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Archaea
Volume 2017, Article ID 2136287, 13 pages
https://doi.org/10.1155/2017/2136287
Research Article

Archaeal Diversity and CO2 Fixers in Carbonate-/Siliciclastic-Rock Groundwater Ecosystems

1Aquatic Geomicrobiology, Institute of Ecology, Friedrich Schiller University Jena, Jena, Germany
2Department of Hydrogeology, Institute of Geosciences, Friedrich Schiller University Jena, Jena, Germany
3German Centre for Integrative Biodiversity Research (iDiv) Halle-Jena-Leipzig, Leipzig, Germany
4Institute of Geosciences, Friedrich Schiller University Jena, Jena, Germany
5U.S. Geological Survey National Research Program, Reston, VA, USA
6Department of Soil Ecology, Helmholtz Centre for Environmental Research-UFZ, Halle (Saale), Germany

Correspondence should be addressed to Kirsten Küsel; ed.anej-inu@leseuk.netsrik

Received 16 November 2016; Revised 22 February 2017; Accepted 18 April 2017; Published 13 June 2017

Academic Editor: Chuanlun Zhang

Copyright © 2017 Cassandre Sara Lazar et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. C. Griebler and T. Lueders, “Microbial biodiversity in groundwater ecosystems,” Freshwater Biology, vol. 54, no. 4, pp. 649–677, 2009. View at Publisher · View at Google Scholar · View at Scopus
  2. K. Pedersen, “Microbial life in deep granitic rock,” FEMS Microbiology Reviews, vol. 20, no. 3-4, pp. 399–414, 1997. View at Publisher · View at Google Scholar
  3. K. Takai, M. R. Mormile, J. P. McKinley et al., “Shifts in archaeal communities associated with lithological and geochemical variations in subsurface Cretaceous rock,” Environmental Microbiology, vol. 5, no. 4, pp. 309–320, 2003. View at Publisher · View at Google Scholar · View at Scopus
  4. K. Küsel, K. U. Totsche, S. E. Trumbore, R. Lehmann, C. Steinhäuser, and M. Herrmann, “How deep can surface signals be traced in the critical zone? Merging biodiversity with biogeochemistry research in a central German Muschelkalk landscape,” Frontiers in Earth Science, vol. 4, p. 32, 2016. View at Publisher · View at Google Scholar · View at Scopus
  5. A. Teske and K. B. Sorensen, “Uncultured archaea in deep marine subsurface sediments: have we caught them all?” The ISME Journal, vol. 2, no. 1, pp. 3–18, 2008. View at Publisher · View at Google Scholar · View at Scopus
  6. S. T. Bates, D. Berg-Lyons, G. Caporaso, W. A. Walters, R. Knight, and N. Fierer, “Examining the global distribution of dominant archaeal populations in soil,” The ISME Journal, vol. 5, no. 5, pp. 908–917, 2011. View at Publisher · View at Google Scholar · View at Scopus
  7. C. J. Castelle, K. C. Wrighton, B. C. Thomas et al., “Genomic expansion of domain Archaea highlights roles for organisms from new phyla in anaerobic carbon cycling,” Current Microbiology, vol. 25, no. 6, pp. 690–701, 2015. View at Publisher · View at Google Scholar · View at Scopus
  8. K. W. Seitz, C. S. Lazar, K.-U. Hinrichs, A. P. Teske, and B. J. Baker, “Genomic reconstruction of a novel, deeply branched sediment archaeal phylum with pathways for acetogenesis and sulfur reduction,” The ISME Journal, vol. 10, no. 7, pp. 1696–1705, 2016. View at Publisher · View at Google Scholar · View at Scopus
  9. B. J. Baker, J. H. Saw, A. E. Lind et al., “Genomic inference of the metabolism of cosmopolitan subsurface Archaea, Hadesarchaea,” Nature Microbiology, vol. 1, p. 16002, 2016. View at Publisher · View at Google Scholar
  10. C. Rinke, P. Schwientek, A. Sczyrba et al., “Insights into the phylogeny and coding potential of microbial dark matter,” Nature, vol. 499, no. 7459, pp. 431–437, 2013. View at Publisher · View at Google Scholar · View at Scopus
