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.

Spatial patterns of benthic biofilm diversity among streams draining proglacial floodplains

“…How habitat heterogeneity along chronosequences affects biodiversity has been relatively well studied for aquatic invertebrates ( Milner and Petts, 1994 ; Milner et al, 2010 ; Cauvy-Fraunié and Dangles, 2019 ; Muhlfeld et al, 2020 ); however, less so for microorganisms. The bulk of our current understanding on the microbial life in proglacial streams remains limited to the main channels directly fed by glacier meltwaters (e.g., Battin et al, 2004 ; Wilhelm et al, 2013 ; Ren et al, 2017 ; Roncoroni et al, 2019 ; Busi et al, 2021 ). Some of these earlier studies have presented tentative evidence toward longitudinal shifts in community structure and function of benthic biofilms in glacier-fed streams ( Battin et al, 2004 ; Ren et al, 2017 ).…”

Multi-omics analysis of mouse fecal microbiome reveals supplier-dependent functional differences and novel metagenome-assembled genomes

“…As newly recognized epibionts within the candidate phylum radiation (CPR), the Saccharimonadaceae were of particular interest since their reports in laboratory mouse strains are limited. MAGs identified as Saccharimonadaceae have been found in diverse environmental samples including deep sea hydrothermal vents, glacial-fed stream biofilms, 28 and petrochemical plant sludge. 29 Regarding host-associated samples, Saccharimonadaceae are most commonly identified in human oral cavity samples, 30,31 although a handful of rumen 32 and fecal 33 samples have also yielded MAGs.…”

Glacier-Fed Stream Biofilms Harbor Diverse Resistomes and Biosynthetic Gene Clusters

“…Eight GFSs were sampled in early to mid-2019 from the New Zealand Southern Alps and the Russian Caucasus, respectively, for a total of 21 epilithic biofilms (Table S1). The biofilm samples were collected from each stream reach, depending on the stream geomorphology, i.e., the presence of boulders, as described previously by Busi et al ( 18 ). One to three biofilm samples were collected per reach (Table S1), taken using sterilized metal spatulas to scrape rocks, followed by their immediate transfer to cryovials.…”

“…IMP’s workflow includes preprocessing, contig assembly, genome reconstruction (metagenome-assembled genomes, i.e., MAGs), and taxonomic and additional functional analysis of genes based on custom databases in a reproducible manner ( 61 ). Eukaryotic binning was performed in addition to the processing with the IMP workflow as described in Busi et al ( 18 ). Briefly, eukaryotic MAGs were binned using CONCOCT ( 62 ), using contigs that were identified as eukaryotic, including those not mapping to bacteria or viruses in the maxikraken2 database available at https://lomanlab.github.io/mockcommunity/mc_databases.html .…”

“…We have recently reported the genomic and metabolic adaptations of epilithic biofilms to environmental conditions in glacier-fed streams (GFSs) ( 18 ). For example, given the short flow season during glacial melt in summer, the incentive to reproduce quickly while conditions are favorable, is high.…”