Microbial formation of labile organic carbon in Antarctic glacial environments

Journal name:
Nature Geoscience
Volume:
10,
Pages:
356–359
Year published:
DOI:
doi:10.1038/ngeo2925
Received
Accepted
Published online

Abstract

Roughly six petagrams of organic carbon are stored within ice worldwide. This organic carbon is thought to be of old age and highly bioavailable. Along with storage of ancient and new atmospherically deposited organic carbon, microorganisms may contribute substantially to the glacial organic carbon pool. Models of glacial microbial carbon cycling vary from net respiration to net carbon fixation. Supraglacial streams have not been considered in models although they are amongst the largest ecosystems on most glaciers and are inhabited by diverse microbial communities. Here we investigate the biogeochemical sequence of organic carbon production and uptake in an Antarctic supraglacial stream in the McMurdo Dry Valleys using nanometre-scale secondary ion mass spectrometry, fluorescence spectroscopy, stable isotope analysis and incubation experiments. We find that heterotrophic production relies on highly labile organic carbon freshly derived from photosynthetic bacteria rather than legacy organic carbon. Exudates from primary production were utilized by heterotrophs within 24h, and supported bacterial growth demands. The tight coupling of microbially released organic carbon and rapid uptake by heterotrophs suggests a dynamic local carbon cycle. Moreover, as temperatures increase there is the potential for positive feedback between glacial melt and microbial transformations of organic carbon.

At a glance

Figures

  1. Microbial uptake of in situ released organic matter.
    Figure 1: Microbial uptake of in situ released organic matter.

    a,b, Example of cells analysed. a, Epifluorescence overlay confirming identification of Polaromonas sp. cells hybridized with HRP-labelled Pomo828 oligonucleotide probe (green signal). b, NanoSIMS 13C/12C isotope ratio image of cells enriched in 13C-labelled exudates; white lines indicate regions of interest used for calculating 13C/12C ratios. c,d, Summary boxplots of nanoSIMS analyses in atom% (AT%) (c) and in fmol C cell−1d−1 (d) for Alphaproteobacteria, Bacteroidetes, Betaproteobacteria and Polaromonas sp. Whiskers represent the 25th and 75th percentile (lower and upper quartiles, respectively); the mean is a solid line with outliers represented by a filled black circle.

  2. Organic carbon cycling in supraglacial environments.
    Figure 2: Organic carbon cycling in supraglacial environments.

    Schematic depicting sources and sinks of OC on glaciers. Four major compartments of supraglacial OC cycling are shown: cryoconites, aeolian deposition, in-ice processes and in-stream cycling. The first step in the supraglacial microbial loop (represented by spirals) is the fixation of atmospheric CO2 by photoautotrophic microorganisms; this fixed OC is released (brown cloud) and successively taken up by heterotrophic organisms. OC utilized by microorganisms is either partially or completely photo-oxidized or biologically oxidized to CO2. In-stream arrows represent OC being transported downstream with eventual export to the oceans.

