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

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.

Fig. 1.

Quantification of bacterial and fungal cells in samples from high altitudes in the atmosphere. Concentration of bacterial (A) and fungal (B) cells based on qPCR analysis of SSU rRNA gene copies in the samples. Note that samples are ordered by the collection time on the x axis except for blank samples, which are shown at the rightmost part of the graphs in light gray. (C) Live/dead microscopy image of two samples from the California coast and transit flights. Green-stained cells represent cells with viable/intact membrane (e.g., cell indicated by left arrow), and red/yellow-stained cells represent cells with a damaged membrane (e.g., cell indicated by right arrow).

Fig. 2.

Composition of tropospheric bacterial communities. (A) Relative abundance (y axis) of taxa (see key) represented by the partial SSU rRNA gene sequences recovered in each sample (x axis). Black vertical lines next to the bars underline the core OTUs that are present in all samples. “*Others” refers to low-abundance OTUs; for a complete list of the OTUs grouped under “*Others,” refer to SI Appendix, Table S3. (B) Principal coordinates analysis based on the β-diversity values calculated by the weighted UniFrac distance metric of samples collected during the GRIP campaign and samples from previous studies (see key). Samples from this study are represented with open and closed squares and color-coded as follows: red, California/transit; blue, clouds; purple, low altitude; green, Hurricane Earl; orange, Hurricane Karl.

Fig. 3.

Habitat of origin of the SSU rRNA gene sequences recovered in the GRIP samples. Sequences were assigned to a habitat (see key) based on the source of isolation of their best match in the GreenGenes database. The graph represents the relative abundance of each habitat (vertical axis) for each sample (x axis). Numbers on the top denote the fraction of sequences that were assignable to a habitat for each sample. For a similar analysis that normalized for the differential representation of habitats among the reference GreenGenes sequences, see SI Appendix, Fig. S6.