Endolithic Fungal Species Markers for Harshest Conditions in the McMurdo Dry Valleys, Antarctica

Abstract

The microbial communities that inhabit lithic niches inside sandstone in the Antarctic McMurdo Dry Valleys of life's limits on Earth. The cryptoendolithic communities survive in these ice-free areas that have the lowest temperatures on Earth coupled with strong thermal fluctuations, extreme aridity, oligotrophy and high levels of solar and UV radiation. In this study, based on DNA metabarcoding, targeting the fungal Internal Transcribed Spacer region 1 (ITS1) and multivariate statistical analyses, we supply the first comprehensive overview onto the fungal diversity and composition of these communities sampled over a broad geographic area of the Antarctic hyper-arid cold desert. Six locations with surfaces that experience variable sun exposure were sampled to compare communities from a common area across a gradient of environmental pressure. The Operational Taxonomic Units (OTUs) identified were primarily members of the Ascomycota phylum, comprised mostly of the Lecanoromycetes and Dothideomycetes classes. The fungal species Friedmanniomyces endolithicus, endemic to Antarctica, was found to be a marker species to the harshest conditions occurring in the shady, south exposed rock surfaces. Analysis of community composition showed that sun exposure was an environmental property that explained community diversity and structured endolithic colonization.

Keywords: Antarctica; ITS metabarcoding; McMurdo Dry Valleys; cryptoendolithic communities; fungi; marker species.

Figure 1

Map of the McMurdo Dry Valleys (Southern Victoria Land), by Google Earth. (A,B) Siegfried Peak north and south, respectively; (C,D) Knobhead north and south, respectively; (E,F). Sample collected at Linnaeus Terrace north and sampling site in south sun-exposure, respectively; (G,H) Samples collected at University Valley north and south, respectively; (I,L) Samples collected at Finger Mt. north and south, respectively; (M) Mt. Elektra north; (N) View of Mt. Elektra peak (southern surface has not been sampled).

Figure 2

(A) Fungal taxonomic composition bar plot at class level; (B) alpha diversity measure of Dothideomycetes class; (C) Fungal taxonomic composition bar plot at family level; (D) alpha diversity measure of Teratosphaeriaceae family; (E) Fungal taxonomic composition bar plot at genus level; (F) alpha diversity measure of Friedmanniomyces genus. Taxa with <1% abundance were not included. Boxplots show 25th and 75th percentile, while error bars 1st and 99th. percentile. Tukey HSD significant differences (P < 0.05) are indicated by different letters. Classes (Leotiomycetes, Sordariomycetes, Taphrinomycetes, Basidiobolomycetes, Arthoniomycetes, Mortierellomycetes, and Pezizomycetes), families (Didymellaceae, Extremaceae, Taphrinaceae, Herpotrichiellaceae, and Cladosporiaceae) and genera (Pleopsidium, Extremus, Taphrina, Elasticomyces, Cryomyces, Cladophialophora, and Knufia) with <1% abundance were not showed.

Figure 3

Boxplots show biodiversity measures in north and south sun-exposed cryptoendolithic communities. (A) Number of reads, (B) richness, (C) Shannon’s index, (D) Simpson’s index. Boxplots show 25th and 75th percentile, while error bars show 1st and 99th percentile. Letters indicate no significant differences in one-way ANOVA Tukey test (significant for p < 0.05).

Figure 4

(A) Non-metric multidimensional scaling (NMDS) ordination plots for fungal cryptoendolithic communities differently sun-exposed, based on square-root transformed abundance data (PERMANOVA, p < 0.05). Stress value is 0.07. Since both approaches produced similar results, we showed results based on abundance only. MtEN1, MtEN2, MtEN3 = Mt. Elektra north sample 1, 2, and 3, respectively; FMtN1 and FMtN2 = Finger Mt. north sample 1 and 2, respectively; FMtS1 and FMtS2 = Finger Mt. south sample 1 and 2, respectively; UVS2 = University Valley south sample 2. (B) Venn diagram shows the distribution of fungal OTUs between north and south exposition. Both the percentages of OTUs that were shared and found exclusively in each sun exposure are indicated.