Dataset Information

Genomic and metabolic adaptations of biofilms to ecological windows of opportunity in glacier-fed streams.

ABSTRACT: 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.

SUBMITTER: Busi SB

PROVIDER: S-EPMC9021309 | biostudies-literature | 2022 Apr

REPOSITORIES: biostudies-literature

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Genomic and metabolic adaptations of biofilms to ecological windows of opportunity in glacier-fed streams.

Busi Susheel Bhanu SB Bourquin Massimo M Fodelianakis Stilianos S Michoud Grégoire G Kohler Tyler J TJ Peter Hannes H Pramateftaki Paraskevi P Styllas Michail M Tolosano Matteo M De Staercke Vincent V Schön Martina M de Nies Laura L Marasco Ramona R Daffonchio Daniele D Ezzat Leïla L Wilmes Paul P Battin Tom J TJ

Nature communications 20220420 1

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 acquisiti ...[more]

PMID: 35444202

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Project description:Glacier-fed streams are permanently cold, ultra-oligotrophic, and physically unstable environments, yet microbial life thrives in benthic biofilm communities. Within biofilms, microorganisms rely on secondary metabolites for communication and competition. However, the diversity and genetic potential of secondary metabolites in glacier-fed stream biofilms remain poorly understood. In this study, we present the first large-scale exploration of biosynthetic gene clusters (BGCs) from benthic glacier-fed stream biofilms sampled by the Vanishing Glaciers project from the world's major mountain ranges. We found a remarkable diversity of BGCs, with more than 8,000 of them identified within 2,868 prokaryotic metagenome-assembled genomes, some of them potentially conferring ecological advantages, such as UV protection and quorum sensing. The BGCs were distinct from those sourced from other aquatic microbiomes, with over 40% of them being novel. The glacier-fed stream BGCs exhibited the highest similarity to BGCs from glacier microbiomes. BGC composition displayed geographic patterns and correlated with prokaryotic alpha diversity. We also found that BGC diversity was positively associated with benthic chlorophyll a and prokaryotic diversity, indicative of more biotic interactions in more extensive biofilms. Our study provides new insights into a hitherto poorly explored microbial ecosystem, which is now changing at a rapid pace as glaciers are shrinking due to climate change.ImportanceGlacier-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.

Project description:Bacterial and fungal communities in biofilms are important components in driving biogeochemical processes in stream ecosystems. Previous studies have well documented the patterns of bacterial alpha diversity in stream biofilms in glacier-fed streams, where, however, beta diversity of the microbial communities has received much less attention especially considering both bacterial and fungal communities. A focus on beta diversity can provide insights into the mechanisms driving community changes associated to large environmental fluctuations and disturbances, such as in glacier-fed streams. Moreover, modularity of co-occurrence networks can reveal more ecological and evolutionary properties of microbial communities beyond taxonomic groups. Here, integrating beta diversity and co-occurrence approach, we explored the network topology and modularity of the bacterial and fungal communities with consideration of environmental variation in glacier-fed streams in Central Asia. Combining results from hydrological modeling and normalized difference of vegetation index, this study highlighted that hydrological variables and vegetation status are major variables determining the environmental heterogeneity of glacier-fed streams. Bacterial communities formed a more complex and connected network, while the fungal communities formed a more clustered network. Moreover, the strong interrelations among the taxonomic dissimilarities of bacterial community (BC) and modules suggest they had common processes in driving diversity and taxonomic compositions across the heterogeneous environment. In contrast, fungal community (FC) and modules generally showed distinct driving processes to each other. Moreover, bacterial and fungal communities also had different driving processes. Furthermore, the variation of BC and modules were strongly correlated with hydrological properties and vegetation status but not with nutrients, while FC and modules (except one module) were not associated with environmental variation. Our results suggest that bacterial and fungal communities had distinct mechanisms in structuring microbial networks, and environmental variation had strong influences on bacterial communities but not on fungal communities. The fungal communities have unique assembly mechanisms and physiological properties which might lead to their insensitive responses to environmental variations compared to bacterial communities. Overall, beyond alpha diversity in previous studies, these results add our knowledge that bacterial and fungal communities have contrasting assembly mechanisms and respond differently to environmental variation in glacier-fed streams.

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Project description:Glacier-fed streams (GFSs) exhibit near-freezing temperatures, variable flows, and often high turbidities. Currently, the rapid shrinkage of mountain glaciers is altering the delivery of meltwater, solutes, and particulate matter to GFSs, with unknown consequences for their ecology. Benthic biofilms dominate microbial life in GFSs, and play a major role in their biogeochemical cycling. Mineralization is likely an important process for microbes to meet elemental budgets in these systems due to commonly oligotrophic conditions, and extracellular enzymes retained within the biofilm enable the degradation of organic matter and acquisition of carbon (C), nitrogen (N), and phosphorus (P). The measurement and comparison of these extracellular enzyme activities (EEA) can in turn provide insight into microbial elemental acquisition effort relative to environmental availability. To better understand how benthic biofilm communities meet resource demands, and how this might shift as glaciers vanish under climate change, we investigated biofilm EEA in 20 GFSs varying in glacier influence from New Zealand's Southern Alps. Using turbidity and distance to the glacier snout normalized for glacier size as proxies for glacier influence, we found that bacterial abundance (BA), chlorophyll a (Chl a), extracellular polymeric substances (EPS), and total EEA per gram of sediment increased with decreasing glacier influence. Yet, when normalized by BA, EPS decreased with decreasing glacier influence, Chl a still increased, and there was no relationship with total EEA. Based on EEA ratios, we found that the majority of GFS microbial communities were N-limited, with a few streams of different underlying bedrock geology exhibiting P-limitation. Cell-specific C-acquiring EEA was positively related to the ratio of Chl a to BA, presumably reflecting the utilization of algal exudates. Meanwhile, cell-specific N-acquiring EEA were positively correlated with the concentration of dissolved inorganic nitrogen (DIN), and both N- and P-acquiring EEA increased with greater cell-specific EPS. Overall, our results reveal greater glacier influence to be negatively related to GFS biofilm biomass parameters, and generally associated with greater microbial N demand. These results help to illuminate the ecology of GFS biofilms, along with their biogeochemical response to a shifting habitat template with ongoing climate change.

Dataset Information

Genomic and metabolic adaptations of biofilms to ecological windows of opportunity in glacier-fed streams.

Publications

Genomic and metabolic adaptations of biofilms to ecological windows of opportunity in glacier-fed streams.

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