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Lichens are the archetypal symbiosis and the one for which the term was coined. Although application of shotgun sequencing techniques has shown that many lichen symbioses can harbour more symbionts than the canonically recognized fungus and photobiont, no global census of lichen organismal composition has been undertaken. Here, we analyze the genome content of 437 lichen metagenomes from six continents, and show that four bacterial lineages occur in the majority of lichen symbioses, at a frequency on par with algal photobionts. A single bacterial genus,Lichenihabitans, occurs in nearly one-third of all lichens sampled. Genome annotations from the most common lichen bacterial symbionts suggest they are aerobic anoxygenic photoheterotrophs and produce essential vitamins, but do not fix nitrogen. We also detected secondary basidiomycete symbionts in about two-thirds of analyzed metagenomes. Our survey suggests a core set of four to seven microbial symbionts are involved in forming and maintaining lichen symbioses.

Ascomycota account for about two-thirds of named fungal species.1 Over 98% of known Ascomycota belong to the Pezizomycotina, including many economically important species as well as diverse pathogens, decomposers, and mutualistic symbionts.2 Our understanding of Pezizomycotina evolution has until now been based on sampling traditionally well-defined taxonomic classes.3,4,5 However, considerable diversity exists in undersampled and uncultured, putatively early-diverging lineages, and the effect of these on evolutionary models has seldom been tested. We obtained genomes from 30 putative early-diverging lineages not included in recent phylogenomic analyses and analyzed these together with 451 genomes covering all available ascomycete genera. We show that 22 of these lineages, collectively representing over 600 species, trace back to a single origin that diverged from the common ancestor of Eurotiomycetes and Lecanoromycetes over 300 million years BP. The new clade, which we recognize as a more broadly defined Lichinomycetes, includes lichen and insect symbionts, endophytes, and putative mycorrhizae and encompasses a range of morphologies so disparate that they have recently been placed in six different taxonomic classes. To test for shared hidden features within this group, we analyzed genome content and compared gene repertoires to related groups in Ascomycota. Regardless of their lifestyle, Lichinomycetes have smaller genomes than most filamentous Ascomycota, with reduced arsenals of carbohydrate-degrading enzymes and secondary metabolite gene clusters. Our expanded genome sample resolves the relationships of numerous “orphan” ascomycetes and establishes the independent evolutionary origins of multiple mutualistic lifestyles within a single, morphologically hyperdiverse clade of fungi.

Basidiomycete yeasts have recently been reported as stably associated secondary fungal symbionts of many lichens, but their role in the symbiosis remains unknown. Attempts to sequence their genomes have been hampered both by the inability to culture them and their low abundance in the lichen thallus alongside two dominant eukaryotes (an ascomycete fungus and chlorophyte alga). Using the lichen Alectoria sarmentosa, we selectively dissolved the cortex layer in which secondary fungal symbionts are embedded to enrich yeast cell abundance and sequenced DNA from the resulting slurries as well as bulk lichen thallus. In addition to yielding a near-complete genome of the filamentous ascomycete using both methods, metagenomes from cortex slurries yielded a 36- to 84-fold increase in coverage and near-complete genomes for two basidiomycete species, members of the classes Cystobasidiomycetes and Tremellomycetes. The ascomycete possesses the largest gene repertoire of the three. It is enriched in proteases often associated with pathogenicity and harbors the majority of predicted secondary metabolite clusters. The basidiomycete genomes possess ∼35% fewer predicted genes than the ascomycete and have reduced secretomes even compared with close relatives, while exhibiting signs of nutrient limitation and scavenging. Furthermore, both basidiomycetes are enriched in genes coding for enzymes producing secreted acidic polysaccharides, representing a potential contribution to the shared extracellular matrix. All three fungi retain genes involved in dimorphic switching, despite the ascomycete not being known to possess a yeast stage. The basidiomycete genomes are an important new resource for exploration of lifestyle and function in fungal-fungal interactions in lichen symbioses.

