Dust is a well-recognized vector for the long-range microbial transport of microorganisms and pollution.12,64,66,67 Recent studies suggest that aerosol microbiomes are most affected by the microbiomes of underlying environments.19,64,68 Variations over seasons and in airmass origin were also linked to changes in aerosol microbial community composition.1,2,6,9,69,70 The aerobiome community composition displays mixtures of sources, and detecting a constant and stable indigenous microbial community was not yet reported. As such, the identified microorganisms may serve as tracers for the sources contributing to the aerobiome. Previous studies comparing aerobiomes to possible sources have shown that soils, leaf surfaces, chicken coops, humans and farm animals contribute to the composition of the aerobiome to varying extents. However, most of these studies relied on amplicon sequencing of taxonomic genetic markers, e.g., the 16S rRNA-encoding gene; focused on a single kingdom, e.g., bacteria; and overlooked functional differences between closely related taxa.
In this study, we sampled dust under different atmospheric conditions, representing various sources, transport trajectories and different concentrations of mineral dust expressed by varying concentrations of PM10. The collected dust metagenomes were compared to metagenomes from three major environments: atmospheric (air and smog sample types), terrestrial (soils) and marine. This comparison, based on taxonomic classification as well as functional gene annotation of metagenomes, was conducted to better understand the similarities and differences among the different microbiomes, infer their functional capacities, and potentially elucidate the contribution of different sources to the atmospheric microbiomes.
Our results show that the metagenomes of dust sampled in Israel in this study most closely resembled dust metagenomes sampled in Saudi Arabia, close to the Red Sea, over 1000 km away, on different sampling dates3. A common source that is attributed to soils contributed to the two dust datasets, according to the SourceTracker analysis. However, variability within Dust IL and Dust Red Sea samples was observed. This variability in Dust IL was correlated with PM10 concentrations, i.e., a higher relative contribution of the soil microbiome was observed in samples with higher PM10 concentrations. This is expected for this region, since a major source of PM10 is mineral dust originating in desert soils. Dust IL samples with low PM10 loading showed higher similarity to atmospheric microbiomes of cloud condensation samples collected in France (cloud samples) and of urban areas in the USA (urban air samples). Sea sample metagenomes contributed very little to all the dust samples, i.e., both Dust IL and Dust Red Sea, despite the proximity to the Mediterranean and Red Seas, respectively. Some of the trajectories of the dust sampled in Israel included a marine component, which was previously linked to an effect on the aerobiome composition7. Moreover, all Dust Red Sea samples were collected in a location adjacent to the Red Sea, and some were even collected on a ship in the Red Sea. Nonetheless, the contribution of the Mediterranean and Red Seas to the dust microbiomes was always below 3.1%. For reference, the contribution of the air microbiomes sampled in France (cloud dataset) and North America (urban air dataset) to the dust microbiome ranged between 3.8% and 12% (Fig. 2). This suggests that the marine environment does not contribute much to transported dust. This conclusion is consistent with another study showing that the marine environment did not significantly contribute to the airborne microbiome over the Atlantic and Pacific Oceans.71 In contrast, dust deposition can contribute to the composition and functional capacity of the marine microbiome, as shown in a few previous studies.14,72−76
Since elevated PM10 concentrations in Israel usually indicate dust events, we looked for correlations between PM10 concentrations and taxonomic and functional gene composition in Dust IL samples. The results indicated that dust storms changed the aerobiome community composition and the functional profile from a fungal-dominated environment to a bacterial-dominated environment. A significant part of the functions that were previously suggested to be linked to microbial survival in the atmosphere, e.g., UV, oxidative and envelope stress resistance, was positively correlated with PM10 concentrations, suggesting that dust-borne bacteria might be a global source of viable or even active bacteria in the atmosphere.
Genes associated with the biodegradation of organic contaminants such as aromatic compounds were relatively more abundant in dust than in any other environment examined and positively correlated with PM10 concentrations. Most of these genes were also common to soils. Previous studies indicated the cometabolism of organic contaminants along with methane and ammonia, due to the presence of di- or monooxygenases with a broad substrate range77. Accordingly, we found that along with genes associated with the biodegradation of organic contaminants, methane metabolism genes were also positively correlated with PM10 concentration, as well as genes associated with glyoxylate and dicarboxylate metabolism, which includes formate metabolism. All or some of these substances might be relevant to metabolic activity in the atmosphere due to their biodegradation, as suggested in other studies,65,78 as well as in dust-affected terrestrial and marine regions.
