in

Carbon fixation rates in groundwater similar to those in oligotrophic marine systems

  • Falkowski, P. et al. The global carbon cycle: a test of our knowledge of Earth as a system. Science 290, 291–296 (2000).

    Article 

    Google Scholar 

  • McMahon, S. & Parnell, J. Weighing the deep continental biosphere. FEMS Microbiol. Ecol. 87, 113–120 (2014).

    Article 

    Google Scholar 

  • Magnabosco, C. et al. The biomass and biodiversity of the continental subsurface. Nat. Geosci. 11, 707–717 (2018).

    Article 

    Google Scholar 

  • Gleeson, T., Befus, K. M., Jasechko, S., Luijendijk, E. & Cardenas, M. B. The global volume and distribution of modern groundwater. Nat. Geosci. 9, 161–167 (2016).

    Article 

    Google Scholar 

  • Stevanović, Z. Karst waters in potable water supply: a global scale overview. Environ. Earth Sci. 78, 662 (2019).

    Article 

    Google Scholar 

  • Poulson, T. L. & White, W. B. The cave environment. Science 165, 971–981 (1969).

    Article 

    Google Scholar 

  • Rusterholtz, K. J. & Mallory, L. M. Density, activity, and diversity of bacteria indigenous to a karstic aquifer. Microb. Ecol. 28, 79–99 (1994).

    Article 

    Google Scholar 

  • Smith, H. J. et al. Impact of hydrologic boundaries on microbial planktonic and biofilm communities in shallow terrestrial subsurface environments. FEMS Microbiol. Ecol. 94, fiy191 (2018).

    Google Scholar 

  • Alexander, M. Introduction to Soil Microbiology (Wiley, 1977).

  • Griebler, C. & Lueders, T. Microbial biodiversity in groundwater ecosystems. Freshw. Biol. 54, 649–677 (2009).

    Article 

    Google Scholar 

  • Krumholz, L. R., McKinley, J. P., Ulrich, G. A. & Suflita, J. M. Confined subsurface microbial communities in Cretaceous rock. Nature 386, 64–66 (1997).

    Article 

    Google Scholar 

  • Probst, A. J. et al. Differential depth distribution of microbial function and putative symbionts through sediment-hosted aquifers in the deep terrestrial subsurface. Nat. Microbiol. 3, 328–336 (2018).

    Article 

    Google Scholar 

  • Magnabosco, C. et al. A metagenomic window into carbon metabolism at 3 km depth in Precambrian continental crust. ISME J. 10, 730–741 (2016).

    Article 

    Google Scholar 

  • Stevens, T. O. & McKinley, J. P. Lithoautotrophic microbial ecosystems in deep basalt aquifers. Science 270, 450–455 (1995).

    Article 

    Google Scholar 

  • Tiago, I. & Veríssimo, A. Microbial and functional diversity of a subterrestrial high pH groundwater associated to serpentinization. Environ. Microbiol. 15, 1687–1706 (2013).

    Article 

    Google Scholar 

  • Mccollom, T. M. & Amend, J. P. A thermodynamic assessment of energy requirements for biomass synthesis by chemolithoautotrophic micro-organisms in oxic and anoxic environments. Geobiology 3, 135–144 (2005).

    Article 

    Google Scholar 

  • Momper, L., Jungbluth, S. P., Lee, M. D. & Amend, J. P. Energy and carbon metabolisms in a deep terrestrial subsurface fluid microbial community. ISME J. 11, 2319–2333 (2017).

    Article 

    Google Scholar 

  • Jewell, T. N. M., Karaoz, U., Brodie, E. L., Williams, K. H. & Beller, H. R. Metatranscriptomic evidence of pervasive and diverse chemolithoautotrophy relevant to C, S, N and Fe cycling in a shallow alluvial aquifer. ISME J. 10, 2106–2117 (2016).

    Article 

    Google Scholar 

  • Herrmann, M., Rusznyák, A. & Akob, D. M. Large fractions of CO2-fixing microorganisms in pristine limestone aquifers appear to be involved in the oxidation of reduced sulfur and nitrogen compounds. Appl. Environ. Microbiol. 81, 2384–2394 (2015).

  • Peterson, B. J. Aquatic primary productivity and the 14C–CO2 method: a history of the productivity problem. Annu. Rev. Ecol. Syst. 11, 359–385 (1980).

