Mosaic genome of endobacteria in arbuscular mycorrhizal fungi: Transkingdom gene transfer in an ancient mycoplasma-fungus association

• Published in: Proceedings of the National Academy of Sciences - PNAS 2015-06, Vol.112 (25), p.7785-7790
• Main Authors: Torres-Cortés, Gloria, Ghignone, Stefano, Bonfante, Paola, Schüßler, Arthur
• Format: Article
• Language: English
• Subjects: ancestry; arbuscular mycorrhizal fungi; Bacteria; Bacteria - genetics; Biological Sciences; cytoplasm; endobacteria; Flowers & plants; Fungi; gene transfer; Gene Transfer Techniques; genome; Genome, Bacterial; Genomes; Gigaspora margarita; Glomeromycota; horizontal gene transfer; hosts; intracellular symbiont; Molecular Sequence Data; Mortierella; Mosaicism; Mycoplasma; Mycorrhizae; mycorrhizal fungi; Proteins; Rhizophagus; sequence analysis; Symbiosis; Terrestrial ecosystems
• ISSN: 0027-8424; 1091-6490
• DOI: 10.1073/pnas.1501540112

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 yet enigmatic MRE, we sequenced the genome of Dh MRE living in the AMF Dentiscutata heterogama . Multilocus phylogenetic analyses showed that MRE form a previously unidentified lineage sister to the hominis group of Mycoplasma species. Dh MRE 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 Dh MRE proteins show similarities to nuclear-encoded proteins of the AMF Rhizophagus irregularis , which itself lacks MRE. Nuclear-encoded homologs could moreover be identified for another AMF, Gigaspora margarita , and surprisingly, also the non-AMF Mortierella verticillata . Our data indicate a possible origin of the MRE-fungus association in ancestors of the Glomeromycota and Mucoromycotina . The Dh MRE 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 symbiosis. Significance Obligate plant-symbiotic, arbuscular mycorrhizal fungi (AMF) are major drivers of terrestrial ecosystems and host enigmatic Mollicutes -related endobacteria (MRE) in their cytoplasm. The genome analysis of a MRE living in the AMF Dentiscutata heterogama revealed it to represent a previously unidentified bacterial lineage of Mycoplasma -related species. Dh MRE shows strongly reduced metabolic capacity and underwent trans-kingdom gene transfer: its genome codes for an arsenal of eukaryotic-like putative effector proteins, with nuclear encoded homologues in AMF and Mortierella . The MRE-fungus (-plant) association probably evolved in ancestors of Glomeromycota and Mucoromycotina . Thi