Antarctic ice-free terrestrial microbial functional redundancy in core ecological functions and microhabitat-specific microbial taxa and adaptive strategy

Abstract

Background: Although ice-free terrestrial ecosystems in Antarctica cover only limited areas, they harbor diverse and metabolically active microbial communities. These ecosystems encompass distinct microhabitats such as mosses, lichens, and soils, each offering unique ecological niches. However, how different microbial taxa respond to microhabitat heterogeneity, ecological strategies such as functional redundancy and specialization contribute to adaptation in extreme environments remains underexplored. To address these questions, we employed high-throughput 16 S rRNA gene and ITS sequencing in combination with GeoChip-based functional gene profiling to assess the structure and functional potential of microbial communities across moss, lichen and soil microhabitats in Antarctic ice-free terrestrial ecosystem.

Results: Microhabitat type has a greater influence on microbial community structure and function in the ice-free Antarctic terrestrial ecosystem than geographical location. Though all prokaryotic communities were dominated by Pseudomonadota, Nostoc and Endobacter were significantly enriched in the moss and lichen microhabitats, respectively. Meanwhile, all fungal communities were primarily dominated by Ascomycota and Basidiomycota, with Byssoloma and Usnea showing significant enrichment in the moss and lichen microhabitats, respectively. Despite these taxonomic differences, the three microhabitats show similar core ecological functions with widespread microbial functional redundancy. Nevertheless, clear microhabitat-specific functional specialization was suggested. For example, moss microhabitat was enriched in Pyoverdin_pvcC and Zeaxanthin_glucosyltransferase, sdhA, lichen microhabitat harbored higher levels of nhaA, nikC, vacuolar_iron_transport, mttB, glucoamylase, pel_Cdeg, pme_Cdeg, rgh, rgl, while soil microhabitat was enriched in 5f1_ppn and isopullulanase. Notably, genes involved in carotenoid biosynthesis were significantly more abundant in moss and lichen microhabitats than in soil microhabitat, indicating the adaptive capacity of symbiotic microorganisms to mitigate ultraviolet radiation and oxidative stress to protect their hosts.

Conclusions: Microbial communities associated with distinct microhabitats (i.e. mosses, lichens, and soils) in Antarctic ice-free terrestrial ecosystem exhibit both functional redundancy in core ecological functions and microhabitat-specific specialization in key microbial taxa and adaptive strategy.

Keywords: Geochip functional microarray; High-throughput sequencing; Ice-free Antarctic terrestrial ecosystem; Lichen; Microbiome; Moss; Soil.

Fig. 1

Comparative analysis of microbial and gene diversity among moss, lichen and soil microhabitats. a: The box plot displays the Shannon diversity index of prokaryotes for GM, GL, GS, NL, NS, PL and PS. b: Prokaryotic NMDS analysis of GM, GL, GS, NL, NS, PL and PS based on weighted Unifrac distances. c: Venn diagrams showing prokaryotic shared and unique OTU among moss, lichen and soil samples. d: The box plot displays the Shannon diversity index of fungi for GM, GL, GS, NL, NS, PL and PS. e: Fungal PCA analysis of sample GM, GL, GS, NL, NS, PL and PS. f: Venn diagrams showing fungal shared and unique OTU among moss, lichen and soil samples. g: The box plot displays the Shannon diversity index of functional genes for GM, GL, GS, NL, NS, PL, and PS. h: PCA clustering analysis of functional genes of all samples. i: Venn diagrams showing shared and unique functional genes among moss, lichen and soil samples. Note: GM-Great Wall Station moss; GL-Great Wall Station lichen; GS-Great Wall Station soil; NL-Nelson Island lichen; NS-Nelson Island soil; PL-Penguin Island lichen; PS-Penguin Island soil. Letter is used to distinguish whether there is significant difference between groups, and different letters indicate the presence of display differences between groups (P < 0.05, ANOVA, Tukey HSD test)

Fig. 2

Statistical analysis of top 20 prokaryotic and fungal genera. a: Box plot showing differences in prokaryote diversity among moss, lichen, and soil samples. b: Box plot showing differences in fungal diversity among moss, lichen, and soil samples. The same letter means no significant difference while the different letters mean significant difference according to Tukey’s HSD test results

