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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. In glacier-fed streams, ecological windows of opportunity allow complex microbial biofilms to develop and transiently form the basis of the food web. Using metagenomics, this study reveals the metabolic strategies and key genomic underpinnings of adaptive traits that enable these biofilms to exploit environmental opportunities.

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.

The rapid melting of mountain glaciers and the vanishing of their streams is emblematic of climate change 1 , 2 . Glacier-fed streams (GFSs) are cold, oligotrophic and unstable ecosystems in which life is dominated by microbial biofilms 2 , 3 . However, current knowledge on the GFS microbiome is scarce 4 , 5 , precluding an understanding of its response to glacier shrinkage. Here, by leveraging metabarcoding and metagenomics, we provide a comprehensive survey of bacteria in the benthic microbiome across 152 GFSs draining the Earth’s major mountain ranges. We find that the GFS bacterial microbiome is taxonomically and functionally distinct from other cryospheric microbiomes. GFS bacteria are diverse, with more than half being specific to a given mountain range, some unique to single GFSs and a few cosmopolitan and abundant. We show how geographic isolation and environmental selection shape their biogeography, which is characterized by distinct compositional patterns between mountain ranges and hemispheres. Phylogenetic analyses furthermore uncovered microdiverse clades resulting from environmental selection, probably promoting functional resilience and contributing to GFS bacterial biodiversity and biogeography. Climate-induced glacier shrinkage puts this unique microbiome at risk. Our study provides a global reference for future climate-change microbiology studies on the vanishing GFS ecosystem. Leveraging metabarcoding and metagenomics, a survey of bacteria in the benthic microbiome across 152 glacier-fed streams (GFSs) provides a global reference for future climate-change microbiology studies on the vanishing GFS ecosystem.

Most cryospheric ecosystems are energy limited. How their energetics will respond to climate change remains largely unknown. This is particularly true for glacier-fed streams, which interface with the cryosphere and initiate some of Earth’s largest river systems. Here, by studying resource stoichiometry and microbial energetics in 154 glacier-fed streams sampled by the Vanishing Glaciers project across Earth’s major mountain ranges, we show that these ecosystems and their benthic microbiome are overall carbon and phosphorus limited. Threshold elemental ratios and low carbon use efficiencies (median: 0.15) modelled from extracellular enzymatic activities corroborate resource limitation in agreement with maintenance metabolism of benthic microorganisms. Space-for-time substitution analyses suggest that glacier shrinkage will stimulate benthic primary production in glacier-fed streams, thereby relieving microbial metabolism from carbon limitation. Concomitantly, we find that increasing streamwater temperature will probably stimulate microbial growth (temperature sensitivity: 0.62 eV). Consequently, elevated microbial demands for phosphorus, but diminishing inputs from subglacial sources, may intensify phosphorus limitation as glaciers shrink. Our study thus unveils a ‘green transition’ towards autotrophy in the world’s glacier-fed streams, entailing shifts in the energetics of their microorganisms. Glacier shrinkage intensifies phosphorus limitation but alleviates carbon limitation in glacier-fed streams, according to analyses of resource stoichiometry and microbial metabolism in glacier-fed streams from mountain regions.

The shrinkage of glaciers and the vanishing of glacier-fed streams (GFSs) are emblematic of climate change. However, forecasts of how GFS microbiome structure and function will change under projected climate change scenarios are lacking. Combining 2,333 prokaryotic metagenome-assembled genomes with climatic, glaciological, and environmental data collected by the Vanishing Glaciers project from 164 GFSs draining Earth’s major mountain ranges, we here predict the future of the GFS microbiome until the end of the century under various climate change scenarios. Our model framework is rooted in a space-for-time substitution design and leverages statistical learning approaches. We predict that declining environmental selection promotes primary production in GFSs, stimulating both bacterial biomass and biodiversity. Concomitantly, predictions suggest that the phylogenetic structure of the GFS microbiome will change and entire bacterial clades are at risk. Furthermore, genomic projections reveal that microbiome functions will shift, with intensified solar energy acquisition pathways, heterotrophy and algal-bacterial interactions. Altogether, we project a ‘greener’ future of the world’s GFSs accompanied by a loss of clades that have adapted to environmental harshness, with consequences for ecosystem functioning. Little is known about how climate change impacts glacier-fed streams (GFSs) microbiomes. Here, using a modelling framework based on global GFS metagenomic, climatic and environmental data the authors predict future increases in GFS bacterial biomass and diversity, but potential loss of clades adapted to extreme conditions.

