Global biogeography of atmospheric microorganisms reflects diverse recruitment and environmental filtering

Abstract

Atmospheric transport is critical to dispersal of microorganisms between habitats, and this underpins resilience in terrestrial and marine ecosystems globally. A key unresolved question is whether microorganisms assemble to form a taxonomically distinct, geographically variable, and functionally adapted atmospheric microbiota. This question is made more complex by the unique challenges of separating potential contaminants from atmospheric signal, particularly given the ultra-low biomass of air and the long durations of sampling where contamination may occur. Here we adopted a comprehensive data filtering approach to mitigate contamination and characterise inter-continental patterns of microbial taxonomic and functional diversity in air within and above the atmospheric boundary layer and in underlying soils for 596 globally sourced samples. Bacterial and fungal assemblages in air were taxonomically structured and deviated significantly from purely stochastic assembly. Patterns differed with location and reflected climate, underlying surface cover and environmental filtering. Source-tracking indicated a complex recruitment process involving local soils plus globally distributed inputs from drylands and the phyllosphere. Assemblages displayed stress-response and metabolic traits relevant to survival in air, and taxonomic and functional diversity were correlated with macroclimate and atmospheric variables. Our findings highlight complexity in the atmospheric microbiota that is key to understanding regional and global ecosystem connectivity.

Microbial ecology of the atmosphere

“… 2019 , Archer et al . 2022 ) and historical cultivation approaches (Després et al . 2012 ) collectively indicate that the most abundant cellular microorganisms within the atmospheric boundary layer are bacteria and fungi.…”

“… 2019 , Archer et al . 2022 ). Estimates from fresh snowfall and from cloud water suggest 4 × 10 2 –4 × 10 3 bacterial cells per m 3 and 4 × 10 0 –4 × 10 2 eukaryotic cells per m 3 assuming condensed water content of 0.4 g per m 3 (Christner et al .…”

“…(B) Predicted global relative abundance of bacteria and fungi in the near-surface atmospheric boundary layer from observed quantitative PCR of rRNA genes in air above locations within different climatically defined biomes (Archer et al . 2022 ). The use of quantitative PCR data is cautiously interpreted here as relative abundance and is not used to infer cell numbers.…”

“…(C) Taxonomic composition by class of bacteria and fungi in the near-surface atmospheric boundary layer inferred from rigorously decontaminated environmental rRNA gene sequence data from globally distributed locations, adapted from Archer et al . ( 2022 ). Coloured boxes indicate classes encountered at a relative abundance of ≥0.1%.…”

“… 2019 , Archer et al . 2022 ). Thus theoretical frameworks in ecology that have made implicit assumptions about ubiquitous microbial distribution in air are being validated and revised (Dumbrell et al .…”