Glacier-fed streams (GFSs) are extreme and rapidly vanishing ecosystems, and yet they harbor diverse microbial communities. Although our understanding of the GFS microbiome has recently increased, we do not know which microbial clades are ecologically successful in these ecosystems, nor do we understand potentially underlying mechanisms. Ecologically successful clades should be more prevalent across GFSs compared to other clades, which should be reflected as clade-wise distinctly low phylogenetic turnover. However, methods to assess such patterns are currently missing. Here we developed and applied a novel analytical framework, “phyloscore analysis”, to identify clades with lower spatial phylogenetic turnover than other clades in the sediment microbiome across twenty GFSs in New Zealand. These clades constituted up to 44% and 64% of community α-diversity and abundance, respectively. Furthermore, both their α-diversity and abundance increased as sediment chlorophyll a decreased, corroborating their ecological success in GFS habitats largely devoid of primary production. These clades also contained elevated levels of putative microdiversity than others, which could potentially explain their high prevalence in GFSs. This hitherto unknown microdiversity may be threatened as glaciers shrink, urging towards further genomic and functional exploration of the GFS microbiome.

In glacier-fed streams, ecological windows of opportunity allow complex microbial biofilms to develop and transiently form the basis of the food web, thereby controlling key ecosystem processes. Using metagenome-assembled genomes, we unravel strategies that allow biofilms to seize this opportunity in an ecosystem otherwise characterized by harsh environmental conditions. We observe a diverse microbiome spanning the entire tree of life including a rich virome. Various co-existing energy acquisition pathways point to diverse niches and the exploitation of available resources, likely fostering the establishment of complex biofilms during windows of opportunity. The wide occurrence of rhodopsins, besides chlorophyll, highlights the role of solar energy capture in these biofilms while internal carbon and nutrient cycling between photoautotrophs and heterotrophs may help overcome constraints imposed by oligotrophy in these habitats. Mechanisms potentially protecting bacteria against low temperatures and high UV-radiation are also revealed and the selective pressure of this environment is further highlighted by a phylogenomic analysis differentiating important components of the glacier-fed stream microbiome from other ecosystems. Our findings reveal key genomic underpinnings of adaptive traits contributing to the success of complex biofilms to exploit environmental opportunities in glacier-fed streams, which are now rapidly changing owing to global warming.

The melting of the cryosphere is among the most conspicuous consequences of climate change, with impacts on microbial life and related biogeochemistry. However, we are missing a systematic understanding of microbiome structure and function across cryospheric ecosystems. Here, we present a global inventory of the microbiome from snow, ice, permafrost soils, and both coastal and freshwater ecosystems under glacier influence. Combining phylogenetic and taxonomic approaches, we find that these cryospheric ecosystems, despite their particularities, share a microbiome with representatives across the bacterial tree of life and apparent signatures of early and constrained radiation. In addition, we use metagenomic analyses to define the genetic repertoire of cryospheric bacteria. Our work provides a reference resource for future studies on climate change microbiology.

Glacier shrinkage opens new proglacial terrain with pronounced environmental gradients along longitudinal and lateral chronosequences. Despite the environmental harshness of the streams that drain glacier forelands, their benthic biofilms can harbor astonishing biodiversity spanning all domains of life. Here, we studied the spatial dynamics of prokaryotic and eukaryotic photoautotroph diversity within braided glacier-fed streams and tributaries draining lateral terraces predominantly fed by groundwater and snowmelt across three proglacial floodplains in the Swiss Alps. Along the lateral chronosequence, we found that benthic biofilms in tributaries develop higher biomass than those in glacier-fed streams, and that their respective diversity and community composition differed markedly. We also found spatial turnover of bacterial communities in the glacier-fed streams along the longitudinal chronosequence. These patterns along the two chronosequences seem unexpected given the close spatial proximity and connectivity of the various streams, suggesting environmental filtering as an underlying mechanism. Furthermore, our results suggest that photoautotrophic communities shape bacterial communities across the various streams, which is understandable given that algae are the major source of organic matter in proglacial streams. Overall, our findings shed new light on benthic biofilms in proglacial streams now changing at rapid pace owing to climate-induced glacier shrinkage.

The shrinking of glaciers is among the most iconic consequences of climate change. Despite this, the downstream consequences for ecosystem processes and related microbiome structure and function remain poorly understood. Here, using a space‐for‐time substitution approach across 101 glacier‐fed streams (GFSs) from six major regions worldwide, we investigated how glacier shrinkage is likely to impact the organic matter (OM) decomposition rates of benthic biofilms. To do this, we measured the activities of five common extracellular enzymes and estimated decomposition rates by using enzyme allocation equations based on stoichiometry. We found decomposition rates to average 0.0129 (% d−1), and that decreases in glacier influence (estimated by percent glacier catchment coverage, turbidity, and a glacier index) accelerates decomposition rates. To explore mechanisms behind these relationships, we further compared decomposition rates with biofilm and stream water characteristics. We found that chlorophyll‐a, temperature, and stream water N:P together explained 61% of the variability in decomposition. Algal biomass, which is also increasing with glacier shrinkage, showed a particularly strong relationship with decomposition, likely indicating their importance in contributing labile organic compounds to these carbon‐poor habitats. We also found high relative abundances of chytrid fungi in GFS sediments, which putatively parasitize these algae, promoting decomposition through a fungal shunt. Exploring the biofilm microbiome, we then sought to identify bacterial phylogenetic clades significantly associated with decomposition, and found numerous positively (e.g., Saprospiraceae) and negatively (e.g., Nitrospira) related clades. Lastly, using metagenomics, we found evidence of different bacterial classes possessing different proportions of EEA‐encoding genes, potentially informing some of the microbial associations with decomposition rates. Our results, therefore, present new mechanistic insights into OM decomposition in GFSs by demonstrating that an algal‐based “green food web” is likely to increase in importance in the future and will promote important biogeochemical shifts in these streams as glaciers vanish.