Genome-sequencing of the obligate symbiotic, Mycoplasma-related endobacteria of arbuscular mycorrhizal fungi to uncover their function and coevolution.
Final Report Abstract
For more than 450 million years, arbuscular mycorrhizal fungi (AMF) have formed intimate, mutualistic symbioses with the vast majority of land plants and are major drivers in almost all terrestrial ecosystems. The obligate plant-symbiotic AMF host additional symbionts, so-called Mollicutes-related endobacteria (MRE). To uncover putative functional roles of these widespread but enigmatic MRE, we sequenced the genome of MRE living in the AMF Dentiscutata heterogama (DhMRE). Multilocus phylogenetic analyses showed that MRE form a previously unidentified lineage sister to the hominis group of Mycoplasma species. DhMRE possesses a strongly reduced metabolic capacity with 55% of the proteins having unknown function, which reflects unique adaptations to an intracellular lifestyle. We found evidence for transkingdom gene transfer between MRE and their AMF host. At least 27 annotated DhMRE proteins show similarities to nuclear-encoded proteins of the at the time only genome sequenced AMF Rhizophagus irregularis, which itself lacks MRE. Nuclear-encoded homologs could moreover be identified for another AMF, Gigaspora margarita, and surprisingly, also for the non-AMF Mortierella verticillata. Our data indicate a possible origin of the MRE-fungus association in ancestors of the Glomeromycota (AM fungi) and Mucoromycotina. The DhMRE genome encodes an arsenal of putative regulatory proteins with eukaryotic-like domains, some of them encoded in putative genomic islands. MRE are highly interesting candidates to study the evolution and interactions between an ancient, obligate endosymbiotic prokaryote with its obligate plant-symbiotic fungal host. Our data moreover may be used for further targeted searches for ancient effector-like proteins that may be key components in the regulation of the arbuscular mycorrhiza (AM) symbiosis, with its large potential for application for example as plant growth promoting microorganisms in agriculture. In general, the genome analysis of the widespread obligate symbiont MRE living within obligate plant-symbiont AMF provided first insights into the evolution of MRE and interactions with their fungal host. The model fungus in AM research, R. irregularis, does not host endobacteria, but it is extremely important to realize that its nuclear genome contains a set of genes that were in earlier evolution transferred from the same type of endobacteria to the nuclear fungal genome. This opens an entirely new field of interpretation and research on endobacteria-fungus-plant interaction and regulation in the AM symbiosis, including questions about the origin of the putatively regulatory genes/proteins from putative earlier MRE-ancestor associations with animals or amoeba. These questions and aspects (as the many other interesting and important aspects regarding AM fungi we have worked on) must be evaluated by others.
Publications
- 2015) Mosaic genome of endobacteria in arbuscular mycorrhizal fungi: Transkingdom gene transfer in an ancient mycoplasma-fungus association. Proceedings of the National Academy of Sciences 112 (25): 7785-7790
Gloria Torres-Cortés, Stefano Ghignone, Paola Bonfante, Arthur Schüßler
(See online at https://doi.org/10.1073/pnas.1501540112)
