Abstract
Ice caves constitute the newly investigated frozen and secluded model habitats for evaluating the resilience of ice-entrapped microbiomes in response to climate changes. This survey identified the total and active prokaryotic and eukaryotic communities from millennium-old ice accumulated in Scarisoara cave (Romania) using Illumina shotgun sequencing of the ribosomal RNA (rRNA) and messenger RNA (mRNA)-based functional analysis of the metatranscriptome. Also, the response of active microbiome to heat shock treatment mimicking the environmental shift during ice melting was evaluated at both the taxonomic and metabolic levels. The putatively active microbial community was dominated by bacterial taxa belonging to Proteobacteria and Bacteroidetes, which are highly resilient to thermal variations, while the scarcely present archaea belonging to Methanomicrobia was majorly affected by heat shock. Among eukaryotes, the fungal rRNA community was shared between the resilient Chytridiomycota and Blastocladiomycota, and the more sensitive Ascomycota and Basidiomycota taxa. A complex microeukaryotic community highly represented by Tardigrada and Rotifera (Metazoa), Ciliophora and Cercozoa (Protozoa), and Chlorophyta (Plantae) was evidenced for the first time in this habitat. This community showed a quick reaction to heat shock, followed by a partial recovery after prolonged incubation at 4°C due to possible predation processes on the prokaryotic cluster. Analysis of mRNA differential gene expression revealed the presence of an active microbiome in the perennial ice from the Scarisoara cave and associated molecular mechanisms for coping with temperature variations by the upregulation of genes involved in enzyme recovery, energy storage, carbon and nitrogen regulation, and cell motility. This first report on the active microbiome embedded in perennial ice from caves and its response to temperature stress provided a glimpse into the impact of glaciers melting and the resilience mechanisms in this habitat, contributing to the knowledge on the functional role of active microbes in frozen environments and their response to climatic changes.
Highlights
Ice can be considered as a storage matrix for microorganisms, representing a source of genomic diversity and a reservoir of new microbial species (Priscu et al, 1998; Miteva et al, 2009; Anesio and Laybourn-Parry, 2012; Anesio et al, 2017; Zhong et al, 2021)
This study provides the first evidence of an active microbiome and putatively active microeukaryotic taxa in perennial ice from caves, in addition to initial data on the thermal treatment response of the total and active ice-entrapped microbiomes using Illumina shotgun sequencing of ribosomal RNA (rRNA) and messenger RNA (mRNA) shift analysis
Temperature changes are known to disturb the microbial homeostasis alongside an altered taxon distribution, while little is known about the transcriptomic response to thermal stress
Summary
Ice can be considered as a storage matrix for microorganisms, representing a source of genomic diversity and a reservoir of new microbial species (Priscu et al, 1998; Miteva et al, 2009; Anesio and Laybourn-Parry, 2012; Anesio et al, 2017; Zhong et al, 2021). The culturing method provided a step forward in microbial screening, scientists became aware of the limitations of culture-dependent techniques due to microbial uncultivability in describing the diversity of microbiomes (Hug et al, 2016). To overcome this problem, studies were conducted using denaturing gradient gel electrophoresis (DGGE) to unravel fungal diversity (Brad et al, 2018), while a more advanced sequence identification was achieved with the application of molecular techniques, including 454 pyrosequencing of the prokaryotic community (Itcus et al, 2018) and Illumina sequencing of the fungal communities along the 1,500-year-old ice based on ITS2 Illumina sequencing (Mondini et al, 2018)
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