Basidiomycete yeasts have recently been reported as stably associated secondary fungal symbionts of many lichens, but their role in the symbiosis remains unknown. Attempts to sequence their genomes have been hampered both by the inability to culture them and their low abundance in the lichen thallus alongside two dominant eukaryotes (an ascomycete fungus and chlorophyte alga). Using the lichen Alectoria sarmentosa, we selectively dissolved the cortex layer in which secondary fungal symbionts are embedded to enrich yeast cell abundance and sequenced DNA from the resulting slurries as well as bulk lichen thallus. In addition to yielding a near-complete genome of the filamentous ascomycete using both methods, metagenomes from cortex slurries yielded a 36- to 84-fold increase in coverage and near-complete genomes for two basidiomycete species, members of the classes Cystobasidiomycetes and Tremellomycetes. The ascomycete possesses the largest gene repertoire of the three. It is enriched in proteases often associated with pathogenicity and harbors the majority of predicted secondary metabolite clusters. The basidiomycete genomes possess ∼35% fewer predicted genes than the ascomycete and have reduced secretomes even compared with close relatives, while exhibiting signs of nutrient limitation and scavenging. Furthermore, both basidiomycetes are enriched in genes coding for enzymes producing secreted acidic polysaccharides, representing a potential contribution to the shared extracellular matrix. All three fungi retain genes involved in dimorphic switching, despite the ascomycete not being known to possess a yeast stage. The basidiomycete genomes are an important new resource for exploration of lifestyle and function in fungal–fungal interactions in lichen symbioses.

The lichen, to which the name Lecidea lichenicola is found to have been misapplied, was first described from England and is an extreme specialist of chalk pebbles. It has long been known that it is not closely related to Lecidea in the strict sense, but its true evolutionary relationships have been unknown. Here we use metagenome-assembled genome data to place this fungus in a six-locus phylogeny of Ascomycota, and find strong support for its placement in the class Lichinomycetes. Multiple gene trees using existing data from Lichinomycetes support its further placement within the family Lichinaceae. Based on a revision of types and original descriptions, we conclude that the earliest name for this species is Lecidea obsoleta (syn. Thrombium cretaceum). We neotypify that name by a modern collection and accommodate it in the new genus Watsoniomyces. Type and other original material of L. lichenicola (syn. Discocera lichenicola) was re-examined and found not to be on chalk and to represent a different lichen, Trapelia glebulosa. Watsoniomyces is the first described member of Lichinomycetes with an endolithic thallus.

Colombia, con cerca de 1674 especies de líquenes, es uno de los países con mayor diversidad de estos organismos en el neotrópico. A pesar del gran esfuerzo del Catálogo de Flora de Colombia, no se cuenta con listados de las principales ciudades del país. Este trabajo es el primer esfuerzo en mostrar un listado preliminar de especies de hongos liquenizados de Cali, la tercera la ciudad del país. Este catálogo contiene 208 especies, 68 géneros y 30 familias. La mayoría de las especies de líquenes fueron costrosos (63%) y foliosos (29%). Este listado para Cali representa un 13% de las especies presentes en el catálogo actual de Colombia.

The aim of this study was to evaluate the spatial effect of a natural source of sulphur pollution on the species diversity, richness and distribution of corticolous lichens in a páramo zone at the mine ‘El Vinagre’ (Puracé, Cauca, Colombia). Three zones at different distances from the pollution source were established: zone 1 with a high degree of contamination, a potentially mildly affected or transitional zone 2, and a zone 3 free of disturbance. In each zone, 10 phorophytes ofWeinmannia microphylla(Cunoniaceae) were sampled, and all lichens in a 150 cm vertical transect 50 cm above the ground were collected and identified. Phorophyte parameters were measured (bark pH and diameter at breast height) and the samples were georeferenced. In order to evaluate the impact on lichens, non-metric multidimensional scaling (NMS) and indicator species analysis were carried out. ANOVA and Spearman correlations were performed to assess the relationships of environmental and tree variables between zones and with lichen community structure. The index of atmospheric purity (IAP) and the environmental rating factor (FCA) were evaluated for the three zones. In total, 104 lichen species were recorded, of which 72 were identified to species, 17 to genus, and four to family; 11 samples could not be identified. NMS clustered samples according to zone and the main axis which were correlated with bark pH and distance from pollution source. We found eight indicator species characterizing different zones, and four marginally significant indicator species. Using the IAP, we established three isocontamination areas, with zones 2 and 3 classified as more or less pristine zones and zone 1 as a polluted zone (supported by bark pH as a proxy for current pollution). Diversity was lowest in zone 1, closest to the pollution source, and lichen species composition differed between zones. Differences between lichens in zones 2 and 3 appear mostly unrelated to the current pollution source and might be more related to historical differences in impact from a 20-year-old pollution source.