  11. S. Shimizu, M. Akiyama, Y. Ishijima, K. Hama, T. Kunimaru, and T. Naganuma, “Molecular characterization of microbial communities in fault-bordered aquifers in the Miocene formation of northernmost Japan,” Geobiology, vol. 4, no. 3, pp. 203–213, 2006. View at Publisher · View at Google Scholar · View at Scopus
  12. K. Tischer, S. Kleinsteuber, K. M. Schleinitz et al., “Microbial communities along biogeochemical gradients in a hydrocarbon-contaminated aquifer,” Environmental Microbiology, vol. 15, no. 9, pp. 2603–2615, 2013. View at Publisher · View at Google Scholar · View at Scopus
  13. S. C. Nold, H. A. Zajack, and B. A. Biddanda, “Eukaryal and archaeal diversity in a submerged sinkhole ecosystem influenced by sulfur-rich, hypoxic groundwater,” Journal of Great Lakes Research, vol. 36, no. 2, pp. 366–375, 2010. View at Publisher · View at Google Scholar · View at Scopus
  14. T. M. Flynn, R. A. Sanford, H. Ryu et al., “Functional microbial diversity explains groundwater chemistry in a pristine aquifer,” BMC Microbiology, vol. 13, no. 1, p. 146, 2013. View at Publisher · View at Google Scholar · View at Scopus
  15. A. J. Probst, T. Weinmaier, K. Raymann et al., “Biology of a widespread uncultivated archaeon that contributes to carbon fixation in the subsurface,” Nature Communications, vol. 5, p. 5497, 2014. View at Publisher · View at Google Scholar · View at Scopus
  16. G. W. Weidler, M. Dornmayr-Pfaffenhuemer, F. W. Gerbl, W. Heinen, and H. Stan-Lotter, “Communities of Archaea and bacteria in a subsurface radioactive thermal spring in the Austrian Central Alps, and evidence of ammonia-oxidizing Crenarchaeota,” Applied and Environmental Microbiology, vol. 73, no. 1, pp. 259–270, 2007. View at Publisher · View at Google Scholar · View at Scopus
  17. G. W. Weidler, F. W. Gerbl, and H. Stan-Lotter, “Crenarchaeota and their role in the nitrogen cycle in a subsurface radioactive thermal spring in the Austrian Central Alps,” Applied and Environmental Microbiology, vol. 74, no. 19, pp. 5934–5942, 2008. View at Publisher · View at Google Scholar · View at Scopus
  18. K. Takai, D. P. Moser, M. DeFlaun, T. C. Onstott, and J. K. Frederickson, “Archaeal diversity in waters from deep South African gold mines,” Applied and Environmental Microbiology, vol. 67, no. 12, pp. 5750–5760, 2001. View at Publisher · View at Google Scholar · View at Scopus
  19. C. S. Lazar, J. Dinasquet, P. Pignet, D. Prieur, and L. Toffin, “Active archaeal communities at cold seep sediments populated by Siboglinidae tubeworms from the Storegga Slide,” Microbial Ecology, vol. 60, no. 3, pp. 516–527, 2010. View at Publisher · View at Google Scholar · View at Scopus
  20. M. Herrmann, A. Hädrich, and K. Küsel, “Predominance of thaumarchaeotal ammonia abundance and transcriptional activity in an acidic fen,” Environmental Microbiology, vol. 14, no. 11, pp. 3013–3025, 2012. View at Publisher · View at Google Scholar · View at Scopus
  21. S. O. L. Direito, A. Marees, and W. F. M. Röling, “Sensitive life detection strategies for low-biomass environments: optimizing extraction of nucleic acids adsorbing to terrestrial and Mars analogue minerals,” FEMS Microbiology Ecology, vol. 81, no. 1, pp. 111–123, 2012. View at Publisher · View at Google Scholar · View at Scopus
  22. D. D. I. F. Normung, DIN EN 1484: Wasseranalytik - Anleitungen zur Bestimmung des gesamten organischen Kohlenstoffs (TOC) und des gelösten organischen Kohlenstoffs (DOC), Beuth Verlag GmbH, Berlin, 1997.
