A glimpse of the paleome in endolithic microbial communities
Abstract Background The terrestrial subsurface is home to a significant proportion of the Earth’s microbial biomass. Our understanding about terrestrial subsurface microbiomes is almost exclusively derived from groundwater and porous sediments mainly by using 16S rRNA gene surveys. To obtain more in...
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| Format: | Article |
| Language: | English |
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BMC
2023-09-01
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| Series: | Microbiome |
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| Online Access: | https://doi.org/10.1186/s40168-023-01647-2 |
| _version_ | 1827633658157072384 |
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| author | Carl-Eric Wegner Raphaela Stahl Irina Velsko Alex Hübner Zandra Fagernäs Christina Warinner Robert Lehmann Thomas Ritschel Kai U. Totsche Kirsten Küsel |
| author_facet | Carl-Eric Wegner Raphaela Stahl Irina Velsko Alex Hübner Zandra Fagernäs Christina Warinner Robert Lehmann Thomas Ritschel Kai U. Totsche Kirsten Küsel |
| author_sort | Carl-Eric Wegner |
| collection | DOAJ |
| description | Abstract Background The terrestrial subsurface is home to a significant proportion of the Earth’s microbial biomass. Our understanding about terrestrial subsurface microbiomes is almost exclusively derived from groundwater and porous sediments mainly by using 16S rRNA gene surveys. To obtain more insights about biomass of consolidated rocks and the metabolic status of endolithic microbiomes, we investigated interbedded limestone and mudstone from the vadose zone, fractured aquifers, and deep aquitards. Results By adapting methods from microbial archaeology and paleogenomics, we could recover sufficient DNA for downstream metagenomic analysis from seven rock specimens independent of porosity, lithology, and depth. Based on the extracted DNA, we estimated between 2.81 and 4.25 × 105 cells × g−1 rock. Analyzing DNA damage patterns revealed paleome signatures (genetic records of past microbial communities) for three rock specimens, all obtained from the vadose zone. DNA obtained from deep aquitards isolated from surface input was not affected by DNA decay indicating that water saturation and not flow is controlling subsurface microbial survival. Decoding the taxonomy and functional potential of paleome communities revealed increased abundances for sequences affiliated with chemolithoautotrophs and taxa such as Cand. Rokubacteria. We also found a broader metabolic potential in terms of aromatic hydrocarbon breakdown, suggesting a preferred utilization of sedimentary organic matter in the past. Conclusions Our study suggests that limestones function as archives for genetic records of past microbial communities including those sensitive to environmental stress at modern times, due to their specific conditions facilitating long-term DNA preservation. Video Abstract |
| first_indexed | 2024-03-09T15:02:36Z |
| format | Article |
| id | doaj.art-079eadc9ac3743cf96cfb3264dd46193 |
| institution | Directory Open Access Journal |
| issn | 2049-2618 |
| language | English |
| last_indexed | 2024-03-09T15:02:36Z |
| publishDate | 2023-09-01 |
| publisher | BMC |
| record_format | Article |
| series | Microbiome |
| spelling | doaj.art-079eadc9ac3743cf96cfb3264dd461932023-11-26T13:47:50ZengBMCMicrobiome2049-26182023-09-0111111810.1186/s40168-023-01647-2A glimpse of the paleome in endolithic microbial communitiesCarl-Eric Wegner0Raphaela Stahl1Irina Velsko2Alex Hübner3Zandra Fagernäs4Christina Warinner5Robert Lehmann6Thomas Ritschel7Kai U. Totsche8Kirsten Küsel9Aquatic Geomicrobiology, Institute of Biodiversity, Friedrich Schiller University JenaDepartment of Archaeogenetics, Max Planck Institute for Evolutionary AnthropologyDepartment of Archaeogenetics, Max Planck Institute for Evolutionary AnthropologyDepartment of Archaeogenetics, Max Planck Institute for Evolutionary AnthropologyDepartment of Archaeogenetics, Max Planck Institute for Evolutionary AnthropologyDepartment of Archaeogenetics, Max Planck Institute for Evolutionary AnthropologyHydrogeology, Institute of Geosciences, Friedrich Schiller University JenaHydrogeology, Institute of Geosciences, Friedrich Schiller University JenaCluster of Excellence Balance of the Microverse, Friedrich Schiller University JenaAquatic Geomicrobiology, Institute of Biodiversity, Friedrich Schiller University JenaAbstract Background The terrestrial subsurface is home to a significant proportion of the Earth’s microbial biomass. Our understanding about terrestrial subsurface microbiomes is almost exclusively derived from groundwater and porous sediments mainly by using 16S rRNA gene surveys. To obtain more insights about biomass of consolidated rocks and the metabolic status of endolithic microbiomes, we investigated interbedded limestone and mudstone from the vadose zone, fractured aquifers, and deep aquitards. Results By adapting methods from microbial archaeology and paleogenomics, we could recover sufficient DNA for downstream metagenomic analysis from seven rock specimens independent of porosity, lithology, and depth. Based on the extracted DNA, we estimated between 2.81 and 4.25 × 105 cells × g−1 rock. Analyzing DNA damage patterns revealed paleome signatures (genetic records of past microbial communities) for three rock specimens, all obtained from the vadose zone. DNA obtained from deep aquitards isolated from surface input was not affected by DNA decay indicating that water saturation and not flow is controlling subsurface microbial survival. Decoding the taxonomy and functional potential of paleome communities revealed increased abundances for sequences affiliated with chemolithoautotrophs and taxa such as Cand. Rokubacteria. We also found a broader metabolic potential in terms of aromatic hydrocarbon breakdown, suggesting a preferred utilization of sedimentary organic matter in the past. Conclusions Our study suggests that limestones function as archives for genetic records of past microbial communities including those sensitive to environmental stress at modern times, due to their specific conditions facilitating long-term DNA preservation. Video Abstracthttps://doi.org/10.1186/s40168-023-01647-2SubsurfaceMetagenomicsEndolithicDNA damageChemolithotrophy |
| spellingShingle | Carl-Eric Wegner Raphaela Stahl Irina Velsko Alex Hübner Zandra Fagernäs Christina Warinner Robert Lehmann Thomas Ritschel Kai U. Totsche Kirsten Küsel A glimpse of the paleome in endolithic microbial communities Microbiome Subsurface Metagenomics Endolithic DNA damage Chemolithotrophy |
| title | A glimpse of the paleome in endolithic microbial communities |
| title_full | A glimpse of the paleome in endolithic microbial communities |
| title_fullStr | A glimpse of the paleome in endolithic microbial communities |
| title_full_unstemmed | A glimpse of the paleome in endolithic microbial communities |
| title_short | A glimpse of the paleome in endolithic microbial communities |
| title_sort | glimpse of the paleome in endolithic microbial communities |
| topic | Subsurface Metagenomics Endolithic DNA damage Chemolithotrophy |
| url | https://doi.org/10.1186/s40168-023-01647-2 |
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