic properties of the organism and are likely directly associated with the morphological changes that occur during the multicellular life cycle of this species.