    Article 

    Google Scholar 

  • Viviani, D. A., Karl, D. M. & Church, M. J. Variability in photosynthetic production of dissolved and particulate organic carbon in the North Pacific Subtropical Gyre. Front. Mar. Sci. 2, 73 (2015).

    Article 

    Google Scholar 

  • Kohlhepp, B. et al. Aquifer configuration and geostructural links control the groundwater quality in thin-bedded carbonate–siliciclastic alternations of the Hainich CZE, central Germany. Hydrol. Earth Syst. Sci. 21, 6091–6116 (2017).

    Article 

    Google Scholar 

  • Pedersen, K. & Ekendahl, S. Assimilation of CO2 and introduced organic compounds by bacterial communities in groundwater from southeastern Sweden deep crystalline bedrock. Microb. Ecol. 23, 1–14 (1992).

    Article 

    Google Scholar 

  • Partensky, F. & Garczarek, L. Prochlorococcus: advantages and limits of minimalism. Ann. Rev. Mar. Sci. 2, 305–331 (2010).

    Article 

    Google Scholar 

  • Karl, D. M., Hebel, D. V., Björkman, K. & Letelier, R. M. The role of dissolved organic matter release in the productivity of the oligotrophic North Pacific Ocean. Limnol. Oceanogr. 43, 1270–1286 (1998).

    Article 

    Google Scholar 

  • Liang, Y. et al. Estimating primary production of picophytoplankton using the carbon-based ocean productivity model: a preliminary study. Front. Microbiol. 8, 1926 (2017).

    Article 

    Google Scholar 

  • Steinberg, D. K. et al. Overview of the US JGOFS Bermuda Atlantic Time-series Study (BATS): a decade-scale look at ocean biology and biogeochemistry. Deep Sea Res. 2 48, 1405–1447 (2001).

    Article 

    Google Scholar 

  • Gundersen, K., Orcutt, K. M., Purdie, D. A., Michaels, A. F. & Knap, A. H. Particulate organic carbon mass distribution at the Bermuda Atlantic Time-series Study (BATS) site. Deep Sea Res. 2 48, 1697–1718 (2001).

    Article 

    Google Scholar 

  • Karl, D. M. & Lukas, R. The Hawaii Ocean Time-series (HOT) program: background, rationale and field implementation. Deep Sea Res. 2 43, 129–156 (1996).

    Article 

    Google Scholar 

  • Martiny, A. C., Vrugt, J. A. & Lomas, M. W. Concentrations and ratios of particulate organic carbon, nitrogen, and phosphorus in the global ocean. Sci. Data 1, 140048 (2014).

    Article 

    Google Scholar 

  • Martiny, A. C., Vrugt, J. A. & Lomas, M. W. Data from: Concentrations and ratios of particulate organic carbon, nitrogen, and phosphorus in the global ocean. Dryad https://doi.org/10.5061/dryad.d702p (2015).

  • Schwab, V. F. et al. 14C-free carbon Is a major contributor to cellular biomass in geochemically distinct groundwater of shallow sedimentary bedrock aquifers. Water Resour. Res. 55, 2104–2121 (2019).

    Article 

    Google Scholar 

  • Taubert, M. et al. Bolstering fitness via CO2 fixation and organic carbon uptake: mixotrophs in modern groundwater. ISME J 16, 1153–1162 (2022).

    Article 

    Google Scholar 

  • Rimstidt, J. D. & Vaughan, D. J. Pyrite oxidation: a state-of-the-art assessment of the reaction mechanism. Geochim. Cosmochim. Acta 67, 873–880 (2003).

    Article 

    Google Scholar 

  • Lin, W. et al. Genomic insights into the uncultured genus “Candidatus Magnetobacterium” in the phylum Nitrospirae. ISME J. 8, 2463–2477 (2014).

    Article 

    Google Scholar 

  • Kato, S. et al. Genome-enabled metabolic reconstruction of dominant chemosynthetic colonizers in deep-sea massive sulfide deposits. Environ. Microbiol. 20, 862–877 (2018).

    Article 

    Google Scholar 

  • Anantharaman, K. et al. Thousands of microbial genomes shed light on interconnected biogeochemical processes in an aquifer system. Nat. Commun. 7, 13219 (2016).

