Mosses are the dominant flora in Antartica, providing habitat for multiple microbial and invertebrate taxa and communities1,14. Endophytic and epiphytic fungi and bacteria are considered to be the dominant microorganisms present in these habitats, known as the bryosphere42,43,44.
A range of Antarctic moss species have been documented to be vulnerable to infection by ‘fairy ring disease’. In the current study comparing the microbial communities present in healthy, visibly infected (within the ring) and dead moss from the same moss carpet, we detected complex and diverse fungal and bacterial communities using a metabarcoding approach. Overall, the fungal community was richer (3.2 times greater) than that reported recently14 in a study using culture methods which detected 40 taxa in eight moss species sampled from different locations in the north-west Antarctic Peninsula region. Among the taxa reported by Rosa et al.14, only representatives of the genera Alpinaria, Helotiales, Cladosporium, Cadophora, Pseudogymnoascus, Glarea, Chalara, Ophiocordycipitaceae, Juncaceicola and the species Mortierella fimbricystis and Gyoerffyella entomobryoides were shared with the current study.
In the current study, relative abundance of the fungal taxa Alpinaria sp., Helotiaceae sp. 2, Coleophoma sp., Helotiales sp. 1, Chytridiomycota sp. 2, Rozellomycota sp. and Fungi sp. increased between healthy and infected moss samples, but was lower in dead moss. The genus Alpinaria (Melanommataceae) includes only a single described species (A. rhododendri) and seems to be common in the subalpine to alpine zone worldwide on twigs or buds of Rhododendron spp. (Ericaceae)45. It has recently been reported on mosses affected by fairy ring disease in maritime Antarctica14. The family Melanommataceae includes plant pathogenic species such as Gemmamyces piceae46 and, according to the FunGuild database47, A. rhododendri is considered a problable plant pathogenic and/or wood saprotrophic species.
The genus Coleophoma includes species reported as plant pathogenic, saprophytic or endophytic on different plant species48. Plant pathogens in the genus include C. fusiformis on leaves of Rhododendron49, C. eucalypti and C. eucalyptorum on Eucalyptus50, C. gevuinae on Gevuina51, C. empetri on Vaccinium52 and C. proteae on Protea caffra53. Rozellomycota species are common in temperate, sub-Arctic and Antarctic environments18. According to Grossart et al.54, all known Rozellomycota taxa are obligate pathogens of eukaryotes, including amoebae, fungi and algae. However, there are no reports of Rozellomycota acting as plant pathogens. Chytridiomycota, known as chytrids, primarily includes free-living saprophytic taxa present in aquatic and terrestrial environments. However, some species are reconized as plant pathogens, such as Synchytrium endobioticum that causes potato wart disease55.
The taxa Chaetothyriales sp. 1, Serendipita sp., Agaricomycetes sp., Sebacinales sp. and Knufia peltigerae are notable due their increase in abundance in dead relative to healthy moss carpet. They may therefore represent major decomposing taxa in the ecological succession following the death of Antarctic moss carpet. The order Chaetothyriales (Ascomycota) includes species with multiple ecological roles, including soil saprophytes, human and animal opportunistic pathogens and plant epi- and/or endophytes56. In addition, some representatives of Chaetothyriales are known to colonize extreme environments characterized by drought, oligotrophic conditions, extreme temperatures and high UV-radiation exposure 57. Some species are known phytopathogens 58.
Serendipita is a genus with eight known species38, including S. indica, formerly known as Piriformospora indica 59, an endophytic fungus detected in low-nutrient desert soil in Rajasthan, India60, which acts to increase nutrient uptake and utilization in its host61,62. Serendipita has been reported as an endophyte of bryophytes 63. Agaricomycetes is a class of Basidiomycota that includes almost 21,000 described species38 whose members play different ecologicals role such as decomposers, pathogens and mutualists in different environments64.
The order Sebacinales (Agaricomycetes, Basidiomycota) includes species recognized to show diverse interactions with plants, which range from mutualistic root endophytes (obligate biotrophs, mycorrhizae) to saprophytes59. Within the order, members of the family Serendipitaceae have been reported from the Antarctic Peninsula associated with the liverwort Barbilophozia hatcheri and the mosses Chorisodontium aciphyllum and Sanionia uncinata65.
The genus Knufa comprises black fungi and has six known species66. Knufia peltigerae is a lichenicolous fungus58 which, according to Lawrey & Diederich67, represents an important ecological group that form obligate associations with lichens. The ascomata of K. peltigerae (originally reported as Capronia peltigerae) was first described on thalli of the lichen Peltigera rufescens68,69. Peltigera rufescens is a cosmopolitan lichen that occurs on sub-Antarctic South Georgia, the South Orkney Islands and in various locations along the Antarctic Pensinula (both east and west coasts, including James Ross and Alexander Islands)70. Possibly analogous to the bleaching effect of fairy rings on mosses, Untereiner et al.69 reported the presence of K. peltigerae ascomata on decolourized or moribund P. rufescens thalli. However, it is unclear if K. peltigerae was responsible for the discolouration or represents an opportunistic fungus occurring on aging parts of the lichen thalli. The species has been rarely recorded taxa in Antarctica using culture approaches. de Souza et al.71 detected the DNA of K. peltigerae in cotton baits deposited in a lake at Hennequin point, King George Island, close to a moss carpet that was under attack from fairy ring disease.
