Metatranscriptomes Reveal That All Three Domains of Life Are Active but Are Dominated by Bacteria in the Fennoscandian Crystalline Granitic Continental Deep Biosphere

ABSTRACT The continental subsurface is suggested to contain a significant part of the earth’s total biomass. However, due to the difficulty of sampling, the deep subsurface is still one of the least understood ecosystems. Therefore, microorganisms inhabiting this environment might profoundly influen...

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Autores principales: Margarita Lopez-Fernandez, Domenico Simone, Xiaofen Wu, Lucile Soler, Emelie Nilsson, Karin Holmfeldt, Henrik Lantz, Stefan Bertilsson, Mark Dopson
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Publicado: American Society for Microbiology 2018
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spelling oai:doaj.org-article:c65b0a4b481c4614b34088a88b3487fc2021-11-15T15:52:20ZMetatranscriptomes Reveal That All Three Domains of Life Are Active but Are Dominated by Bacteria in the Fennoscandian Crystalline Granitic Continental Deep Biosphere10.1128/mBio.01792-182150-7511https://doaj.org/article/c65b0a4b481c4614b34088a88b3487fc2018-12-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01792-18https://doaj.org/toc/2150-7511ABSTRACT The continental subsurface is suggested to contain a significant part of the earth’s total biomass. However, due to the difficulty of sampling, the deep subsurface is still one of the least understood ecosystems. Therefore, microorganisms inhabiting this environment might profoundly influence the global nutrient and energy cycles. In this study, in situ fixed RNA transcripts from two deep continental groundwaters from the Äspö Hard Rock Laboratory (a Baltic Sea-influenced water with a residence time of <20 years, defined as “modern marine,” and an “old saline” groundwater with a residence time of thousands of years) were subjected to metatranscriptome sequencing. Although small subunit (SSU) rRNA gene and mRNA transcripts aligned to all three domains of life, supporting activity within these community subsets, the data also suggested that the groundwaters were dominated by bacteria. Many of the SSU rRNA transcripts grouped within newly described candidate phyla or could not be mapped to known branches on the tree of life, suggesting that a large portion of the active biota in the deep biosphere remains unexplored. Despite the extremely oligotrophic conditions, mRNA transcripts revealed a diverse range of metabolic strategies that were carried out by multiple taxa in the modern marine water that is fed by organic carbon from the surface. In contrast, the carbon dioxide- and hydrogen-fed old saline water with a residence time of thousands of years predominantly showed the potential to carry out translation. This suggested these cells were active, but waiting until an energy source episodically becomes available. IMPORTANCE A newly designed sampling apparatus was used to fix RNA under in situ conditions in the deep continental biosphere and benchmarks a strategy for deep biosphere metatranscriptomic sequencing. This apparatus enabled the identification of active community members and the processes they carry out in this extremely oligotrophic environment. This work presents for the first time evidence of eukaryotic, archaeal, and bacterial activity in two deep subsurface crystalline rock groundwaters from the Äspö Hard Rock Laboratory with different depths and geochemical characteristics. The findings highlight differences between organic carbon-fed shallow communities and carbon dioxide- and hydrogen-fed old saline waters. In addition, the data reveal a large portion of uncharacterized microorganisms, as well as the important role of candidate phyla in the deep biosphere, but also the disparity in microbial diversity when using standard microbial 16S rRNA gene amplification versus the large unknown portion of the community identified with unbiased metatranscriptomes.Margarita Lopez-FernandezDomenico SimoneXiaofen WuLucile SolerEmelie NilssonKarin HolmfeldtHenrik LantzStefan BertilssonMark DopsonAmerican Society for MicrobiologyarticlemetatranscriptomesmRNArRNAdeep biospheregroundwatersmetatranscriptomesMicrobiologyQR1-502ENmBio, Vol 9, Iss 6 (2018)
institution DOAJ
collection DOAJ
language EN
topic metatranscriptomes
mRNA
rRNA
deep biosphere
groundwaters
metatranscriptomes
Microbiology
QR1-502
spellingShingle metatranscriptomes
mRNA
rRNA
deep biosphere
groundwaters
metatranscriptomes
Microbiology
QR1-502
Margarita Lopez-Fernandez
Domenico Simone