    Article 

    Google Scholar 

  • Kojima, H., Watanabe, T. & Fukui, M. Sulfuricaulis limicola gen. nov., sp. nov., a sulfur oxidizer isolated from a lake. Int. J. Syst. Evol. Microbiol. 66, 266–270 (2016).

    Article 

    Google Scholar 

  • Strous, M., Van Gerven, E., Kuenen, J. G. & Jetten, M. Effects of aerobic and microaerobic conditions on anaerobic ammonium-oxidizing (anammox) sludge. Appl. Environ. Microbiol. 63, 2446–2448 (1997).

    Article 

    Google Scholar 

  • Ji, X., Wu, Z., Sung, S. & Lee, P.-H. Metagenomics and metatranscriptomics analyses reveal oxygen detoxification and mixotrophic potentials of an enriched anammox culture in a continuous stirred-tank reactor. Water Res. 166, 115039 (2019).

    Article 

    Google Scholar 

  • Dalsgaard, T. et al. Oxygen at nanomolar levels reversibly suppresses process rates and gene expression in anammox and denitrification in the oxygen minimum zone off northern Chile. mBio 5, e01966 (2014).

    Article 

    Google Scholar 

  • Smith, R. L., Böhlke, J. K., Song, B. & Tobias, C. R. Role of anaerobic ammonium oxidation (anammox) in nitrogen removal from a freshwater aquifer. Environ. Sci. Technol. 49, 12169–12177 (2015).

    Article 

    Google Scholar 

  • Strous, M., Heijnen, J. J., Kuenen, J. G. & Jetten, M. S. M. The sequencing batch reactor as a powerful tool for the study of slowly growing anaerobic ammonium-oxidizing microorganisms. Appl. Microbiol. Biotechnol. 50, 589–596 (1998).

    Article 

    Google Scholar 

  • Kits, K. D. et al. Kinetic analysis of a complete nitrifier reveals an oligotrophic lifestyle. Nature 549, 269–272 (2017).

    Article 

    Google Scholar 

  • Rittmann, B. E. & McCarty, P. L. Environmental Biotechnology: Principles and Applications (McGraw-Hill Education, 2001).

  • Zhang, Y. et al. Nitrifier adaptation to low energy flux controls inventory of reduced nitrogen in the dark ocean. Proc. Natl. Acad. Sci. USA 117, 4823–4830 (2020).

    Article 

    Google Scholar 

  • Field, C. B., Behrenfeld, M. J., Randerson, J. T. & Falkowski, P. Primary production of the biosphere: integrating terrestrial and oceanic components. Science 281, 237–240 (1998).

    Article 

    Google Scholar 

  • Lehmann, R. & Totsche, K. U. Multi-directional flow dynamics shape groundwater quality in sloping bedrock strata. J. Hydrol. 580, 124291 (2020).

    Article 

    Google Scholar 

  • Küsel, K. et al. How deep can surface signals be traced in the Critical Zone? Merging biodiversity with biogeochemistry research in a central German Muschelkalk landscape. Front. Earth Sci. 4, 32 (2016).

    Article 

    Google Scholar 

  • Yan, L. et al. Environmental selection shapes the formation of near-surface groundwater microbiomes. Water Res. 170, 115341 (2019).

    Article 

    Google Scholar 

  • Pack, M. A. et al. A method for measuring methane oxidation rates using low levels of 14C-labeled methane and accelerator mass spectrometry: methane oxidation rates by AMS. Limnol. Oceanogr. Methods 9, 245–260 (2011).

    Article 

    Google Scholar 

  • Nielsen, E. S. The use of radio-active carbon (C14) for measuring organic production in the sea. ICES J. Mar. Sci. 18, 117–140 (1952).

    Article 

    Google Scholar 

  • Xu, X. et al. Modifying a sealed tube zinc reduction method for preparation of AMS graphite targets: reducing background and attaining high precision. Nucl. Instrum. Methods Phys. Res. B 259, 320–329 (2007).

