Exploring the Metagenome of Geosiphon pyriformis: The Only Known Fungus with a Photosynthetic Endosymbiont

Abstract

Arbuscular mycorrhizal fungi (AMF), belonging to the Glomeromycotina sub-phylum, are vital symbionts for roughly 80% of terrestrial plants, providing essential services like water, nutrients, and pathogen protection in exchange for photosynthetic products. These natural "biofertilizers" play a crucial role in enhancing plant biodiversity and sustaining terrestrial ecosystems. Interestingly, AMF not only engage in endosymbiosis with plants but also harbor their own unique endobacterial microbiota. A prominent example of this is Geosiphon pyriformis, distinct within the AMF group for its ability to host a cyanobacterium within its fungal cells - a unique symbiotic relationship in the Fungal Kingdom. This specialized interaction, occurring in bladder-like structures, involves G. pyriformis nuclei, mollicute-like bacterial endosymbionts (MRE), and photosynthetically active Nostoc punctiforme cells; a cyanobacteria. This setup makes G. pyriformis an ideal model for studying the complex dynamics of microbial interactions in AMF systems. Despite advancements in genomic research shedding light on G. pyriformis, there remains a gap in fully understanding the genomics of its endosymbionts. To bridge this gap, I have assembled and analyzed genome data from N. punctiforme and MRE using metagenomic datasets from G. pyriformis bladders. This analysis, juxtaposed with genomes of related cyanobacteria and MRE, unveiled notable gene expansions in the Nostoc endosymbiont, particularly in mobile genetic elements. I also found that the G. pyriformis MRE is part of one of two distinct monophyletic MRE groups, all of which characterized by streamlined genomes that differ significantly in structure and composition from other MRE relatives. Overall, the current work provided new insights into the evolutionary and functional complexity of these symbiotic relationships.