Fig. 3

Relative abundance difference of genes among moss, lichen and soil microhabitats. The statistical significance among moss, lichen, and soil samples was tested using a two-sided Student’s t test (*p < 0.05, **p < 0.01, ***p < 0.001, ****p < 0.0001)

Fig. 4

Relative abundance difference of metal homeostasis among moss, lichen and soil microhabitats. a: Comparison of metal homeostasis categories. b: Comparison of transport categories. c: Relative abundance comparison of functional genes related to iron, magnesium, nickel, potassium, sodium. The heatmap displays variations in the relative abundance of genes. Z-score normalization was applied across rows to standardize the data. The color scale ranges from blue, representing lower gene abundance (negative Z-scores), to red, representing higher gene abundance (positive Z-scores). Blue corresponds to mosses, orange to lichens, and gray to soil microbes. The size of the circles indicates statistical significance, with larger circles representing smaller p-values and thus more pronounced differences. The color depth signifies the degree of difference, with deeper red indicating greater disparities. The statistical significance among moss, lichen, and soil samples was tested using pairwise t-tests. The p-values were adjusted for multiple comparisons using the Benjamini-Hochberg method to control the false discovery rate (FDR). Genes with an adjusted p-value less than 0.05 were considered to have significantly different relative abundance

Fig. 5

C/N/S cycling of moss, lichen and soil microhabitats. a: Comparison of subcategory1 in carbon cycling categories. b: Carbon cycling process. c: Comparison of subcategory1 in nitrogen cycling categories. d: Nitrogen cycling process. e: Comparison of subcategory1 in sulfur cycling categories. f: Sulfur cycling process. The statistical significance among moss, lichen, and soil samples was tested using a two-sided Student’s t test (*p < 0.05, **p < 0.01, ***p < 0.001, ****p < 0.0001)

Fig. 6

Statistical analysis of functional genes involved in C, N, S, and P cycling across moss, lichen, and soil microhabitats. a: Comparison of carbon degradation categories. b: Comparison of subcategory1 differences in phosphorus cycling categories. c Statistical analysis on the relative abundance of functional genes related to carbon degradation, denitrification, sulfite reduction, polyphosphate degradation. The heatmap displays variations in the relative abundance of different genes in moss, lichen, and soil samples. Z-score normalization was applied across rows to standardize the data. The color scale ranges from blue, representing lower gene abundance (negative Z-scores), to red, representing higher gene abundance (positive Z-scores). Blue, orange and gray correspond to moss, lichen and soil samples, respectively. Bubble plots show the differences in gene intensity and statistical significance between moss and lichen samples, moss and soil samples, and lichen and soil samples. The size of the circles indicates statistical significance, with larger circles representing smaller p-values and thus more pronounced differences. The color depth signifies the degree of difference, with deeper red indicating greater disparities. The statistical significance among moss, lichen, and soil samples was tested using pairwise t-tests. The p-values were adjusted for multiple comparisons using the Benjamini-Hochberg method to control the false discovery rate (FDR). Genes with an adjusted p-value less than 0.05 were considered to have significantly different relative abundance. The statistical significance among moss, lichen and soil samples was tested using a two-sided Student’s t test (*p < 0.05, **p < 0.01, ***p < 0.001, ****p < 0.0001)

Fig. 7

Adaptation to Antarctic environment of moss, lichen and soil microbiome. a: Oligotrophy. b: Cold adaptation. c: UV resistance. d: Relative abundance comparison of functional genes related to carotenoid. The heatmap displays variations in the relative abundance of genes. Z-score normalization was applied across rows to standardize the data. The color scale ranges from blue, representing lower gene abundance (negative Z-scores), to red, representing higher gene abundance (positive Z-scores). Blue corresponds to mosses, orange to lichens, and gray to soil microbes. The size of the circles indicates statistical significance, with larger circles representing smaller p-values and thus more pronounced differences. The color depth signifies the degree of difference, with deeper red indicating greater disparities. The statistical significance among moss, lichen, and soil samples was tested using pairwise t-tests. The p-values were adjusted for multiple comparisons using the Benjamini-Hochberg method to control the false discovery rate (FDR). Genes with an adjusted p-value less than 0.05 were considered to have significantly different relative abundance