Deep biosphere


Metaproteogenomics resolution of a high-CO2 aquifer community reveals a complex cellular adaptation of groundwater Gracilibacteria to a host-dependent lifestyle

Microbiome volume 12, Article number: 194 (2024)


Background

Bacteria of the candidate phyla radiation (CPR), constituting about 25% of the bacterial biodiversity, are characterized by small cell size and patchy genomes without complete key metabolic pathways, suggesting a symbiotic lifestyle. Gracilibacteria (BD1-5), which are part of the CPR branch, possess alternate coded genomes and have not yet been cultivated. The lifestyle of Gracilibacteria, their temporal dynamics, and activity in natural ecosystems, particularly in groundwater, has remained largely unexplored. Here, we aimed to investigate Gracilibacteria activity in situ and to discern their lifestyle based on expressed genes, using the metaproteogenome of Gracilibacteria as a function of time in the cold-water geyser Wallender Born in the Volcanic Eifel region in Germany.

Results

We coupled genome-resolved metagenomics and metaproteomics to investigate a cold-water geyser microbial community enriched in Gracilibacteria across a 12-day time-series. Groundwater was collected and sequentially filtered to fraction CPR and other bacteria. Based on 725 Gbps of metagenomic data, 1129 different ribosomal protein S3 marker genes, and 751 high-quality genomes (123 population genomes after dereplication), we identified dominant bacteria belonging to Gallionellales and Gracilibacteria along with keystone microbes, which were low in genomic abundance but substantially contributing to proteomic abundance. Seven high-quality Gracilibacteria genomes showed typical limitations, such as limited amino acid or nucleotide synthesis, in their central metabolism but no co-occurrence with potential hosts. The genomes of these Gracilibacteria were encoded for a high number of proteins involved in cell to cell interaction, supporting the previously surmised host-dependent lifestyle, e.g., type IV and type II secretion system subunits, transporters, and features related to cell motility, which were also detected on protein level.

Conclusions

We here identified microbial keystone taxa in a high-CO2 aquifer, and revealed microbial dynamics of Gracilibacteria. Although Gracilibacteria in this ecosystem did not appear to target specific organisms in this ecosystem due to lack of co-occurrence despite enrichment on 0.2-µm filter fraction, we provide proteomic evidence for the complex machinery behind the host-dependent lifestyle of groundwater Gracilibacteria.


https://microbiomejournal.biomedcentral.com/articles/10.1186/s40168-024-01889-8



Genetic diversity in terrestrial subsurface ecosystems impacted by geological degassing

Nature Communications volume 13, Article number: 284 (2022)


Abstract

Earth’s mantle releases 38.7 ± 2.9 Tg/yr CO2 along with other reduced and oxidized gases to the atmosphere shaping microbial metabolism at volcanic sites across the globe, yet little is known about its impact on microbial life under non-thermal conditions. Here, we perform comparative metagenomics coupled to geochemical measurements of deep subsurface fluids from a cold-water geyser driven by mantle degassing. Key organisms belonging to uncultivated Candidatus Altiarchaeum show a global biogeographic pattern and site-specific adaptations shaped by gene loss and inter-kingdom horizontal gene transfer. Comparison of the geyser community to 16 other publicly available deep subsurface sites demonstrate a conservation of chemolithoautotrophic metabolism across sites. In silico replication measures suggest a linear relationship of bacterial replication with ecosystems depth with the exception of impacted sites, which show near surface characteristics. Our results suggest that subsurface ecosystems affected by geological degassing are hotspots for microbial life in the deep biosphere.



https://www.nature.com/articles/s41467-021-27783-7



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