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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.

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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].

References

  1. Dick GJ. The microbiomes of deep-sea hydrothermal vents: distributed globally, shaped locally. Nat Rev Microbiol. 2019;17:271–83.

    CAS  PubMed  Google Scholar 

  2. Lanzén A, Jørgensen SL, Bengtsson MM, Jonassen I, Øvreås L, Urich T. Exploring the composition and diversity of microbial communities at the Jan Mayen hydrothermal vent field using RNA and DNA. FEMS Microbiol Ecol. 2011;77:577–89.

    PubMed  Google Scholar 

  3. Biddle JF, Cardman Z, Mendlovitz H, Albert DB, Lloyd KG, Boetius A, et al. Anaerobic oxidation of methane at different temperature regimes in Guaymas Basin hydrothermal sediments. ISME J. 2012;6:1018–31.

    CAS  PubMed  Google Scholar 

  4. Lesniewski R, Jain S, Anantharaman K, Schloss PD, Dick GJ. The metatranscriptome of a deep-sea hydrothermal plume is dominated by water column methanotrophs and lithotrophs. ISME J. 2012;6:2257–68.

    CAS  PubMed  PubMed Central  Google Scholar 

  5. Urich T, Lanzén A, Stokke R, Pedersen RB, Bayer C, Thorseth IH, et al. Microbial community structure and functioning in marine sediments associated with diffuse hydrothermal venting assessed by integrated meta-omics. Environ Microbiol. 2014;16:2699–710.

    CAS  PubMed  Google Scholar 

  6. Stokke R, Dahle H, Roalkvam I, Wissuwa J, Daae FL, Tooming-Klunderud A, et al. Functional interactions among filamentous Epsilonproteobacteria and bacteroidetes in a deep-sea hydrothermal vent biofilm. Environ Microbiol 2015;17:4063–77.

    CAS  PubMed  Google Scholar 

  7. Fortunato CS, Butterfield DA, Larson B, Lawrence-Slavas N, Algar CK, Zeigler Allen L, et al. Seafloor incubation experiment with deep-sea hydrothermal vent fluid reveals effect of pressure and lag time on autotrophic microbial communities. Appl Environ Microbiol. 2021;87:e00078–21.

    CAS  PubMed  PubMed Central  Google Scholar 

  8. Fortunato C, Huber J. Coupled RNA-SIP and metatranscriptomics of active chemolithoautotrophic communities at a deep-sea hydrothermal vent. ISME J. 2016;10:1925–38.

    CAS  PubMed  PubMed Central  Google Scholar 

  9. Lonsdale P, Becker K. Hydrothermal plumes, hot springs, and conductive heat flow in the Southern Trough of Guaymas Basin. Earth Planet Sci Lett 1985;73:211–25.

    CAS  Google Scholar 

  10. Von Damm KL, Edmond JM, Measures CI, Grant B. Chemistry of submarine hydrothermal solutions at Guaymas Basin, Gulf of California. Geochim Cosmochim Acta. 1985;49:2221–37.

    Google Scholar 

  11. Simoneit BRT, Schoell M. Carbon isotope systematics of individual hydrocarbons in hydrothermal petroleums from the Guaymas Basin, Gulf of California. Org Geochem 1995;23:857–63.

    CAS  Google Scholar 

  12. Cruaud P, Vigneron A, Pignet P, Caprais J-C, Lesongeur F, Toffin L, et al. Comparative study of Guaymas Basin microbiomes: cold seeps vs. hydrothermal vents sediments. Front Mar Sci 2015;4:417.

    Google Scholar 

  13. Ramírez GA, Mara P, Sehein T, Wegener G, Chambers CR, Joye SB, et al. Environmental factors shaping bacterial, archaeal and fungal community structure in hydrothermal sediments of Guaymas Basin, Gulf of California. PLoS One. 2021;16:e0256321.

    PubMed  PubMed Central  Google Scholar 

  14. Dombrowski N, Teske AP, Baker BJ. Expansive microbial metabolic versatility and biodiversity in dynamic Guaymas Basin hydrothermal sediments. Nat Commun. 2018;9:4999.

    PubMed  PubMed Central  Google Scholar 

  15. Seitz KW, Dombrowski N, Eme L, Spang A, Lombard J, Sieber JR, et al. Asgard archaea capable of anaerobic hydrocarbon cycling. Nat Commun. 2019;10:1822.

