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Molecular evidence for an active endogenous microbiome beneath glacial ice.

ABSTRACT: Geologic, chemical and isotopic evidence indicate that Earth has experienced numerous intervals of widespread glaciation throughout its history, with roughly 11% of present day Earth's land surface covered in ice. Despite the pervasive nature of glacial ice both today and in Earth's past and the potential contribution of these systems to global biogeochemical cycles, the composition and phylogenetic structure of an active microbial community in subglacial systems has yet to be described. Here, using RNA-based approaches, we demonstrate the presence of active and endogenous archaeal, bacterial and eukaryal assemblages in cold (0-1?°C) subglacial sediments sampled from Robertson Glacier, Alberta, Canada. Patterns in the phylogenetic structure and composition of subglacial sediment small subunit (SSU) ribosomal RNA (rRNA) assemblages indicate greater diversity and evenness than in glacial surface environments, possibly due to facilitative or competitive interactions among populations in the subglacial environment. The combination of phylogenetically more even and more diverse assemblages in the subglacial environment suggests minimal niche overlap and optimization to capture a wider spectrum of the limited nutrients and chemical energy made available from weathering of bedrock minerals. The prevalence of SSU rRNA affiliated with lithoautotrophic bacteria, autotrophic methane producing archaea and heterotrophic eukarya in the subglacial environment is consistent with this hypothesis and suggests an active contribution to the global carbon cycle. Collectively, our findings demonstrate that subglacial environments harbor endogenous active ecosystems that have the potential to impact global biogeochemical cycles over extended periods of time.

SUBMITTER: Hamilton TL

PROVIDER: S-EPMC3695297 | biostudies-literature | 2013 Jul

REPOSITORIES: biostudies-literature

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Molecular evidence for an active endogenous microbiome beneath glacial ice.

Hamilton Trinity L TL Peters John W JW Skidmore Mark L ML Boyd Eric S ES

The ISME journal 20130314 7

Geologic, chemical and isotopic evidence indicate that Earth has experienced numerous intervals of widespread glaciation throughout its history, with roughly 11% of present day Earth's land surface covered in ice. Despite the pervasive nature of glacial ice both today and in Earth's past and the potential contribution of these systems to global biogeochemical cycles, the composition and phylogenetic structure of an active microbial community in subglacial systems has yet to be described. Here, u ...[more]

PMID: 23486249

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Project description:Our understanding of the icy-habitat microbiome is likely limited by a lack of reliable data on microorganisms inhabiting underground ice that has accumulated inside caves. To characterize how environmental variation impacts cave ice microbial community structure, we determined the composition of total and potentially active bacterial communities along a 13,000-year-old ice core from Scarisoara cave (Romania) through 16S rRNA gene Illumina sequencing. An average of 2,546 prokaryotic gDNA operational taxonomic units (OTUs) and 585 cDNA OTUs were identified across the perennial cave ice block and analyzed in relation to the geochemical composition of ice layers. The total microbial community and the putative active fraction displayed dissimilar taxa profiles. The ice-contained microbiome was dominated by Actinobacteria with a variable representation of Proteobacteria, while the putative active microbial community was equally shared between Proteobacteria and Firmicutes. Accordingly, a major presence of Cryobacterium, Lysinomonas, Pedobacter, and Aeromicrobium phylotypes homologous to psychrotrophic and psychrophilic bacteria from various cold environments were noted in the total community, while the prevalent putative active bacteria belonged to Clostridium, Pseudomonas, Janthinobacterium, Stenotrophomonas, and Massilia genera. Variation in the microbial cell density of ice strata with the dissolved organic carbon (DOC) content and the strong correlation of DOC and silicon concentrations revealed a major impact of depositional processes on microbial abundance throughout the ice block. Post-depositional processes appeared to occur mostly during the 4,000-7,000 years BP interval. A major bacterial composition shift was observed in 4,500-5,000-year-old ice, leading to a high representation of Beta- and Deltaproteobacteria in the potentially active community in response to the increased concentrations of DOC and major chemical elements. Estimated metabolic rates suggested the presence of a viable microbial community within the cave ice block, characterized by a maintenance metabolism in most strata and growth capacity in those ice deposits with high microbial abundance and DOC content. This first survey of microbial distribution in perennial cave ice formed since the Last Glacial period revealed a complex potentially active community, highlighting major shifts in community composition associated with geochemical changes that took place during climatic events that occurred about 5,000 years ago, with putative formation of photosynthetic biofilms.

Project description: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.

Dataset Information

Molecular evidence for an active endogenous microbiome beneath glacial ice.

Publications

Molecular evidence for an active endogenous microbiome beneath glacial ice.

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