Evolutionary history of arbuscular mycorrhizal fungi and genomic signatures of obligate symbiosis.

BACKGROUND: The colonization of land and the diversification of terrestrial plants is intimately linked to the evolutionary history of their symbiotic fungal partners. Extant representatives of these fungal lineages include mutualistic plant symbionts, the arbuscular mycorrhizal (AM) fungi in Glomeromycota and fine root endophytes in Endogonales (Mucoromycota), as well as fungi with saprotrophic, pathogenic and endophytic lifestyles. These fungal groups separate into three monophyletic lineages but their evolutionary relationships remain enigmatic confounding ancestral reconstructions. Their taxonomic ranks are currently fluid. RESULTS: In this study, we recognize these three monophyletic linages as phyla, and use a balanced taxon sampling and broad taxonomic representation for phylogenomic analysis that rejects a hard polytomy and resolves Glomeromycota as sister to a clade composed of Mucoromycota and Mortierellomycota. Low copy numbers of genes associated with plant cell wall degradation could not be assigned to the transition to a plant symbiotic lifestyle but appears to be an ancestral phylogenetic signal. Both plant symbiotic lineages, Glomeromycota and Endogonales, lack numerous thiamine metabolism genes but the lack of fatty acid synthesis genes is specific to AM fungi. Many genes previously thought to be missing specifically in Glomeromycota are either missing in all analyzed phyla, or in some cases, are actually present in some of the analyzed AM fungal lineages, e.g. the high affinity phosphorus transporter Pho89. CONCLUSION: Based on a broad taxon sampling of fungal genomes we present a well-supported phylogeny for AM fungi and their sister lineages. We show that among these lineages, two independent evolutionary transitions to mutualistic plant symbiosis happened in a genomic background profoundly different from that known from the emergence of ectomycorrhizal fungi in Dikarya. These results call for further reevaluation of genomic signatures associated with plant symbiosis.

Naming the untouchable - environmental sequences and niche partitioning as taxonomical evidence in fungi.

Due to their submerged and cryptic lifestyle, the vast majority of fungal species are difficult to observe and describe morphologically, and many remain known to science only from sequences detected in environmental samples. The lack of practices to delimit and name most fungal species is a staggering limitation to communication and interpretation of ecology and evolution in kingdom Fungi. Here, we use environmental sequence data as taxonomical evidence and combine phylogenetic and ecological data to generate and test species hypotheses in the class Archaeorhizomycetes (Taphrinomycotina, Ascomycota). Based on environmental amplicon sequencing from a well-studied Swedish pine forest podzol soil, we generate 68 distinct species hypotheses of Archaeorhizomycetes, of which two correspond to the only described species in the class. Nine of the species hypotheses represent 78% of the sequenced Archaeorhizomycetes community, and are supported by long read data that form the backbone for delimiting species hypothesis based on phylogenetic branch lengths.Soil fungal communities are shaped by environmental filtering and competitive exclusion so that closely related species are less likely to co-occur in a niche if adaptive traits are evolutionarily conserved. In soil profiles, distinct vertical horizons represent a testable niche dimension, and we found significantly differential distribution across samples for a well-supported pair of sister species hypotheses. Based on the combination of phylogenetic and ecological evidence, we identify two novel species for which we provide molecular diagnostics and propose names. While environmental sequences cannot be automatically translated to species, they can be used to generate phylogenetically distinct species hypotheses that can be further tested using sequences as ecological evidence. We conclude that in the case of abundantly and frequently observed species, environmental sequences can support species recognition in the absences of physical specimens, while rare taxa remain uncaptured at our sampling and sequencing intensity.