    PubMed  PubMed Central  Google Scholar 

  16. Ramírez GA, McKay LJ, Fields MW, Buckley A, Mortera C, Hensen C, et al. The Guaymas Basin subseafloor sedimentary archaeome reflects complex environmental histories. iScience. 2020;23:101459.

    PubMed  PubMed Central  Google Scholar 

  17. Lizarralde D, Teske A, Höfig TW, González-Fernández A, the IODP Expedition 385 Scientists. Carbon release by sill intrusion into young sediments measured through scientific drilling. Geology. 2023;51:329–33.

    CAS  Google Scholar 

  18. Kikuchi G, Motokawa Y, Yoshida T, Hiraga K. Glycine cleavage system: reaction mechanism, physiological significance, and hyperglycinemia. Proc Jpn Acad Ser B Phys Biol Sci. 2008;84:246–63.

    CAS  PubMed  PubMed Central  Google Scholar 

  19. Price MN, Deutschbauer AM, Arkin AP. Four families of folate-independent methionine synthases. PLoS Genet. 2021;17:e1009342.

    CAS  PubMed  PubMed Central  Google Scholar 

  20. Danchin A, Sekowska A, You C. One-carbon metabolism, folate, zinc and translation. Micro Biotechnol. 2020;13:899–925.

    CAS  Google Scholar 

  21. Büttner K, Wenig K, Hopfner KP. Structural framework for the mechanism of archaeal exosomes in RNA processing. Mol Cell. 2005;20:461–71.

    PubMed  Google Scholar 

  22. Johnson SJ, Jackson RN. Ski2-like RNA helicase structures: common themes and complex assemblies. RNA Biol. 2013;10:33–43.

    CAS  PubMed  PubMed Central  Google Scholar 

  23. Clouet-d’Orval B, Phung DK, Langendijk-Genevaux PS, Quentin Y. Universal RNA-degrading enzymes in Archaea: Prevalence, activities and functions of β-CASP ribonucleases. Biochimie. 2015;118:278–85.

    PubMed  Google Scholar 

  24. Cousineau B, Smith D, Lawrence-Cavanagh S, Mueller JE, Yang J, Mills D, et al. Retrohoming of a bacterial group II intron: mobility via complete reverse splicing, independent of homologous DNA recombination. Cell. 1995;94:451–62.

    Google Scholar 

  25. Evguenieva-Hackenberg, E The archaeal exosome. in RNA Exosome. Advances in Experimental Medicine and Biology (eds Jensen, TH) 29–38 (Springer, New York, 2010).

  26. Cameron TA, Matz LM, De Lay NR. Polynucleotide phosphorylase: Not merely an RNase but a pivotal post-transcriptional regulator. PLoS Genet. 2018;14:e1007654.

    PubMed  PubMed Central  Google Scholar 

  27. Gottesman ME, Mustaev A. Ribonucleoside-5’-diphosphates (NDPs) support RNA polymerase transcription, suggesting NDPs may have been substrates for primordial nucleic acid biosynthesis. J Biol Chem. 2019;294:11785–92.

    CAS  PubMed  PubMed Central  Google Scholar 

  28. Guzmán EC, Caballero JL, Jiménez-Sánchez A. Ribonucleoside diphosphate reductase is a component of the replication hyperstructure in Escherichia coli. Mol Microbiol. 2002;43:487–95.

    PubMed  Google Scholar 

  29. Burke CR, Lupták A. DNA synthesis from diphosphate substrates by DNA polymerases. Proc Natl Acad Sci USA. 2018;115:980–5.

    CAS  PubMed  PubMed Central  Google Scholar 

  30. Orsi WD, Edgcomb VP, Christman GD, Biddle JF. Gene expression in the deep biosphere. Nature. 2013;499:205–8.

    CAS  PubMed  Google Scholar 

  31. Beulig F, Schubert F, Adhikari RR, Glombitza C, Heuer VB, Hinrichs KU, et al. Rapid metabolism fosters microbial survival in the deep, hot subseafloor biosphere. Nat Commun. 2022;13:312.

    CAS  PubMed  PubMed Central  Google Scholar 

  32. Rath D, Amlinger L, Rath A, Lundgren M. The CRISPR-Cas immune system: biology, mechanisms and applications. Biochimie. 2015;117:119–28.