The taxa Serendipita sp. and Agaricomycetes sp. occurred exclusively and were dominant in the dead moss carpet. Serendipita species include root fungal endophytes and arbuscular mycorrhizal fungi (AMF) known as plant growth promoters60. Bridge & Newsham72 reported Serendipita-like Sebacinale fungi in soil at Mars Oasis, Alexander Island, in the southern maritime Antarctic. The class Agaricomycetes includes about 21,000 described mushroom-forming species with ecological roles such as decomposers, pathogens and mutualists in different terrestrial and aquatic environments64.
Chalara sp. displayed high dominance in the healthy moss carpet, decreasing in dominance in infected moss. The genus includes 103 widespread species with multiple ecological functions38. Among Chalara species, C. fraxinea (teleomorph: Hymenoscyphus pseudoalbidus) has been reported as an emerging epidemic plant pathogen that has severely affected ash tree stands in Europe since 199073,74.
Previous studies have concluded that the causative agent of the fairy ring disease in Antarctica is Psychronectria hyperantarctica, identified using classical morphological techniques from its fruiting body9,13. However, despite the potentially high taxonomic resolution of the metabarcoding approach, we did not detect sequences of P. hyperantarctica in any samples. Rather, our data indicated the presence of several other recognized plant pathogenic fungi, supporting the suggestion of Rosa et al.14 that the disease may be caused by multiple fungal infections in parallel. The fungal taxa Alpinaria sp., Helotiaceae sp. 2, Coleophoma sp., Helotiales sp., Rozellomycota sp. and Chytridiomycota sp. 2 showed high levels of dominance in infected moss showing fairy ring symtoms, which deserve further detailed taxonomic characterization and assays in vivo using plant models to confirm whether they are able to cause plant disease symptoms. Robinson et al.6 demonstrated that moss vegetation in the Windmill Islands, East Antarctica is changing rapidly in response to a drying climate causing declining viability in some species. It is possible that the incidence of fungal attack, evidenced by the fairy ring disease, might be connected to a decrease in moss health resulting from climatic changes in the Antarctic Peninsula region in recent decades, although no studies have specifically addressed this or directly quantified disease incidence.
Few studies have addressed the bacterial communities associated with Antarctic mosses. Park et al.75 studied endophytic bacteria associated with healthy material of the moss Sanionia uncinata. To our knowledge, no studies have focused on the bacterial diversity present specifically in mosses affected by the fairy ring disease in Antartica. However, the overall dominance of the phyla Actinobacteriota, Proteobacteria, Bacteroidota and Cyanobacteria documented here are consistent with studies such as those of Holland-Moritz et al.76 and Wang et al.77, which reported that moss-associated bacterial communities were commonly dominated by Proteobacteria and Bacteroidetes. Using molecular phylogenetic techniques to analyse the bacterial diversity associated with aquatic moss pillars in continental Antarctic lakes, Nakai et al.78 reported Proteobacteria, Cyanobacteria and Firmicutes as dominant groups. Park et al.75 and Câmara et al.79 reported highest relative abundances of sequences representing the phylum Actinobacteria in a transplanted S. uncinata carpet moss in a study also carried out on Keller Peninsula. Raymond80 reported Actinobacteria (genera Conexibacter, Rhodococcus, Marmoricola, Micromonospora and Streptomyces) and Bacteroidetes (genera Flavobacterium, Segetibacterium, Epilithonimonas and Pedobacter) from Bryum argenteum leaves, further suggesting that they may offer the moss some freezing protection.
The dominance of Microbacteriaceae sp. (Actinobacteriota) in the assemblage of fairy ring affected moss may be notable. Representatives of Actinobacteria are among the most common prokaryotic organisms in Antarctic terrestrial environments81. They are also known as prolific producers of bioactive natural products82, including some able to suppress plant diseases83. Gu et al.84 analysed the diversity and composition of fungal and bacterial communities in continuous cropping soil from Chinese chive cultivation, reporting dominance of Actinobacteria in the same samples where potential phytopathogenic fungi were detected. We found a similar high Actinobacteria abundance pattern to that reported by Gu et al.84 in fairy ring infected moss, which may suggest that the abundance of Microbacteriaceae sp. is linked with the presence of pathogenic fungi causing the fairy ring symptons.
The presence of members of the phylum Chloroflexi may indicate involvement with organic matter degradation85. Suominen et al.86 reported Chloroflexi as important agents of decomposition in the Black Sea sulphidic zone. Colatriano et al.87 reported that the genomes of Chloroflexi from the Arcic Ocean include several aromatic compound degradation genes.
Cyanobacteriia sp. and Haliangium sp. (Myxococcota) were present in all moss samples, but were the most abundant taxa detected in dead moss. Cyanobacteria are the dominant phototrophs in Antarctic terrestrial and freshwater ecosystems88 and represent the greatest accumulation of biomass the benthic habitats of lakes and ponds89. Pandey et al.90 reported several cyanobacterial taxa in association with mosses sampled in the Schirmacher Oasis, continental Antarctica. The primary habitats of myxobacteria such as Haliangium are rich in organic matter91. These bacteria are strictly aerobic and usually live in the surface layers of the soil, but can also be found in decaying plant material92. The dominance of these two taxa in dead moss may be due the high concentration of minerals released during the organic decomposition of the moss.