Xiaofen Wu
Lucile Soler
Emelie Nilsson
Karin Holmfeldt
Henrik Lantz
Stefan Bertilsson
Mark Dopson
Metatranscriptomes Reveal That All Three Domains of Life Are Active but Are Dominated by Bacteria in the Fennoscandian Crystalline Granitic Continental Deep Biosphere
description ABSTRACT The continental subsurface is suggested to contain a significant part of the earth’s total biomass. However, due to the difficulty of sampling, the deep subsurface is still one of the least understood ecosystems. Therefore, microorganisms inhabiting this environment might profoundly influence the global nutrient and energy cycles. In this study, in situ fixed RNA transcripts from two deep continental groundwaters from the Äspö Hard Rock Laboratory (a Baltic Sea-influenced water with a residence time of <20 years, defined as “modern marine,” and an “old saline” groundwater with a residence time of thousands of years) were subjected to metatranscriptome sequencing. Although small subunit (SSU) rRNA gene and mRNA transcripts aligned to all three domains of life, supporting activity within these community subsets, the data also suggested that the groundwaters were dominated by bacteria. Many of the SSU rRNA transcripts grouped within newly described candidate phyla or could not be mapped to known branches on the tree of life, suggesting that a large portion of the active biota in the deep biosphere remains unexplored. Despite the extremely oligotrophic conditions, mRNA transcripts revealed a diverse range of metabolic strategies that were carried out by multiple taxa in the modern marine water that is fed by organic carbon from the surface. In contrast, the carbon dioxide- and hydrogen-fed old saline water with a residence time of thousands of years predominantly showed the potential to carry out translation. This suggested these cells were active, but waiting until an energy source episodically becomes available. IMPORTANCE A newly designed sampling apparatus was used to fix RNA under in situ conditions in the deep continental biosphere and benchmarks a strategy for deep biosphere metatranscriptomic sequencing. This apparatus enabled the identification of active community members and the processes they carry out in this extremely oligotrophic environment. This work presents for the first time evidence of eukaryotic, archaeal, and bacterial activity in two deep subsurface crystalline rock groundwaters from the Äspö Hard Rock Laboratory with different depths and geochemical characteristics. The findings highlight differences between organic carbon-fed shallow communities and carbon dioxide- and hydrogen-fed old saline waters. In addition, the data reveal a large portion of uncharacterized microorganisms, as well as the important role of candidate phyla in the deep biosphere, but also the disparity in microbial diversity when using standard microbial 16S rRNA gene amplification versus the large unknown portion of the community identified with unbiased metatranscriptomes.
format article
author Margarita Lopez-Fernandez
Domenico Simone
Xiaofen Wu
Lucile Soler
Emelie Nilsson
Karin Holmfeldt
Henrik Lantz
Stefan Bertilsson
Mark Dopson
author_facet Margarita Lopez-Fernandez
Domenico Simone
Xiaofen Wu
Lucile Soler
Emelie Nilsson
Karin Holmfeldt
Henrik Lantz
Stefan Bertilsson
Mark Dopson
author_sort Margarita Lopez-Fernandez
title Metatranscriptomes Reveal That All Three Domains of Life Are Active but Are Dominated by Bacteria in the Fennoscandian Crystalline Granitic Continental Deep Biosphere
title_short Metatranscriptomes Reveal That All Three Domains of Life Are Active but Are Dominated by Bacteria in the Fennoscandian Crystalline Granitic Continental Deep Biosphere
title_full Metatranscriptomes Reveal That All Three Domains of Life Are Active but Are Dominated by Bacteria in the Fennoscandian Crystalline Granitic Continental Deep Biosphere
title_fullStr Metatranscriptomes Reveal That All Three Domains of Life Are Active but Are Dominated by Bacteria in the Fennoscandian Crystalline Granitic Continental Deep Biosphere
title_full_unstemmed Metatranscriptomes Reveal That All Three Domains of Life Are Active but Are Dominated by Bacteria in the Fennoscandian Crystalline Granitic Continental Deep Biosphere
title_sort metatranscriptomes reveal that all three domains of life are active but are dominated by bacteria in the fennoscandian crystalline granitic continental deep biosphere
publisher American Society for Microbiology
publishDate 2018
url https://doaj.org/article/c65b0a4b481c4614b34088a88b3487fc
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