    CAS  PubMed  Google Scholar 

  33. Matsuura M. A bacterial group II intron encoding reverse transcriptase, maturase, and DNA endonuclease activities. Genes Dev. 1997;11:2910–24.

    CAS  PubMed  PubMed Central  Google Scholar 

  34. Palchevskiy V, Finkel SE. Escherichia coli competence gene homologs are essential for competitive fitness and the use of DNA as a nutrient. J Bacteriol. 2006;188:3902–10.

    CAS  PubMed  PubMed Central  Google Scholar 

  35. Auxilien S, El Khadali F, Rasmussen A, Douthwaite S, Grosjean H. Archease from Pyrococcus abyssi improves substrate specificity and solubility of a tRNA m5C methyltransferase. J Biol Chem. 2007;282:18711–21.

    CAS  PubMed  Google Scholar 

  36. Klumpp M, Baumeister W. The thermosome: archetype of group II chaperonins. FEBS Lett. 1998;430:73–7.

    CAS  PubMed  Google Scholar 

  37. Whittaker CA, Hynes RO. Distribution and evolution of von Willebrand/integrin A domains: widely dispersed domains with roles in cell adhesion and elsewhere. Mol Biol Cell. 2002;13:3369–87.

    CAS  PubMed  PubMed Central  Google Scholar 

  38. Hoffmann L, Anders K, Bischof LF, Ye X, Reimann J, Khadouma S, et al. Structure and interactions of the archaeal motility repression module ArnA-ArnB that modulates archaellum gene expression in Sulfolobus acidocaldarius. J Biol Chem. 2019;294:7460–71.

    CAS  PubMed  PubMed Central  Google Scholar 

  39. Schmelling NM, Lehmann R, Chaudhury P, Beck C, Albers SV, Axmann IM, et al. Minimal tool set for a prokaryotic circadian clock. BMC Evol Biol. 2017;17:169.

    PubMed  PubMed Central  Google Scholar 

  40. Jabbur ML, Johnson CH. Spectres of clock evolution: past, present, and yet to come. Front Physiol. 2022;12:815847.

    PubMed  PubMed Central  Google Scholar 

  41. Rosato E, Kyriacou CP. Origins of circadian rhythmicity. J Biol Rhythms. 2002;17:506–11.

    PubMed  Google Scholar 

  42. Makarova KS, Galperin MY, Koonin EV. Proposed role for KaiC-like ATPases as major signal transduction hubs in Archaea. mBio. 2017;8:e01959–17.

    CAS  PubMed  PubMed Central  Google Scholar 

  43. Lin YS, Koch BP, Feseker T, Ziervogel K, Goldhammer T, Schmidt F, et al. Near-surface heating of young rift sediment causes mass production and discharge of reactive dissolved organic matter. Sci Rep. 2017;7:44864.

    CAS  PubMed  PubMed Central  Google Scholar 

  44. Vigneron A, Cruaud P, Roussel EG, Pignet P, Caprais JC, Callac N, et al. Phylogenetic and functional diversity of microbial communities associated with subsurface sediments of the Sonora Margin, Guaymas Basin. PLoS One. 2014;9:e104427.

    PubMed  PubMed Central  Google Scholar 

  45. Jones ME. Carbamyl Phosphate: Many forms of life use this molecule to synthesize arginine, uracil, and adenosine triphosphate. Science. 1963;140:1373–9.

    CAS  PubMed  Google Scholar 

  46. Xin K, Zhang Y, Fan L, Qi Z, Feng C, Wang Q, et al. Experimental evidence for the functional importance and adaptive advantage of A-to-I RNA editing in fungi. Proc Natl Acad Sci USA. 2023;120:e2219029120.

    CAS  PubMed  PubMed Central  Google Scholar 

  47. Pierrel F, Hernandez HL, Johnson MK, Fontecave M, Atta M. MiaB protein from Thermotoga maritima. Characterization of an extremely thermophilic tRNA-methylthiotransferase. J Biol Chem. 2003;278:29515–24.

    CAS  PubMed  Google Scholar 

  48. Teske A, Callaghan AV, LaRowe DE. Biosphere frontiers of subsurface life in the sedimented hydrothermal system of Guaymas Basin. Front Microbiol 2014;5:362.