Tropical moist forests are ecosystems of high biodiversity and high endemism, like the Choco biogeographic ecoregion. Few studies have characterized this vegetation system, and less attention has been given to the epiphytes. The aim of this study, was to evaluate the diversity and composition of vascular and nonvascular epiphytes, in a transition zone between tropical moist forest and tropical dry forest in the Choco biogeographic region of Valle del Cauca, Colombia. For this study, the data were grouped into six zones along the Loboguerrero-Buenaventura road: Zone 1 was closest to the Pacific Ocean (tropical moist forest) and Zone 6 was closest to the subxerophytic enclave of The Dagua River (transition zone to tropical dry forest). The data also were grouped depending on exposure to light (microsites), and the sites were categorized as open, semi-open and closed. A total of 43 trees densely covered by epiphytes were sampled: non-vascular epiphytes were sampled up to 2 m high, while vascular epiphytes were sampled along the entire phorophyte. A total of 485 specimens of non-vascular epiphytes belonging to 77 species of lichens, five of liverworts and eight of mosses were collected, for a total of 90 species. In addition, 5 987 individuals belonging to 24 species of vascular epiphytes were found; Bromeliaceae (six species) was the richest in species, followed by Gesneriaceae, Orchidaceae and Polypodiaceae (each with four species). We found 25 new records of lichens for Colombia and 26 for the Choco biogeographic region; for vascular epiphytes, we found 11 new records for this same Choco region. The richness and diversity of nonvascular epiphytic communities were affected by the zone and the microsite in which the trees were located, while the vascular epiphytic communities, were affected by the zone along the road. Thus, the richness and diversity of the communities of nonvascular epiphytes were affected by both the forest type and the microsite where the trees were found, while communities of vascular epiphytes, were affected only by the forest type. Los bosques húmedos tropicales son ecosistemas que acumulan una alta biodiversidad y alto endemismo, principalmente en la ecorregión del Chocó biogeográfico. La vegetación en esta zona ha sido poco estudiada, sobre todo para el grupo de las epífitas. De esta forma, el objetivo de este trabajo fue evaluar la diversidad y composición de estas plantas (vasculares y no vasculares) en una zona de transición entre bosque húmedo tropical y bosque seco tropical en el Chocó biogeográfico. Se muestrearon 43 árboles con abundante cobertura de epífitas: las no vasculares fueron muestreadas hasta los 2 m de altura, mientras que las vasculares a lo largo de todo el forófito. Los datos se agruparon en seis zonas a lo largo de la vía, siendo la zona 1 la más cercana al Pacífico (bosque húmedo tropical) y la zona 6 la más cercana al enclave subxerofítico del río Dagua (bosque seco tropical); también se agruparon dependiendo de la exposición a la luz en tres micrositios: abiertos, semi abiertos y cerrados. Se recolectaron 485 ejemplares de epífitas no vasculares pertenecientes a 77 especies de líquenes, cinco de hepáticas y ocho de musgos, para un total de 90 especies. Por otro lado, se registraron 5 987 individuos pertenecientes a 24 especies de epífitas vasculares, siendo la familia Bromeliaceae la más rica en especies (seis especies), seguida de Gesneriaceae, Orchidaceae y Polypodiaceae (cuatro especies). Se encontraron 25 nuevos registros de líquenes para Colombia, 26 para el Chocó biogeográfico, también 11 nuevos registros de epífitas vasculares para Chocó biogeográfico. La riqueza y diversidad de las comunidades de no vasculares fueron afectadas por la zona y el micrositio donde estaban los árboles, mientras que en las comunidades de vasculares, fueron afectadas por la zona a lo largo de la carretera.