Spatial variability in airborne bacterial communities across land-use types and their relationship to the bacterial communities of potential source environments

Abstract

Although bacteria are ubiquitous in the near-surface atmosphere and they can have important effects on human health, airborne bacteria have received relatively little attention and their spatial dynamics remain poorly understood. Owing to differences in meteorological conditions and the potential sources of airborne bacteria, we would expect the atmosphere over different land-use types to harbor distinct bacterial communities. To test this hypothesis, we sampled the near-surface atmosphere above three distinct land-use types (agricultural fields, suburban areas and forests) across northern Colorado, USA, sampling five sites per land-use type. Microbial abundances were stable across land-use types, with ∼10(5)-10(6) bacterial cells per m(3) of air, but the concentrations of biological ice nuclei, determined using a droplet freezing assay, were on average two and eight times higher in samples from agricultural areas than in the other two land-use types. Likewise, the composition of the airborne bacterial communities, assessed via bar-coded pyrosequencing, was significantly related to land-use type and these differences were likely driven by shifts in the sources of bacteria to the atmosphere across the land-uses, not local meteorological conditions. A meta-analysis of previously published data shows that atmospheric bacterial communities differ from those in potential source environments (leaf surfaces and soils), and we demonstrate that we may be able to use this information to determine the relative inputs of bacteria from these source environments to the atmosphere. This work furthers our understanding of bacterial diversity in the atmosphere, the terrestrial controls on this diversity and potential approaches for source tracking of airborne bacteria.

Figure 1

Map of the locations from which aerosol samples were collected over a 2-week time span during the end of June to early July, 2009. Symbols indicate land-use type (circles=forest, diamonds=suburban and the upside down triangles=mixed agricultural sites). Inset graph shows the state of Colorado and the surrounding states, with the star representing the sampled region for this study.

Figure 2

Left y axis. () Total bacterial abundance in the collected samples from the Colorado Front Range as determined via direct microscopy, and right y axis, (□) total number of high-temperature ice nuclei as determined via the drop-freeze assay. Letters above the bars indicate a significant difference at P<0.05. Error bars indicate±1 s.e.m.

Figure 3

The dominant bacterial phyla and subphyla found in air samples collected from across the three land-use types of the Colorado Front Range: forest (n=5), agricultural (n=5) and suburban (n=5). Proteobacterial groups are designated by the Greek symbols α and β. Error bars indicate±1 s.e.m.

Figure 4

Principal coordinates analysis (PCoA) of the pair-wise distances between bacterial communities as calculated using the UniFrac algorithm (a–c). (a) represents the relationship between the bacterial communities of the three dominant land-use types of the Colorado Front Range and (b) shows the relationship between the bacterial communities from the Colorado Front Range and those collected at 3200 m elevation at Storm Peak laboratory. Panel (c) show the relationships between the bacterial communities found in the three distinct habitats: air, leaf-surfaces and soil. Filled symbols refer to the air samples across land-use type and from Storm Peak laboratory and the open symbols correspond to the two source environments, leaf-surface and soils.

Figure 5

Heatmap displaying the relative abundances across a wide range of air, leaf-surface and soil samples. Soil samples were binned into six different pH categories. Leaf-surface samples were split into gymnosperms and angiosperms and air samples are represented by the Storm Peak laboratory samples collected at the Storm Peak research facility (3200 m above sea level), and the air samples of the three dominant land-use types of the Colorado Front Range: forest, agricultural and suburban sample types. These three ecosystem level groups: air, leaf-surface and soils are designated as blue, green and brown on the color bar, respectively. Environments are clustered based on the percent relative abundance of the nine phylum to subphylum level classifications shown as rows in this figure. Each row was scaled so that the mean of each taxonomic group across sample types was calculated and colored by corresponding z-score of each cell. The heatmap was made with R version 2.11.0 using the heatmap function.

Figure 6

Percent relative abundance of airborne bacterial taxa across the three land-use types that were designated as indicator taxa from soil and leaf-surface environments. Inset. The indicator taxa derived from soil and leaf-surface environments and their percent relative abundances.