References

  1. Hood, E. et al. Glaciers as a source of ancient and labile organic matter to the marine environment. Nat. Geosci. 462, 10441047 (2009).
  2. Stubbins, A. et al. Anthropogenic aerosols as a source of ancient dissolved organic matter in glaciers. Nat. Geosci. 5, 198201 (2012).
  3. Singer, G. A. et al. Biogeochemically diverse organic matter in Alpine glaciers and its downstream fate. Nat. Geosci. 5, 710714 (2012).
  4. Bhatia, M. P. et al. Organic carbon export from the Greenland ice sheet. Geochim. Cosmochim. Acta 109, 329344 (2013).
  5. Antony, R. et al. Origin and sources of dissolved organic matter in snow on the East Antarctic ice sheet. Environ. Sci. Technol. 48, 61516159 (2014).
  6. Smith, H. J. et al. Biofilms on glacial surfaces: hotspots for biological activity. NPJ Biofilms Microbiomes 2, 16008 (2016).
  7. Cook, J., Edwards, A., Takeuchi, N. & Irvine-Fynn, T. Cryoconite: the dark biological secret of the cryosphere. Prog. Phys. Geogr. 40, 66111 (2016).
  8. Anesio, A. M., Hodson, A. J. & Fritz, A. High microbial activity on glaciers: importance to the global carbon cycle. Glob. Change Biol. 15, 955960 (2009).
  9. Li, F., Ginoux, P. & Ramaswamy, V. Distribution, transport, and deposition of mineral dust in the Southern Ocean and Antarctica: contribution of major sources. J. Geophys. Res. 113 (2008).
  10. Bauer, S. E. et al. Historical and future black carbon deposition on the three ice caps: ice core measurements and model simulations from 1850 to 2100. J. Geophys. Res. 118, 79487961 (2013).
  11. Stibal, M., Sabacka, M. & Zarsky, J. Biological processes on glacier and ice sheet surfaces. Nat. Geosci. 5, 771774 (2012).
  12. Sanclements, M. D. et al. Biogeophysical properties of an expansive Antarctic supraglacial stream. Ant. Sci. 29, 3344 (2017).
  13. Foreman, C. M. et al. Microbial growth under humic-free conditions in a supraglacial stream system on the Cotton Glacier, Antarctica. Environ. Res. Lett. 8, 035022 (2013).
  14. Barker, J. D., Dubnick, A., Lyons, W. B. & Chin, Y. P. Changes in dissolved organic matter (DOM) fluorescence in proglacial Antarctic streams. Arct. Ant. Alp. Res. 45, 305317 (2013).
  15. Ogawa, H., Amagai, Y., Koike, I., Kaiser, K. & Benner, R. Production of refractory dissolved organic matter by bacteria. Science 292, 917920 (2001).
  16. Teira, E., Pazó, M. J. & Serret, P. Dissolved organic carbon production by microbial populations in the Atlantic Ocean. Limnol. Oceanogr. 46, 13701377 (2001).
  17. Coveney, M. F. Bacterial uptake of photosynthetic carbon from freshwater phytoplankton. Oikos 38, 820 (1982).
  18. Van den Meersche, K. & Middelburg, J. J. Carbon-nitrogen coupling and algal-bacterial interactions during an experimental bloom: modeling a 13C tracer experiment. Limnol. Oceanogr. 49, 862878 (2004).
  19. Takacs, C. D., Priscu, J. C. & McKnight, D. M. Bacterial dissolved organic carbon demand in McMurdo Dry Valley lakes, Antarctica. Limnol. Oceanogr. 46, 11891194 (2001).
  20. Suttle, C. A. Marine viruses—major players in the global ecosystem. Nat. Rev. Microbiol. 5, 801812 (2007).
  21. Säwström, C., Lisle, J., Anesio, A. M., Priscu, J. C. & Laybourn-Parry, J. Bacteriophage in polar inland waters. Extremophiles 12, 167175 (2008).
  22. Wigington, C. H. Re-examination of the relationship between marine virus and microbial cell abundances. Nature 1, 15024 (2016).
  23. Säwström, C., Anesio, M. A., Granéli, W. & Laybourn-Parry, J. Seasonal viral loop dynamics in two large ultraoligotrophic Antarctic freshwater lakes. Microb. Ecol. 53, 111 (2007).
  24. Boetius, A., Anesio, A. M., Deming, J. W., Mikucki, J. A. & Rapp, J. Z. Microbial ecology of the cryosphere: sea ice and glacial habitats. Nat. Rev. Microbiol. (2015).
  25. Musat, N. et al. The effect of FISH and CARD-FISH on the isotopic composition of 13C- and 15N-labeled Pseudomonas putida cells measured by nanoSIMS. Syst. Appl. Microbiol. 37, 267276 (2014).
  26. Langley, E. S., Leeson, A. A., Stokes, C. R. & Jamieson, S. S. R. Seasonal evolution of supraglacial lakes on an East Antarctic outlet glacier. Sci. Invest. Rep. 43, 85638571 (2016).
  27. Priscu, J. C. & Christner, B. C. Microbial Diversity and Bioprospecting (ed. Bull, A.) (ASM Press, 2004).
  28. Kohler, T. J. et al. Life in the main channel: long-term hydrologic control of microbial mat abundance in McMurdo Dry Valley streams, Antarctica. Ecosystems 18, 310327 (2015).
  29. Hood, E., Battin, T. J., Fellman, J., O’Neel, S. & Spencer, R. G. M. Storage and release of organic carbon from glaciers and ice sheets. Nat. Geosci. 8, 9196 (2015).
  30. Kuipers Munneke, P., Picard, G., Broeke den, M. R., Lenaerts, J. T. M. & Meijgaard, E. Insignificant change in Antarctic snowmelt volume since 1979. Sci. Invest. Rep. 39 (2012).
  31. Hodson, A. et al. The cryoconite ecosystem on the Greenland ice sheet. Ann. Glaciol. 51, 123129 (2010).
  32. Kirchman, D., K’nees, E. & Hodson, R. Leucine incorporation and its potential as a measure of protein synthesis by bacteria in natural aquatic systems. Appl. Environ. Microbiol. 49, 599607 (1985).
  33. Lizotte, M. P., Sharp, T. R. & Priscu, J. C. Phytoplankton dynamics in the stratified water column of Lake Bonney, Antarctica. Polar Biol. 16, 155162 (1996).
  34. Vick, T. J. & Priscu, J. C. Bacterioplankton productivity in lakes of the Taylor Valley, Antarctica, during the polar night transition. Aquat. Microb. Ecol. 68, 7790 (2012).
  35. Musat, N. et al. A single-cell view on the ecophysiology of anaerobic phototrophic bacteria. Proc. Natl Acad. Sci. USA 105, 1786117866 (2008).
  36. Pernthaler, A. et al. Sensitive multi-color fluorescence in situ hybridization for the identification of environmental microorganisms. Mol. Microb. Ecol. Manual 2, 711725 (2004).
  37. Pernthaler, A., Pernthaler, J. & Amann, R. Fluorescence in situ hybridization and catalyzed reporter deposition for the identification of marine bacteria. Appl. Environ. Microbiol. 68, 30943101 (2002).
  38. Polerecky, L. Look@NanoSIMS–a tool for the analysis of nanoSIMS data in environmental microbiology. Environ. Microbiol. 14, 10091023 (2012).
  39. Foster, R. A. et al. Nitrogen fixation and transfer in open ocean diatom–cyanobacterial symbioses. ISME J. 5, 14841493 (2011).
  40. R Development Core Team R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2008); http://www.R-project.org
  41. Coble, P. G. Characterization of marine and terrestrial DOM in seawater using excitation-emission matrix spectroscopy. 51, 325346 (1996).
  42. McKnight, D. M., Boyer, E. W. & Westerhoff, P. K. Spectrofluorometric characterization of dissolved organic matter for indication of precursor organic material and aromaticity. Limnol. Oceanogr. 46, 3848 (2001).
  43. Brussaard, C. P. D. Optimization of procedures for counting viruses by flow cytometry. Appl. Environ. Microbiol. 70, 15061513 (2004).