    PubMed  PubMed Central  Google Scholar 

  49. Schaefer M, Kapoor U, Jantsch MF. Understanding RNA modifications: the promises and technological bottlenecks of the ‘epitranscriptome’. Open Biol. 2017;7:170077.

    PubMed  PubMed Central  Google Scholar 

  50. Laxman S, Sutter BM, Wu X, Kumar S, Guo X, Trudgian DC, et al. Sulfur amino acids regulate translational capacity and metabolic homeostasis through modulation of tRNA thiolation. Cell. 2013;154:416–42.

    CAS  PubMed  PubMed Central  Google Scholar 

  51. Thompson KM, Gottesman S. The MiaA tRNA modification enzyme is necessary for robust RpoS expression in Escherichia coli. J Bacteriol. 2014;196:754–61.

    PubMed  PubMed Central  Google Scholar 

  52. Teske A, Lizarralde D, Höfig TW, and the Expedition 385 Scientists. Guaymas Basin Tectonics and Biosphere. Proceedings of the International Ocean Discovery Program, 385: College Station, TX (International Ocean Discovery Program) (2021). https://doi.org/10.14379/iodp.proc.385.2021.

  53. Cheng-Guang H, Gualerzi CO. The ribosome as a switchboard for bacterial stress response. Front Microbiol. 2021;11:619038.

    PubMed  PubMed Central  Google Scholar 

  54. Starnawski P, Bataillon T, Ettema TJ, Jochum LM, Schreiber L, Chen X, et al. Microbial community assembly and evolution in subseafloor sediment. Proc Natl Acad Sci USA. 2017;114:2940–5.

    CAS  PubMed  PubMed Central  Google Scholar 

  55. Kirkpatrick JB, Walsh EA, D’Hondt S. Microbial selection and survival in subseafloor sediment. Front Micro. 2019;10:9566.

    Google Scholar 

  56. Hui MP, Foley PL, Belasco JG. Messenger RNA degradation in bacterial cells. Annu Rev Genet. 2014;48:537–59.

    CAS  PubMed  PubMed Central  Google Scholar 

  57. Finkel SE, Kolter R. DNA as a nutrient: novel role for bacterial competence gene homologs. J Bacteriol. 2001;183:6288–93.

    CAS  PubMed  PubMed Central  Google Scholar 

  58. Jørgensen BB. Shrinking majority of the deep biosphere. Proc Natl Acad Sci USA. 2012;109:15976–7.

    PubMed  PubMed Central  Google Scholar 

  59. Biddle JF, Lipp JS, Lever MA, Lloyd KG, Sørensen KB, Anderson R et al. Heterotrophic archaea dominate sedimentary subsurface ecosystems off Peru. Proc Natl Acad Sci USA. 2006;103:3846–51.

    CAS  PubMed  PubMed Central  Google Scholar 

  60. Lynch M, Marinov GK. The bioenergetic costs of a gene. Proc Natl Acad Sci USA. 2015;11:15690–5.

    Google Scholar 

  61. Goyal M, Banerjee C, Nag S, Bandyopadhyay U. The Alba protein family: structure and function. Biochim Biophys Acta. 2016;1864:570–83.

    CAS  PubMed  Google Scholar 

  62. Anantharaman V, Koonin EV, Aravind L. Comparative genomics and evolution of proteins involved in RNA metabolism. Nucleic Acids Res. 2002;30:1427–64.

    CAS  PubMed  PubMed Central  Google Scholar 

  63. Aravind L, Iyer LM, Anantharaman V. The two faces of Alba: the evolutionary connection between proteins participating in chromatin structure and RNA metabolism. Genome Biol. 2003;4:R64.

    CAS  PubMed  PubMed Central  Google Scholar 

  64. Gupta R, Laxman S. tRNA wobble-uridine modifications as amino acid sensors and regulators of cellular metabolic state. Curr Genet. 2020;66:475–80.

    CAS  PubMed  Google Scholar 

  65. Droogmans L, Roovers M, Bujnicki JM, Tricot C, Hartsch T, Stalon V, et al. Cloning and characterization of tRNA (m1A58) methyltransferase (TrmI) from Thermus thermophilus HB27, a protein required for cell growth at extreme temperatures. Nucleic Acids Res. 2003;31:2148–56.

