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Archaeal dominance in the mesopelagic zone of the Pacific Ocean

Nature volume 409, pages 507–510 (2001)Cite this article

Abstract

The ocean's interior is Earth's largest biome. Recently, cultivation-independent ribosomal RNA gene surveys have indicated a potential importance for archaea1 in the subsurface ocean2,3,4. But quantitative data on the abundance of specific microbial groups in the deep sea are lacking5,6. Here we report a year-long study of the abundance of two specific archaeal groups (pelagic euryarchaeota and pelagic crenarchaeota)2 in one of the ocean's largest habitats. Monthly sampling was conducted throughout the water column (surface to 4,750 m) at the Hawai'i Ocean Time-series station7. Below the euphotic zone (> 150 m), pelagic crenarchaeota comprised a large fraction of total marine picoplankton, equivalent in cell numbers to bacteria at depths greater than 1,000 m. The fraction of crenarchaeota increased with depth, reaching 39% of total DNA-containing picoplankton detected. The average sum of archaea plus bacteria detected by rRNA-targeted fluorescent probes ranged from 63 to 90% of total cell numbers at all depths throughout our survey. The high proportion of cells containing significant amounts of rRNA suggests that most pelagic deep-sea microorganisms are metabolically active. Furthermore, our results suggest that the global oceans harbour approximately 1.3 × 1028 archaeal cells, and 3.1 × 1028 bacterial cells. Our data suggest that pelagic crenarchaeota represent one of the ocean's single most abundant cell types.

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Figure 1: Contour plots of relative abundances with depth of bacteria and pelagic crenarchaeota during a 1-yr sampling effort at the Hawai'i Ocean Time-series station, ALOHA, in the North Pacific subtropical gyre.
Figure 2: Mean annual depth profiles of microbial domains in the North Pacific subtropical gyre.
Figure 3: Mean annual depth profiles of microbial domains in the North Pacific subtropical gyre.

References

  1. Woese, C. R., Kandler, O. & Wheelis, M. L. Towards a natural system of organisms: Proposal for the domains Archaea, Bacteria, and Eucarya. Proc. Natl Acad. Sci. USA 87, 4576–4579 ( 1990).

    ADS  CAS  PubMed  PubMed Central  Google Scholar 

  2. DeLong, E. F. Archaea in coastal marine environments. Proc. Natl Acad. Sci. USA 89, 5685–5689 ( 1992).

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  3. Fuhrman, J. A., McCallum, K. & Davis, A. A. Novel major archaebacterial group from marine plankton. Nature 356, 148–149 (1992).

    Article  ADS  CAS  PubMed  Google Scholar 

  4. Fuhrman, J. A. & Davis, A. A. Widespread Archaea and novel Bacteria from the deep sea as shown by 16S rRNA gene sequences. Mar. Ecol. Prog. Ser. 150, 275–285 (1997).

    Article  ADS  Google Scholar 

  5. Fuhrman, J. A. & Ouverney, C. C. Marine microbial diversity studies via 16S rRNA sequences: cloning results from coastal waters and counting of native archaea with fluorescent single probes. Aquat. Ecol. 32, 3–15 (1998).

    Article  CAS  Google Scholar 

  6. DeLong, E. F., Taylor, L. T., Marsh, T. L. & Preston, C. M. Visualization and enumeration of marine planktonic Archaea and Bacteria by using polyribonucleotide probes and fluorescent in situ hybridization. Appl. Environ. Microbiol. 65, 5554–5563 (1999).

    CAS  PubMed  PubMed Central  Google Scholar 

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

    ADS  CAS  Google Scholar 

  8. Porter, K. & Feig, Y. S. The use of DAPI for identifying and counting aquatic microflora. Limnol. Oceanogr. 25, 943–948 (1980).

    Article  ADS  Google Scholar 

  9. Hicks, R. E., Amann, R. I. & Stahl, D. A. Dual staining of natural bacterioplankton with 4′, 6-diamidino-2-phenylindole and fluorescent oligonucleotide probes targeting kingdom-level 16S rRNA sequences. Appl. Environ. Microbiol. 58, 2158–2163 (1992).

    CAS  PubMed  PubMed Central  Google Scholar 

  10. Massana, R., Murray, A. E., Preston, C. M. & DeLong, E. F. Vertical distribution and phylogenetic characterization of marine planktonic Archaea in the Santa Barbara Channel. Appl. Environ. Microbiol. 63, 50–56 ( 1997).

    CAS  PubMed  PubMed Central  Google Scholar 

  11. Murray, A. E. et al. A time series assessment of planktonic archaeal variability in the Santa Barbara Channel. Aquat. Microb. Ecol. 20, 129–145 (1999).

