Microbial biodiversity in glacier-fed streams

Abstract

While glaciers become increasingly recognised as a habitat for diverse and active microbial communities, effects of their climate change-induced retreat on the microbial ecology of glacier-fed streams remain elusive. Understanding the effect of climate change on microorganisms in these ecosystems is crucial given that microbial biofilms control numerous stream ecosystem processes with potential implications for downstream biodiversity and biogeochemistry. Here, using a space-for-time substitution approach across 26 Alpine glaciers, we show how microbial community composition and diversity, based on 454-pyrosequencing of the 16S rRNA gene, in biofilms of glacier-fed streams may change as glaciers recede. Variations in streamwater geochemistry correlated with biofilm community composition, even at the phylum level. The most dominant phyla detected in glacial habitats were Proteobacteria, Bacteroidetes, Actinobacteria and Cyanobacteria/chloroplasts. Microorganisms from ice had the lowest α diversity and contributed marginally to biofilm and streamwater community composition. Rather, streamwater apparently collected microorganisms from various glacial and non-glacial sources forming the upstream metacommunity, thereby achieving the highest α diversity. Biofilms in the glacier-fed streams had intermediate α diversity and species sorting by local environmental conditions likely shaped their community composition. α diversity of streamwater and biofilm communities decreased with elevation, possibly reflecting less diverse sources of microorganisms upstream in the catchment. In contrast, β diversity of biofilms decreased with increasing streamwater temperature, suggesting that glacier retreat may contribute to the homogenisation of microbial communities among glacier-fed streams.

Figure 1

Community composition in glacial ice, streamwater and biofilms. Non-metric multidimensional scaling analysis of microbial communities based on Bray–Curtis dissimilarities in 26 glacial ecosystems (stress=0.16). Ellipses represent the 95% confidence interval.

Figure 2

Distribution of taxonomic groups in glacial ice, streamwater and biofilm. The percentage of (a) phyla and (b) the 50 most abundant families associated with each habitat is visualised in ternary plots. The position in the triangle indicates the relative abundance of each taxon among the three habitats; the size of the circle represents the relative abundance of taxa.

Figure 3

Heat map of Pearson correlations between environmental variables and families detected in biofilms. Colours represent the r-values of Pearson correlations between relative abundances of the 45 most abundant bacterial families and environmental parameters. Families were ordered according to taxonomic affiliations. We found several families that were strongly correlated to pH and electrical conductivity. Positive correlations with DOC were only found with Proteobacteria. Streamwater temperature and total nitrogen were only weakly related to the abundance of taxonomic families.

Figure 4

Microbial α diversity. (a) Boxplot representation of rarefied richness (all samples rarefied to 1007 reads) and ‘true richness' estimated by fitting Sichel distribution curves to the abundance distributions obtained from the 454-pyrosequencing data. Median (line), 1st and 3rd quartile (box margins), 5 and 95% percentiles (whiskers), outliers (points). Different letters on each box represent significant differences between habitats as determined by Wilcoxon tests followed by Bonferroni correction (P<0.01). (b,c) Microbial richness decreased with higher elevation. Linear regression include 95% confidence intervals in the (b) streamwater and (c) biofilms.

Figure 5

Spatial variation of microbial communities. (a) β diversities of the three habitats as the average distance of communities to the group (that is, habitat) centroid after principal coordinate analysis of the Bray–Curtis dissimilarity matrix. β diversity differed significantly among habitats (pseudo-F=17.082, d.f.₁=2, d.f.₂=75, P<0.001 for all pairwise comparisons). (b) Graphical analysis of biofilm β diversity as a function of streamwater temperature by local polynomial regression fitting. Multiple linear regression on distance matrices revealed β diversity to decline significantly with increasing streamwater temperature (pseudo-t=−4.77, P<0.05). The shaded area gives a bootstrap confidence interval for the generated trendline. See Materials and methods and Supplementary Information for computational details.