    CAS  PubMed  PubMed Central  Google Scholar 

  66. Kimura S, Suzuki T. Iron-sulfur proteins responsible for RNA modifications. Biochim Biophys Acta. 2015;1853:1272–83.

    CAS  PubMed  Google Scholar 

  67. Gupta R, Walvekar AS, Liang S, Rashida Z, Shah P, Laxman S. A tRNA modification balances carbon and nitrogen metabolism by regulating phosphate homeostasis. eLife. 2019;8:e44795.

    CAS  PubMed  PubMed Central  Google Scholar 

  68. Heinemann IU, Söll D, Randau L. Transfer RNA processing in archaea: unusual pathways and enzymes. FEBS Lett. 2010;584:303–9.

    CAS  PubMed  PubMed Central  Google Scholar 

  69. Middelboe M, Glud RN, Wenzhöfer F, Oguri K, Kitazato H. Spatial distribution and activity of viruses in the deep-sea sediments of Sagami Bay, Japan. Deep-Sea Res I. 2006;53:1–13.

    Google Scholar 

  70. Manini E, Luna GM, Corinaldesi C, Zeppilli D, Bortoluzzi G, Caramanna G, et al. Prokaryote diversity and virus abundance in shallow hydrothermal vents of the Mediterranean Sea (Panarea Island) and the Pacific Ocean (North Sulawesi-Indonesia). Microb Ecol 2008;55:626–39.

    CAS  PubMed  Google Scholar 

  71. Zhou YL, Mara P, Vik D, Edgcomb VP, Sullivan MB, Wang Y. Ecogenomics reveals viral communities across the Challenger Deep oceanic trench. Commun Biol. 2022;5:1055.

    CAS  PubMed  PubMed Central  Google Scholar 

  72. Imlay JA. How obligatory is anaerobiosis? Mol Microbiol. 2008;68:801–4.

    CAS  PubMed  PubMed Central  Google Scholar 

  73. Arosio P, Elia L, Poli M. Ferritin, cellular iron storage and regulation. IUBMB Life. 2017;69:414–22.

    CAS  PubMed  Google Scholar 

  74. Eelderink-Chen Z, Bosman J, Sartor F, Dodd AN, Kovács AT, Merrow M. A circadian clock in a nonphotosynthetic prokaryote. Sci Adv. 2021;7:eabe2086.

    CAS  PubMed  PubMed Central  Google Scholar 

  75. Hagelueken G, Wiehlmann L, Adams TM, Kolmar H, Heinz DW, Tümmler B, et al. Crystal structure of the electron transfer complex rubredoxin rubredoxin reductase of Pseudomonas aeruginosa. Proc Natl Acad Sci USA. 2007;104:12276–81.

    PubMed  PubMed Central  Google Scholar 

  76. Giessen TW, Orlando BJ, Verdegaal AA, Chambers MG, Gardener J, Bell DC, et al. Large protein organelles form a new iron sequestration system with high storage capacity. eLife. 2019;8:e46070.

    PubMed  PubMed Central  Google Scholar 

  77. Scholz F, Schmidt M, Hensen C, Eroglu S, Geilert S, Gutjahr M, et al. Shelf-to-basin iron shuttle in the Guaymas Basin, Gulf of California. Geochim Cosmochim Acta. 2019;261:76–92. 2019

    CAS  Google Scholar 

  78. Fauvet B, Rebeaud ME, Tiwari S, De Los Rios P, Goloubinoff P. Repair or degrade: the thermodynamic dilemma of cellular protein quality-control. Front Mol Biosci. 2021;8:768888.

    CAS  PubMed  PubMed Central  Google Scholar 

  79. Sharma SK, De los Rios P, Christen P, Lustig A, Goloubinoff P. The kinetic parameters and energy cost of the Hsp70 chaperone as a polypeptide unfoldase. Nat Chem Biol 2010;6:914–20.

    CAS  PubMed  Google Scholar 

  80. Suzuki MT, Taylor LT, DeLong EF. Quantitative analysis of small-subunit rRNA genes in mixed microbial populations via 5’-nuclease assays. Appl Environ Microbiol. 2000;66:4605–14.

    CAS  PubMed  PubMed Central  Google Scholar 

  81. Chen S, Zhou Y, Chen Y, Gu J. fastp: an ultra-fast all-in-one FASTQ preprocessor. Bioinformatics. 2018;34:i884–90.

    PubMed  PubMed Central  Google Scholar 

  82. Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I, et al. Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol. 2011;29:644–52.

