Benthic Biofilms in Glacier-Fed Streams from Scandinavia to the Himalayas Host Distinct Bacterial Communities Compared with the Streamwater

Abstract

Microbial life in glacier-fed streams (GFSs) is dominated by benthic biofilms which fulfill critical ecosystem processes. However, it remains unclear how the bacterial communities of these biofilms assemble in stream ecosystems characterized by rapid turnover of benthic habitats and high suspended sediment loads. Using16S rRNA gene amplicon sequence data collected from 54 GFSs across the Himalayas, European Alps, and Scandinavian Mountains, we found that benthic biofilms harbor bacterial communities that are distinct from the bacterial assemblages suspended in the streamwater. Our data showed a decrease in species richness in the benthic biofilms compared to the bacterial cells putatively free-living in the water. The benthic biofilms also differed from the suspended water fractions in terms of community composition. Differential abundance analyses highlighted bacterial families that were specific to the benthic biofilms and the suspended assemblages. Notably, source-sink models suggested that the benthic biofilm communities are not simply a subset of the suspended assemblages. Rather, we found evidence that deterministic processes (e.g., species sorting) shape the benthic biofilm communities. This is unexpected given the high vertical mixing of water and contained bacterial cells in GFSs and further highlights the benthic biofilm mode of life as one that is determined through niche-related processes. Our findings therefore reveal a "native" benthic biofilm community in an ecosystem that is currently threatened by climate-induced glacier shrinkage. IMPORTANCE Benthic biofilms represent the dominant form of life in glacier-fed streams. However, it remains unclear how bacterial communities within these biofilms assemble. Our findings from glacier-fed streams from three major mountain ranges across the Himalayas, the European Alps and the Scandinavian Mountains reveal a bacterial community associated with benthic biofilms that is distinct from the assemblage in the overlying streamwater. Our analyses suggest that selection is the underlying process to this differentiation. This is unexpected given that bacterial cells that are freely living or attached to the abundant sediment particles suspended in the water continuously mix with the benthic biofilms. The latter colonize loose sediments that are subject to high turnover owing to the forces of the water flow. Our research unravels the existence of a microbiome specific to benthic biofilms in glacier-fed streams, now under major threats due to global warming.

Keywords: benthic biofilms; community assembly; community composition; glacier-fed streams.

FIG 1

Taxonomic composition of benthic biofilms and source assemblages. (A) The upset plot depicts the number of unique and shared ASVs among benthic biofilms, unattached (UC), and attached cells (UC+AC) from the overlying streamwater and the relative abundance characterizing each set. (B) The stacked bar plot illustrates the average relative abundance of shared and/or unique ASVs across benthic biofilms and water assemblages. To increase clarity on the barplot, features were agglomerated at the family level.

FIG 2

Patterns of alpha and beta diversity for benthic biofilms and water assemblages. (A) Richness of ASV for benthic biofilms (n = 142), composite samples of unattached cells (UC) and cells attached to suspended particles (AC) suspended in the streamwater (AC+UC; n = 46), and UC (n = 45) alone. Box plots show the median (horizontal line), interquartile range (box height), 1.5x beyond the interquartile range (whiskers), and outliers. Letters indicate significant differences based on pairwise comparisons (P < 0.05). (B) Differences in community composition shown in the nonmetric multidimensional scaling (NMDS) space as based on Bray-Curtis dissimilarity.

FIG 3

Differential abundance analyses highlighting taxonomic differences between benthic biofilms and streamwater assemblages across the bacterial tree. (A) Taxonomic tree showing bacterial taxa that are on average over-represented in the benthic biofilms compared with the unattached cells (UC) in the streamwater. (B) Taxonomic tree showing bacterial taxa that are on average over-represented in the benthic biofilms compared with the unattached and attached cells (UC+AC) in the streamwater. Size and color of the edges and nodes are directly correlated with the abundance of bacteria within each fraction.

FIG 4

Dominant assembly processes regarding sample pairs of benthic biofilms compared with the assemblages in the streamwater for glacier-fed streams from each mountain range. (A) Results regarding comparisons of benthic biofilms versus unattached and attached cells (UC+AC). (B) Results regarding comparisons of benthic biofilms versus unattached cells (UC) only.