    Article 

    Google Scholar 

  • Merser, S. Acetabulum online interactive statistical calculators. Accessed Feb, 2021. https://acetabulum.dk/anova.html

  • Bermuda Oceanographic Timeseries, accessed 21 Oct 2020, http://batsftp.bios.edu/BATS/production/bats_primary_production.txt

  • Hawaiian Oceanographic Timeseries, accessed 21 Oct 2020, ftp://ftp.soest.hawaii.edu/hot/primary_production

  • Hawaiian Oceanographic Timeseries, accessed 21 Oct 2020, https://hahana.soest.hawaii.edu/FTP/hot/microscopy/EPIslides.txt

  • Kumar, S. et al. Nitrogen loss from pristine carbonate-rock aquifers of the Hainich Critical Zone Exploratory (Germany) is primarily driven by chemolithoautotrophic anammox processes. Front. Microbiol. 8, 1951 (2017).

    Article 

    Google Scholar 

  • Füssel, J. et al. Nitrite oxidation in the Namibian oxygen minimum zone. ISME J. 6, 1200–1209 (2012).

    Article 

    Google Scholar 

  • McIlvin, M. R. & Altabet, M. A. Chemical conversion of nitrate and nitrite to nitrous oxide for nitrogen and oxygen isotopic analysis in freshwater and seawater. Anal. Chem. 77, 5589–5595 (2005).

    Article 

    Google Scholar 

  • Dalsgaard, T., Thamdrup, B., Farías, L. & Revsbech, N. P. Anammox and denitrification in the oxygen minimum zone of the eastern South Pacific. Limnol. Oceanogr. 57, 1331–1346 (2012).

    Article 

    Google Scholar 

  • Thamdrup, B. et al. Anaerobic ammonium oxidation in the oxygen-deficient waters off northern Chile. Limnol. Oceanogr. 51, 2145–2156 (2006).

    Article 

    Google Scholar 

  • Taubert, M. et al. Tracking active groundwater microbes with D2O labelling to understand their ecosystem function. Environ. Microbiol. 20, 369–384 (2018).

    Article 

    Google Scholar 

  • Bushnell, B. BBMap (SourceForge, 2014); http://sourceforge.net/projects/bbmap

  • Bornemann, T. L. V. et al. Geological degassing enhances microbial metabolism in the continental subsurface. Preprint at bioRxiv https://doi.org/10.1101/2020.03.07.980714 (2020).

  • Nurk, S., Meleshko, D., Korobeynikov, A. & Pevzner, P. A. metaSPAdes: a new versatile metagenomic assembler. Genome Res. 27, 824–834 (2017).

    Article 

    Google Scholar 

  • Hyatt, D. et al. Prodigal: prokaryotic gene recognition and translation initiation site identification. BMC Bioinformatics 11, 119 (2010).

    Article 

    Google Scholar 

  • Langmead, B. & Salzberg, S. L. Fast gapped-read alignment with Bowtie 2. Nat. Methods 9, 357 (2012).

    Article 

    Google Scholar 

  • Wu, Y.-W., Simmons, B. A. & Singer, S. W. MaxBin 2.0: an automated binning algorithm to recover genomes from multiple metagenomic datasets. Bioinformatics 32, 605–607 (2016).

    Article 

    Google Scholar 

  • Brown, C. T. et al. Unusual biology across a group comprising more than 15% of domain bacteria. Nature 523, 208–211 (2015).

    Article 

    Google Scholar 

  • Sieber, C. M. K. et al. Recovery of genomes from metagenomes via a dereplication, aggregation and scoring strategy. Nat. Microbiol. 3, 836–843 (2018).

    Article 

    Google Scholar 

  • Olm, M. R., Brown, C. T., Brooks, B. & Banfield, J. F. dRep: a tool for fast and accurate genomic comparisons that enables improved genome recovery from metagenomes through de-replication. ISME J. 11, 2864–2868 (2017).

    Article 

    Google Scholar 

  • Murat Eren, A. et al. Anvi’o: an advanced analysis and visualization platform for ‘omics data. PeerJ 3, e1319 (2015).

    Article 

    Google Scholar 

  • Aramaki, T. et al. KofamKOALA: KEGG Ortholog assignment based on profile HMM and adaptive score threshold. Bioinformatics 36, 2251–2252 (2020).

    Article 

    Google Scholar 

  • Graham, E. D., Heidelberg, J. F. & Tully, B. J. Potential for primary productivity in a globally-distributed bacterial phototroph. ISME J. 12, 1861–1866 (2018).

    Article 

    Google Scholar 

  • Kanehisa, M., Sato, Y. & Morishima, K. BlastKOALA and GhostKOALA: KEGG tools for functional characterization of genome and metagenome sequences. J. Mol. Biol. 428, 726–731 (2016).