  23. H. A. Barton, N. M. Taylor, B. R. Lubbers, and A. C. Pemberton, “DNA extraction from low-biomass carbonate rock: an improved method with reduced contamination and the low-biomass contaminant database,” Journal of Microbiological Methods, vol. 66, no. 1, pp. 21–31, 2006. View at Publisher · View at Google Scholar · View at Scopus
  24. J. D. Neufeld, J. Vohra, M. G. Dumont et al., “DNA stable-isotope probing,” Nature Protocols, vol. 2, no. 4, pp. 860–866, 2007. View at Publisher · View at Google Scholar · View at Scopus
  25. L. Ovreas, L. Forney, F. L. Daae, and V. Torsvik, “Distribution of bacterioplankton in meromictic Lake Saelenvannet, as determined by denaturing gradient gel electrophoresis of PCR-amplified gene fragments coding for 16S rRNA,” Applied and Environmental Microbiology, vol. 63, no. 9, pp. 3367–3373, 1997. View at Google Scholar
  26. D. A. Stahl and R. Amann, “Development and application of nucleic acid probes,” in Nucleic Acid Techniques in Bacterial Systematics, M. G. E. Stackebrandt, Ed., John Wiley, New York, 1991. View at Google Scholar
  27. L. Durand, M. Zbinden, V. Cueff-Gauchard et al., “Microbial diversity associated with the hydrothermal shrimp Rimicaris exoculata gut and occurrence of a resident microbial community,” FEMS Microbiology Ecology, vol. 71, no. 2, pp. 291–303, 2010. View at Publisher · View at Google Scholar · View at Scopus
  28. D. J. Lane, “16S/23S rRNA sequencing,” in Nucleic Acid Techniques in Bacterial Systematics, E. S. a. M. a. Goodfellow, Ed., pp. 115–175, John Wiley and Sons, New York, 1991. View at Google Scholar
  29. P. D. Schloss, S. L. Westcott, T. Ryabin et al., “Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities,” Applied and Environmental Microbiology, vol. 75, no. 33, pp. 7537–7541, 2009. View at Publisher · View at Google Scholar · View at Scopus
  30. C. Quast, E. Pruesse, P. Yilmaz et al., “The SILVA ribosomal RNA gene database project: improved data processing and web-based tools,” Nucleic Acids Research, vol. 41, no. Database issue, pp. D590–D596, 2013. View at Publisher · View at Google Scholar · View at Scopus
  31. W. Ludwig, O. Strunk, R. Westram et al., “ARB: a software environment for sequence data,” Nucleic Acids Research, vol. 32, no. 4, pp. 1363–1371, 2004. View at Publisher · View at Google Scholar · View at Scopus
  32. T. R Development Core, R: A Language and Environment for Statistical Computing, R Foundation for Statistical Computing, Vienna, Austria, 2008, ISBN 3-900051-07-0.
  33. R. Suzuki and H. Shimodaira, “Pvclust: an R package for assessing the uncertainty in hierarchical clustering,” Bioinformatics, vol. 22, no. 12, pp. 1540–1542, 2006. View at Publisher · View at Google Scholar · View at Scopus
  34. A. Nawaz, W. Purahong, R. Lehmann et al., “Superimposed pristine limestone aquifers with marked hydrochemical differences exhibit distinct fungal communities,” Frontiers in Microbiology, vol. 7, p. 666, 2016. View at Publisher · View at Google Scholar · View at Scopus
  35. N. H. Youssef, C. Rinke, R. Stepanauskas, I. Farag, T. Woyke, and M. S. Elshahed, “Insights into the metabolism, lifestyle and putative evolutionary history of the novel archaeal phylum ‘Diapherotrites’,” The ISME Journal, vol. 9, no. 2, pp. 447–460, 2015. View at Publisher · View at Google Scholar · View at Scopus
  36. C. Lazar, B. Baker, K. Seitz, and A. Teske, “Genomic reconstruction of multiple lineages of uncultured benthic archaea suggests distinct biogeochemical roles and ecological niches,” The ISME Journal, vol. 11, no. 4, p. 1058, 2017. View at Publisher · View at Google Scholar
  37. M. Könneke, A. E. Bernhard, J. R. de la Torre, C. B. Walker, J. B. Waterbury, and D. A. Stahl, “Isolation of an autotrophic ammonia-oxidizing marine archaeon,” Nature, vol. 437, no. 7058, pp. 543–546, 2005. View at Publisher · View at Google Scholar · View at Scopus
  38. S. Opitz, K. Küsel, O. Spott, K. U. Totsche, and M. Herrmann, “Oxygen availability and distance to surface environments determine community composition and abundance of ammonia-oxidizing prokaroytes in two superimposed pristine limestone aquifers in the Hainich region, Germany,” FEMS Microbiology Ecology, vol. 90, no. 1, pp. 39–53, 2014. View at Publisher · View at Google Scholar · View at Scopus