    Article  Google Scholar 

  12. Olsen, G. J. Archaea, archaea everywhere. Nature 371, 657–658 (1994).

    Article  ADS  CAS  PubMed  Google Scholar 

  13. Stein, J. L. & Simon, M. I. Archaeal ubiquity. Proc. Natl Acad. Sci. USA 93, 6228– 6230 (1996).

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  14. DeLong, E., Wu, K. Y., Prézlin, B. B. & Jovine, R. V. M. High abundance of Archaea in Antarctic marine picoplankton. Nature 371, 695–697 ( 1994).

    Article  ADS  CAS  PubMed  Google Scholar 

  15. Massana, R. et al. Vertical distribution and temporal variation of marine planktonic Archaea in the Gerlache strait, Antarctica, during early spring. Limnol. Oceanogr. 43, 607–617 (1998).

    Article  ADS  CAS  Google Scholar 

  16. Amann, R. I., Krumholz, L. & Stahl, D. A. Fluorescent-oligonucleotide probing of whole cells for determinative, phylogenetic, and environmental studies in microbiology. J. Bacteriol. 172, 762– 770 (1990).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Lee, S. & Kemp, P. F. Single-cell RNA content of natural marine planktonic bacteria measured by hybridization with multiple 16S rRNA-targeted fluorescent probes. Limnol. Oceanogr. 39, 869–879 (1994).

    Article  ADS  CAS  Google Scholar 

  18. Murray, A. E. et al. Seasonal and spatial variability of bacterial and archaeal assemblages in the coastal waters near Anvers island, Antarctica. Appl. Environ. Microbiol. 64, 2585– 2595 (1998).

    CAS  PubMed  PubMed Central  Google Scholar 

  19. Glöckner, F. O., Fuchs, B. M. & Amann, R. Bacterioplankton compositions of lakes and oceans: a first comparison based on fluorescence in situ hybridization. Appl. Environ. Microbiol. 65, 3721– 3726 (1999).

    PubMed  PubMed Central  Google Scholar 

  20. Simon, M., Glöckner, F. O. & Amann, R. Different community structure and temperature optima of heterotrophic picoplankton in various regions of the Southern Ocean. Aquat. Microb. Ecol. 18, 275–284 (1999).

    Article  Google Scholar 

  21. Nagata, T., Fukuda, H., Fukuda, R. & Koike, I. Bacterioplankton distribution and production in deep Pacific waters: Large-scale geographic variations and possible coupling with sinking particle fluxes. Limnol. Oceanogr. 45, 426–435 (2000).

    Article  ADS  CAS  Google Scholar 

  22. Courties, C. et al. Smallest eukaryotic organism. Nature 370, 255 (1994).

    Article  ADS  Google Scholar 

  23. Zweifel, U. L. & Hagström, Å. Total counts of marine bacteria include a large fraction of non-nucleoid-containing bacteria (ghosts). Appl. Environ. Microbiol. 61, 2180–2185 (1995).

    CAS  PubMed  PubMed Central  Google Scholar 

  24. Karner, M. & Fuhrman, J. Determination of active marine bacterioplankton: a comparison of universal 16S rRNA probes, autoradiography, and nucleoid staining. Appl. Environ. Microbiol. 63, 1208– 1213 (1997).

    CAS  PubMed  PubMed Central  Google Scholar 

  25. Williams, P. M., Carlucci, A. F. & Olson, R. A deep profile of some biologically important properties in the central North Pacific gyre. Oceanol. Acta 3, 471–476 (1980).

    Google Scholar 

  26. Menard, H. W. & Smith, S. M. Hypsometry of ocean basin provinces. J. Geophys. Res. 71, 4305– 4325 (1966).

    Article  ADS  Google Scholar 

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Acknowledgements

We thank the crew of the RV Moana Wave, L. Tupas and K. Björkman for help with sampling. T. Taylor helped standardizing probing protocols, and L. Fujieki provided computational support. This study was supported by NOAA-Seagrant Office (MBK/DMK), NSF (DMK), and support from the David and Lucile Packard Foundation (EFD). This is SOEST contribution number 5313 and US JGOFS contribution number 647.

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Authors and Affiliations

  1. Department of Oceanography, University of Hawai'i, 1000 Pope Road, Honolulu, 96822, Hawai'i, USA

    Markus B. Karner & David M. Karl

  2. Monterey Bay Aquarium Research Institute , 7700 Sandholdt Road, Moss Landing, 95039, California, USA

    Edward F. DeLong

Authors
  1. Markus B. Karner
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  2. Edward F. DeLong
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  3. David M. Karl
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Correspondence to Markus B. Karner.

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Karner, M., DeLong, E. & Karl, D. Archaeal dominance in the mesopelagic zone of the Pacific Ocean. Nature 409, 507–510 (2001). https://doi.org/10.1038/35054051

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