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Microbial gene expression in Guaymas Basin subsurface sediments responds to hydrothermal stress and energy limitation

The ISME Journal volume 17, pages 1907–1919 (2023)Cite this article

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Abstract

Analyses of gene expression of subsurface bacteria and archaea provide insights into their physiological adaptations to in situ subsurface conditions. We examined patterns of expressed genes in hydrothermally heated subseafloor sediments with distinct geochemical and thermal regimes in Guaymas Basin, Gulf of California, Mexico. RNA recovery and cell counts declined with sediment depth, however, we obtained metatranscriptomes from eight sites at depths spanning between 0.8 and 101.9 m below seafloor. We describe the metabolic potential of sediment microorganisms, and discuss expressed genes involved in tRNA, mRNA, and rRNA modifications that enable physiological flexibility of bacteria and archaea in the hydrothermal subsurface. Microbial taxa in hydrothermally influenced settings like Guaymas Basin may particularly depend on these catalytic RNA functions since they modulate the activity of cells under elevated temperatures and steep geochemical gradients. Expressed genes for DNA repair, protein maintenance and circadian rhythm were also identified. The concerted interaction of many of these genes may be crucial for microorganisms to survive and to thrive in the Guaymas Basin subsurface biosphere.

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Fig. 1: Guaymas Basin overview.
Fig. 2: Cell abundances for eight IODP385 drilling sites sampled for metatranscriptomic analysis.
Fig. 3: Heatmap showing expression levels (log2(TPM + 1)) of selected metabolic and cellular processes in Guaymas Basin subsurface sediment samples.
Fig. 4: Heatmap of expressed genes (log2(TPM + 1)) associated with methanogenesis, folate and glycine biosynthesis, sulfur and nitrogen cycling, and chemoautotrophy in Guaymas Basin subsurface sediments as identified in KEGG modules.
Fig. 5: Overview of expressed genes for DNA maintenance and repair, RNA editing, and protein homeostasis and degradation used by Guaymas Basin subsurface bacteria and archaea.
Fig. 6: Heatmap of expressed genes (log2(TPM + 1)) in Guaymas Basin subsurface sediment samples associated with prokaryotic mRNA modifications, DNA maintenance and repair, proteostasis, proteolysis and electron-transfer proteins as identified with BLASTx against NR.

Data availability

The raw metatranscriptome sequencing data in this study have been deposited in the National Center for Biotechnology Information Sequence Read Archive under the accession numbers SRR22580929-SRR22580947. PacBio reads were deposited to the National Center for Biotechnology Information Sequence Read Archive under access numbers SRR23604162-SRR23604206.

Code availability

The custom R scripts used in this study are publicly available at Zenodo (https://doi.org/10.5281/zenodo.7710615) [99].

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Acknowledgements

We would like to acknowledge the crew and entire science party for IODP Expedition 385 for their assistance with sample collection. Without their assistance this study would have been impossible. We thank Dr. Daniel Lizarralde (WHOI) for the edited bathymetric map of Guaymas Basin. We also thank Takeshi Terada and Megumi Becchaku for assisting with cell counting. This study was supported by the National Science Foundation Grant OCE-2046799 to VE, PM, AT, R. Hatzenpichler, and OCE-1829903 to VE, PM, and AT, JSPS KAKENHI JP19H00730 and JP23H00154 to YM, and China Postdoctoral Science Foundation (2022M720039) and Guangdong Natural Resources Foundation (GDNRC[2023]30) to Y-LZ.

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Authors and Affiliations

  1. Geology and Geophysics Department, Woods Hole Oceanographic Institution, Woods Hole, MA, USA

    Paraskevi Mara & Virginia Edgcomb

  2. Southern Marine Science and Engineering Guangdong Laboratory (Guangzhou), Guangzhou, China

    Ying-Li Zhou

  3. Department of Earth, Marine and Environmental Sciences, University of North Carolina, Chapel Hill, NC, USA

    Andreas Teske

  4. Kochi Institute for Core Sample Research, Institute for Extra-cutting-edge Science and Technology Avant-garde Research (X-star), Japan Agency for Marine-Earth Science and Technology (JAMSTEC), Monobe, Nankoku, Kochi, Japan

    Yuki Morono

  5. Biology Department, Woods Hole Oceanographic Institution, Woods Hole, MA, USA

    David Beaudoin

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  1. Paraskevi Mara
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Contributions

VE, AT and PM conceived of the experiments and designed the sampling strategy for analyses discussed in this paper. AT served as Co-Chief Scientist for IODP Expedition 385. VE collected samples for this study, with assistance from other IODP 385 shipboard microbiologists. YM performed cell counts, and provided cell count data and cell count figures. PM extracted RNA from samples for metatranscriptome analyses and DNA for the 16S rRNA marker gene analyses. PM, Y-LZ and DB analyzed metatranscriptome data. PM and Y-LZ analyzed marker gene data. PM, VE, AT, YM discussed data interpretation. PM wrote the first draft of the paper and all authors contributed to its final form.

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Correspondence to Virginia Edgcomb.

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Mara, P., Zhou, YL., Teske, A. et al. Microbial gene expression in Guaymas Basin subsurface sediments responds to hydrothermal stress and energy limitation. ISME J 17, 1907–1919 (2023). https://doi.org/10.1038/s41396-023-01492-z

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