  39. T. Lundell, A. Leonowicz, J. Rogalski, and A. Hatakka, “Formation and action of lignin-modifying enzymes in cultures of Phlebia radiata supplemented with veratric acid,” Applied and Environmental Microbiology, vol. 56, no. 9, pp. 2623–2629, 1990. View at Google Scholar
  40. C. C. Ouverney and J. A. Fuhrman, “Marine planktonic Archaea take up amino acids,” Applied and Environmental Microbiology, vol. 66, no. 11, pp. 4829–4833, 2000. View at Publisher · View at Google Scholar · View at Scopus
  41. C. B. Walker, J. R. de la Torre, M. G. Klotz et al., “Nitrosopumilus maritimus genome reveals unique mechanisms for nitrification and autotrophy in globally distributed marine Crenarchaea,” Proceedings of the National Academy of Sciences of the United States of America, vol. 107, no. 19, pp. 8818–8823, 2010. View at Publisher · View at Google Scholar · View at Scopus
  42. T. Stevens, “Lithoautotrophy in the subsurface,” FEMS Microbiology Ecology, vol. 20, no. 3-4, pp. 327–337, 1997. View at Google Scholar
  43. A. Alfreider and C. Vogt, “Genetic evidence for bacterial chemolithoautotrophy based on the reductive tricarboxylic acid cycle in groundwater systems,” Microbes and Environments, vol. 27, no. 2, pp. 209–214, 2012. View at Publisher · View at Google Scholar · View at Scopus
  44. C. Kellermann, D. Selesi, N. Lee et al., “Microbial CO2 fixation potential in a tar-oil-contaminated porous aquifer,” FEMS Microbiology Ecology, vol. 81, no. 1, pp. 172–187, 2012. View at Publisher · View at Google Scholar · View at Scopus
  45. K. C. Wrighton, B. C. Thomas, I. Sharon et al., “Fermentation, hydrogen, and sulfur metabolism in multiple uncultivated bacterial phyla,” Science, vol. 337, no. 6102, pp. 1661–1665, 2012. View at Publisher · View at Google Scholar · View at Scopus
  46. M. Herrmann, A. Rusznyák, D. M. Akob et al., “Large fractions of CO2-fixing microorganisms in pristine limestone aquifers appear to be involved in the oxidation of reduced sulfur and nitrogen compounds,” Applied and Environmental Microbiology, vol. 81, no. 7, pp. 2384–2394, 2015. View at Publisher · View at Google Scholar · View at Scopus
  47. C. S. Lazar, B. J. Baker, K. Seitz et al., “Genomic evidence for distinct carbon substrate preferences and ecological niches of Bathyarchaeota in estuarine sediments,” Environmental Microbiology, vol. 18, no. 4, pp. 1200–1211, 2016. View at Publisher · View at Google Scholar · View at Scopus
  48. L. E. Lehtovirta-Morley, K. Stoecker, A. Vilcinskas, J. I. Prosser, and G. W. Nicol, “Cultivation of an obligate acidophilic ammonia oxidizer from a nitrifying acid soil,” Proceedings of the National Academy of Sciences of the United States of America, vol. 208, no. 38, pp. 15892–15897, 2011. View at Publisher · View at Google Scholar · View at Scopus
  49. M. Könneke, D. M. Schubert, P. C. Brown et al., “Ammonia-oxidizing Archaea use the most energy efficient aerobic pathway for CO2 fixation,” Proceedings of the National Academy of Sciences of the United States of America, vol. 111, no. 22, pp. 8239–8244, 2014. View at Publisher · View at Google Scholar · View at Scopus
  50. I. A. Berg, “Ecological aspects of the distribution of different autotrophic CO2 fixation pathways,” Applied and Environmental Microbiology, vol. 77, no. 6, pp. 1925–1936, 2011. View at Publisher · View at Google Scholar · View at Scopus
  51. I. A. Berg, D. Kockelkorn, W. H. Ramos Vera et al., “Autotrophic carbon fixation in Archaea,” Nature Reviews, vol. 8, no. 6, pp. 447–460, 2010. View at Publisher · View at Google Scholar · View at Scopus
  52. M. Tourna, M. Stieglmeier, A. Spang et al., “Nitrososphaera viennensis, an ammonia oxidizing archaeon from soil,” Proceedings of the National Academy of Sciences of the United States of America, vol. 108, no. 20, pp. 8420–8425, 2011. View at Publisher · View at Google Scholar · View at Scopus
  53. A. Spang, A. Poehlein, P. Offre et al., “The genome of the ammonia-oxidizing Candidatus Nitrososphaera gargensis: insights into metabolic versatility and environmental adaptations,” Environmental Microbiology, vol. 14, no. 12, pp. 3122–3145, 2012. View at Publisher · View at Google Scholar · View at Scopus
  54. R. Hatzenpichler, E. V. Lebedeva, E. Spieck et al., “A moderately thermophilic ammonia-oxidizing crenarchaeote from a hot spring,” Proceedings of the National Academy of Sciences of the United States of America, vol. 105, no. 6, pp. 2134–2139, 2008. View at Publisher · View at Google Scholar · View at Scopus