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Research Article

Microbiome of the upper troposphere: Species composition and prevalence, effects of tropical storms, and atmospheric implications

Natasha DeLeon-Rodriguez, Terry L. Lathem, Luis M. Rodriguez-R, James M. Barazesh, Bruce E. Anderson, Andreas J. Beyersdorf, Luke D. Ziemba, Michael Bergin, Athanasios Nenes, and Konstantinos T. Konstantinidis
  1. aSchool of Biology,
  2. bSchool of Earth and Atmospheric Sciences,
  3. cSchool of Civil and Environmental Engineering,
  4. eSchool of Chemical and Biomolecular Engineering, Georgia Institute of Technology, Atlanta, GA 30332; and
  5. dChemistry and Dynamics Branch/Science Directorate, National Aeronautics and Space Administration Langley Research Center, Hampton, VA 23681

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PNAS February 12, 2013 110 (7) 2575-2580; https://doi.org/10.1073/pnas.1212089110
Natasha DeLeon-Rodriguez
aSchool of Biology,
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Terry L. Lathem
bSchool of Earth and Atmospheric Sciences,
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Luis M. Rodriguez-R
aSchool of Biology,
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James M. Barazesh
cSchool of Civil and Environmental Engineering,
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Bruce E. Anderson
dChemistry and Dynamics Branch/Science Directorate, National Aeronautics and Space Administration Langley Research Center, Hampton, VA 23681
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Andreas J. Beyersdorf
dChemistry and Dynamics Branch/Science Directorate, National Aeronautics and Space Administration Langley Research Center, Hampton, VA 23681
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Luke D. Ziemba
dChemistry and Dynamics Branch/Science Directorate, National Aeronautics and Space Administration Langley Research Center, Hampton, VA 23681
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Michael Bergin
bSchool of Earth and Atmospheric Sciences,
cSchool of Civil and Environmental Engineering,
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Athanasios Nenes
bSchool of Earth and Atmospheric Sciences,
eSchool of Chemical and Biomolecular Engineering, Georgia Institute of Technology, Atlanta, GA 30332; and
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  • For correspondence: kostas@ce.gatech.edu athanasios.nenes@gatech.edu
Konstantinos T. Konstantinidis
aSchool of Biology,
cSchool of Civil and Environmental Engineering,
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  • For correspondence: kostas@ce.gatech.edu athanasios.nenes@gatech.edu
  1. Edited by W. Ford Doolittle, Dalhousie University, Halifax, NS, Canada, and approved December 19, 2012 (received for review July 15, 2012)

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Abstract

The composition and prevalence of microorganisms in the middle-to-upper troposphere (8–15 km altitude) and their role in aerosol-cloud-precipitation interactions represent important, unresolved questions for biological and atmospheric science. In particular, airborne microorganisms above the oceans remain essentially uncharacterized, as most work to date is restricted to samples taken near the Earth’s surface. Here we report on the microbiome of low- and high-altitude air masses sampled onboard the National Aeronautics and Space Administration DC-8 platform during the 2010 Genesis and Rapid Intensification Processes campaign in the Caribbean Sea. The samples were collected in cloudy and cloud-free air masses before, during, and after two major tropical hurricanes, Earl and Karl. Quantitative PCR and microscopy revealed that viable bacterial cells represented on average around 20% of the total particles in the 0.25- to 1-μm diameter range and were at least an order of magnitude more abundant than fungal cells, suggesting that bacteria represent an important and underestimated fraction of micrometer-sized atmospheric aerosols. The samples from the two hurricanes were characterized by significantly different bacterial communities, revealing that hurricanes aerosolize a large amount of new cells. Nonetheless, 17 bacterial taxa, including taxa that are known to use C1–C4 carbon compounds present in the atmosphere, were found in all samples, indicating that these organisms possess traits that allow survival in the troposphere. The findings presented here suggest that the microbiome is a dynamic and underappreciated aspect of the upper troposphere with potentially important impacts on the hydrological cycle, clouds, and climate.

  • ice nucleation
  • cloud condensation nuclei
  • microbial community
  • pyrosequencing
  • biogeography

Footnotes

  • ↵1To whom correspondence may be addressed. E-mail: kostas{at}ce.gatech.edu or athanasios.nenes{at}gatech.edu.
  • Author contributions: A.N. and K.T.K. designed research; N.D.-R., T.L.L., L.M.R.-R., J.M.B., A.N., and K.T.K. performed research; N.D.-R., T.L.L., J.M.B., B.E.A., A.J.B., L.D.Z., and M.B. contributed new reagents/analytic tools; N.D.-R., T.L.L., L.M.R.-R., and L.D.Z. analyzed data; and N.D.-R., A.N., and K.T.K. wrote the paper.

  • The authors declare no conflict of interest.

  • This article is a PNAS Direct Submission.

  • Data deposition: The sequence reported in this paper has been deposited in the Short Read Archive database (accession no. SRA056067).

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1212089110/-/DCSupplemental.

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Microbiome of the upper troposphere
Natasha DeLeon-Rodriguez, Terry L. Lathem, Luis M. Rodriguez-R, James M. Barazesh, Bruce E. Anderson, Andreas J. Beyersdorf, Luke D. Ziemba, Michael Bergin, Athanasios Nenes, Konstantinos T. Konstantinidis
Proceedings of the National Academy of Sciences Feb 2013, 110 (7) 2575-2580; DOI: 10.1073/pnas.1212089110

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Microbiome of the upper troposphere
Natasha DeLeon-Rodriguez, Terry L. Lathem, Luis M. Rodriguez-R, James M. Barazesh, Bruce E. Anderson, Andreas J. Beyersdorf, Luke D. Ziemba, Michael Bergin, Athanasios Nenes, Konstantinos T. Konstantinidis
Proceedings of the National Academy of Sciences Feb 2013, 110 (7) 2575-2580; DOI: 10.1073/pnas.1212089110
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