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.

Glacier-fed streams (GFS) feature among Earth’s most extreme aquatic ecosystems marked by pronounced oligotrophy and environmental fluctuations. Microorganisms mainly organize in biofilms within them, but how they cope with such conditions is unknown. Here, leveraging 156 metagenomes from the Vanishing Glaciers project obtained from sediment samples in GFS from 9 mountains ranges, we report thousands of metagenome-assembled genomes (MAGs) encompassing prokaryotes, algae, fungi and viruses, that shed light on biotic interactions within glacier-fed stream biofilms. A total of 2,855 bacterial MAGs were characterized by diverse strategies to exploit inorganic and organic energy sources, in part via functional redundancy and mixotrophy. We show that biofilms probably become more complex and switch from chemoautotrophy to heterotrophy as algal biomass increases in GFS owing to glacier shrinkage. Our MAG compendium sheds light on the success of microbial life in GFS and provides a resource for future research on a microbiome potentially impacted by climate change. Thousands of metagenome-assembled genomes from the Vanishing Glaciers project showcase the interactions between prokaryotes, algae, fungi and viruses in glacier-fed stream environments.

Glacier-fed streams are characterized by low temperatures, high turbidity, and high flow. They host a unique microbiome within biofilms, which form the foundation of the food web and contribute significantly to biogeochemical cycles. Our investigation into secondary metabolites, which likely play an important role in these complex ecosystems, found a unique genetic potential distinct from other aquatic environments. We found the potential to synthesize several secondary metabolites, which may confer ecological advantages, such as UV protection and quorum sensing. This biosynthetic diversity was positively associated with the abundance and complexity of the microbial community, as well as concentrations of chlorophyll a . In the face of climate change, our study offers new insights into a vanishing ecosystem.

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

Background: Antimicrobial resistance (AMR) is a universal phenomenon whose origins lay in natural ecological interactions such as competition within niches, within and between micro- to higher-order organisms. However, the ecological and evolutionary processes shaping AMR need to be better understood in view of better antimicrobial stewardship. Resolving antibiotic biosynthetic pathways, including biosynthetic gene clusters (BGCs), and corresponding antimicrobial resistance genes (ARGs) may therefore help in understanding the inherent mechanisms. However, to study these phenomena, it is crucial to examine the origins of AMR in pristine environments with limited anthropogenic influences. In this context, epilithic biofilms residing in glacier-fed streams (GFSs) are an excellent model system to study diverse, intra- and inter-domain, ecological crosstalk. Results: We assessed the resistomes of epilithic biofilms from GFSs across the Southern Alps (New Zealand) and the Caucasus (Russia) and observed that both bacteria and eukaryotes encoded twenty-nine distinct AMR categories. Of these, beta-lactam, aminoglycoside, and multidrug resistance were both abundant and taxonomically distributed in most of the bacterial and eukaryotic phyla. AMR-encoding phyla included Bacteroidota and Proteobacteria among the bacteria, alongside Ochrophyta (algae) among the eukaryotes. Additionally, BGCs involved in the production of antibacterial compounds were identified across all phyla in the epilithic biofilms. Furthermore, we found that several bacterial genera (Flavobacterium, Polaromonas, etc.) including representatives of the superphylum Patescibacteria encode both ARGs and BGCs within close proximity of each other, thereby demonstrating their capacity to simultaneously influence and compete within the microbial community. Conclusions: Our findings highlight the presence and abundance of AMR in epilithic biofilms within GFSs. Additionally, we identify their role in the complex intra- and inter-domain competition and the underlying mechanisms influencing microbial survival in GFS epilithic biofilms. We demonstrate that eukaryotes may serve as AMR reservoirs owing to their potential for encoding ARGs. We also find that the taxonomic affiliation of the AMR and the BGCs are congruent. Importantly, our findings allow for understanding how naturally occurring BGCs and AMR contribute to the epilithic biofilms mode of life in GFSs. Importantly, these observations may be generalizable and potentially extended to other environments which may be more or less impacted by human activity. Competing Interest Statement The authors have declared no competing interest.