Download references

Author information

Affiliations

  1. Center for Biofilm Engineering, Montana State University, Bozeman, Montana 59717, USA

    • H. J. Smith &
    • C. M. Foreman
  2. Land Resources and Environmental Sciences, Montana State University, Bozeman, Montana 59717, USA

    • H. J. Smith
  3. Department of Ecology, Environment, and Plant Sciences, Stockholm University, Stockholm 10691, Sweden

    • R. A. Foster
  4. Department of Biogeochemistry, Max Planck Institute for Marine Microbiology, Bremen 28359, Germany

    • R. A. Foster,
    • S. Littmann &
    • M. M. M. Kuypers
  5. INSTAAR, University of Colorado, Boulder, Colorado 80309, USA

    • D. M. McKnight
  6. US Geological Survey, St Petersburg Coastal & Marine Science Center, St Petersburg, Florida 33701, USA

    • J. T. Lisle
  7. Chemical and Biological Engineering, Montana State University, Bozeman, Montana 59717, USA

    • C. M. Foreman

Contributions

H.J.S., C.M.F. and R.A.F. conceived and designed experiments. H.J.S., C.M.F., S.L. and J.T.L. performed the experiments. H.J.S., C.M.F., R.A.F., S.L., D.M.M. and J.T.L. analysed the data. C.M.F., J.T.L. and M.M.M.K. contributed materials/analysis tools. H.J.S., C.M.F., R.A.F. and D.M.M. wrote the paper.

Competing financial interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to:

Author details

Supplementary information

PDF files

  1. Supplementary Information (2,400 KB)

    Supplementary Information

Additional data