    Article 

    Google Scholar 

  • Altschul, S. F., Gish, W., Miller, W., Myers, E. W. & Lipman, D. J. Basic local alignment search tool. J. Mol. Biol. 215, 403–410 (1990).

    Article 

    Google Scholar 

  • Pelikan, C. et al. Diversity analysis of sulfite- and sulfate-reducing microorganisms by multiplex dsrA and dsrB amplicon sequencing using new primers and mock community-optimized bioinformatics. Environ. Microbiol. 18, 2994–3009 (2016).

    Article 

    Google Scholar 

  • Lücker, S., Nowka, B., Rattei, T., Spieck, E. & Daims, H. The genome of Nitrospina gracilis Illuminates the metabolism and evolution of the major marine nitrite oxidizer. Front. Microbiol. 4, 27 (2013).

    Article 

    Google Scholar 

  • Orellana, L. H., Rodriguez-R, L. M. & Konstantinidis, K. T. ROCker: accurate detection and quantification of target genes in short-read metagenomic data sets by modeling sliding-window bitscores. Nucleic Acids Res. 45, e14 (2017).

    Google Scholar 

  • Chaumeil, P.-A., Mussig, A. J., Hugenholtz, P. & Parks, D. H. GTDB-Tk: a toolkit to classify genomes with the Genome Taxonomy Database. Bioinformatics 36, 1925–1927 (2020).

    Google Scholar 

  • Parks, D. H. et al. A standardized bacterial taxonomy based on genome phylogeny substantially revises the tree of life. Nat. Biotechnol. 36, 996–1004 (2018).

    Article 

    Google Scholar 

  • Parks, D. H. et al. A complete domain-to-species taxonomy for Bacteria and Archaea. Nat. Biotechnol. https://doi.org/10.1038/s41587-020-0501-8 (2020).

  • Matsen, F. A., Kodner, R. B. & Armbrust, E. V. pplacer: linear time maximum-likelihood and Bayesian phylogenetic placement of sequences onto a fixed reference tree. BMC Bioinformatics 11, 538 (2010).

    Article 

    Google Scholar 

  • Jain, C., Rodriguez-R, L. M., Phillippy, A. M., Konstantinidis, K. T. & Aluru, S. High throughput ANI analysis of 90 K prokaryotic genomes reveals clear species boundaries. Nat. Commun. 9, 5114 (2018).

    Article 

    Google Scholar 

  • Price, M. N., Dehal, P. S. & Arkin, A. P. FastTree 2—approximately maximum-likelihood trees for large alignments. PLoS ONE 5, e9490 (2010).

    Article 

    Google Scholar 

  • Eddy, S. R. Accelerated profile HMM searches. PLoS Comput. Biol. 7, e1002195 (2011).

    Article 

    Google Scholar 

  • Ondov, B. D. et al. Mash: fast genome and metagenome distance estimation using MinHash. Genome Biol. 17, 132 (2016).

    Article 

    Google Scholar 

  • Letunic, I. & Bork, P. Interactive Tree Of Life (iTOL): an online tool for phylogenetic tree display and annotation. Bioinformatics 23, 127–128 (2007).

    Article 

    Google Scholar 

  • Emiola, A. & Oh, J. High throughput in situ metagenomic measurement of bacterial replication at ultra-low sequencing coverage. Nat. Commun. 9, 4956 (2018).

    Article 

    Google Scholar 

  • Wegner, C.-E. et al. Biogeochemical regimes in shallow aquifers reflect the metabolic coupling of the elements nitrogen, sulfur, and carbon. Appl. Environ. Microbiol. 85, e02346-18 (2019).

    Article 

    Google Scholar 

  • R: A Language and Environment for Statistical Computing (R Core Team, 2018).

  • RStudio: Integrated Development Environment for R (RStudio Team, 2016).

  • Wickham, H. et al. Welcome to the tidyverse. J. Open Source Softw. 4, 1686 (2019).

    Article 

    Google Scholar 

  • Neuwirth, E. RColorBrewer: ColorBrewer Palettes. R package version 1.1-2. https://CRAN.R-project.org/package=RColorBrewer (2014).


  • Source: Ecology - nature.com

    Kerry Emanuel: A climate scientist and meteorologist in the eye of the storm

    Better living through multicellular life cycles