    CAS  PubMed  PubMed Central  Google Scholar 

  83. Buchfink B, Reuter K, Drost HG. Sensitive protein alignments at tree-of-life scale using DIAMOND. Nat Methods. 2021;18:366–8.

    CAS  PubMed  PubMed Central  Google Scholar 

  84. Salter SJ, Cox MJ, Turek EM, Calus ST, Cookson WO, Moffatt MF, et al. Reagent and laboratory contamination can critically impact sequence-based microbiome analyses. BMC Biol. 2014;12:87.

    PubMed  PubMed Central  Google Scholar 

  85. Hyatt D, Chen GL, Locascio PF, Land ML, Larimer FW, Hauser LJ. Prodigal: prokaryotic gene recognition and translation initiation site identification. Bmc Bioinforma. 2010;11:119.

    Google Scholar 

  86. Fu L, Niu B, Zhu Z, Wu S, Li W. CD-HIT: accelerated for clustering the next-generation sequencing data. Bioinformatics. 2012;28:3150–2.

    CAS  PubMed  PubMed Central  Google Scholar 

  87. Aramaki T, Blanc-Mathieu R, Endo H, Ohkubo K, Kanehisa M, Goto S, et al. KofamKOALA: KEGG ortholog assignment based on profile HMM and adaptive score threshold. Bioinformatics. 2019;36:2251–2.

    PubMed Central  Google Scholar 

  88. Kanehisa M, Sato Y, Morishima K. BlastKOALA and GhostKOALA: KEGG tools for functional characterization of genome and metagenome sequences. J Mol Biol 2016;428:726–31.

    CAS  PubMed  Google Scholar 

  89. Patro R, Duggal G, Love MI, Irizarry RA, Kingsford C. Salmon provides fast and bias-aware quantification of transcript expression. Nat Methods. 2017;14:417–9.

    CAS  PubMed  PubMed Central  Google Scholar 

  90. Urbach E, Vergin KL, Young L, Morse A, Larson GL, Giovannoni SJ. Unusual bacterioplankton community structure in ultra-oligotrophic Crater Lake. Limnol Oceanogr 2001;46:557–72.

    CAS  Google Scholar 

  91. Takai K, Horikoshi K. Rapid detection and quantification of members of the archaeal community by quantitative PCR using fluorogenic probes. Appl Environ Microbiol. 2000;66:5066–72.

    CAS  PubMed  PubMed Central  Google Scholar 

  92. Boylen E, Rideout JR, Dillon MR, Bokulich NA, Abnet CC, Al-Ghalith GA, et al. Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nat Biotechnol. 2019;37:852–7.

    Google Scholar 

  93. Bokulich NA, Kaehler BD, Rideout JR, Dillon M, Bolyen E, Knight R, et al. Optimizing taxonomic classification of marker-gene amplicon sequences with QIIME 2’s q2-feature-classifier plugin. Microbiome. 2018;6:90.

    PubMed  PubMed Central  Google Scholar 

  94. Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, et al. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res. 2013;41:D590–6.

    CAS  PubMed  Google Scholar 

  95. Morono Y, Terada T, Kallmeyer J, Inagaki F. An improved cell separation technique for marine subsurface sediments: applications for high-throughput analysis using flow cytometry and cell sorting. Environ Microbiol 2013;15:2841–9.

    CAS  PubMed  PubMed Central  Google Scholar 

  96. Kallmeyer J, Smith DC, Spivack AJ, D’Hondt S. New cell extraction procedure applied to deep subsurface sediments. LO Methods. 2008;6:236–45.

    Google Scholar 

  97. Inagaki F, Hinrichs KU, Kubo Y, Bowles MW, Heuer VB, Hong WL, et al. Exploring deep microbial life in coal-bearing sediment down to ~2.5 km below the ocean floor. Science. 2015;349:420–4.

    CAS  PubMed  Google Scholar 

  98. Morono Y, Terada T, Masui N, Inagaki F. Discriminative detection and enumeration of microbial life in marine subsurface sediments. ISME J. 2009;3:503–11.

    CAS  PubMed  Google Scholar 

  99. Zhou YL, Mara P. Analysis of the deep biosphere metatranscriptomes. Zenodo Accessed 2023. https://doi.org/10.5281/zenodo.7710615

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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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