We found that genes encoding beta-lactam and bacitracin resistance were more abundant in transported dust than in other atmospheric samples. Beta-lactam antibiotics such as penicillins and cephalosporins are commonly administered to humans as well as to food-producing animals such as cattle79, and the findings suggest that an anthropogenic source contributes to the dust microbiome, as was suggested previously by Mazar et al and Gat et al, who showed that antibiotic resistance genes are found in aerosols on dusty and nondusty days and that their source is more likely anthropogenic than natural.4,7. Bacitracin is also a common antibiotic that is administered mostly as an ointment to prevent skin infections, yet resistance to bacitracin is commonly found in Bacillus species and other Firmicutes, suggesting that its source might be natural. The presence of resistance to these two antibiotics in dust metagenomes should raise concerns regarding the spread of this resistance and the possible effects on public health.
Overall, fewer KEGG-characterized functional genes were negatively correlated with PM10 concentrations than were positively correlated with PM10 (566 vs. 1518, respectively). This observation emphasizes the role played by dust storms in changing the microbial community composition from a fungal-dominated community to a bacterial-dominated community in the Mediterranean, as well as in the dispersal of environmental functions. Given the changes in dust storm frequency and severity due to global climatic changes,26,80 the possible implications of such transport should be further investigated.
Interestingly, the SourceTracker analysis showed that low-PM10 dust sample microbiomes significantly overlapped with cloud and urban air sample microbiomes. These common taxa and associated functional genes were also negatively correlated with PM10 concentrations. They were more abundant in the aerobiome than in the soil and sea microbiomes and were mostly fungal. We suggest that these fungal taxa constitute a "core microbiome" for the atmosphere and provide insights into their possible functioning. We found that in general, the relative abundance of fungi, especially those of the phylum Ascomycota, increased when PM10 concentrations decreased, with 13 fungal genera found to be common to all atmospheric datasets and only to these datasets. If we extend our definition of "core microbiome" and include taxa that were negatively correlated with PM10 and were rare in soils and marine samples (clusters 1, 2 and 6, Fig. 3), we obtain 56 fungal genera, mostly belonging to Ascomycota, with highly varied environments and functions. Some of these fungi might be carried by long-range transport, such as Cordyceps, Paracoccidioides and Allomyces, which are often found in tropical regions. Other fungi are animal and plant commensals or pathogens, such as Malassezia, Tilletia, Epidermophyton, Mycosphaerella, Arthroderma, Botryotinia and Gibberella. Studies indicate that fungal spores are actively emitted and dispersed into the atmosphere,21,81−86 which explains their ubiquity in atmospheric samples. Another source of fungal spores in the atmosphere is biomass burning,87,88 as fire smoke is transported great distances in the atmosphere.89,90 Both processes could explain the presence of Ascomycota in all atmospheric metagenomes, as well as their negative correlation with high PM10 concentrations.
Often overlooked members of the aerobiome are archaea. In this study, we found a clear correlation between PM10 concentrations and archaeal abundance in Dust IL samples. Many of these archaea were anaerobic methanogens; accordingly, some methanogenesis-associated genes were positively correlated with PM10 concentrations. Methanogenesis-associated genes were also more abundant in dust than in other atmospheric samples. Methanogenesis is carried out solely by archaea under strictly anaerobic conditions, usually in highly reduced soils or sediments but also in the digestive system and feces of ruminants as well as chicken and other farm animals.91,92 Ruminant feces found in farms or grazing grounds or chicken feces found in chicken coops could have contributed to the dust metagenome. In addition, landfills could also be a source of methanogens in the atmosphere.93–95 This finding may suggest that atmospheric conditions that result in high PM10 concentrations may also result in the suspension of particles other than soil and mineral dust. It also suggests that some methanogens in the atmosphere can mark anthropogenic source contributions. The results from this study, showing the enrichment of antibiotic resistance genes in the aerobiome, corroborate this suggestion. Previous studies have suggested that a dust storm collects material over its course, and its microbial community composition is affected accordingly.7,96 In this manner, a dust storm that passes over an urban, agricultural or industrialized area is likely to increase anthropogenic emissions of microorganisms into the atmosphere and increase their potential impact on aerobiome functionality and composition. This is consistent with the presence of anthropogenic organic contaminants that adhere to transported dust, as shown by Falkovich et al.97,98
The importance of anthropogenic influence on the atmospheric microbiome is only now gaining attention.99 It is predicted that the aerobiome will be influenced by the changing chemical and physical characteristics of the atmosphere due to anthropogenic activities such as cooking, agricultural practices and land use change. Climatic changes such as increased temperatures, fires and drought are projected to increase the amount of dust emitted to the atmosphere,26 thus increasing the contribution of soil microbiomes to the composition of the aerobiome. The increasing frequency and intensity of wildfires100,101 also increases the concentration of particles in the atmosphere. These serve as nuclei for bacterial transport in the atmosphere,99 thereby increasing their dispersal and potentially the functional scope of the aerobiome. Recent evidence on the possible metabolic activity of bacteria in the atmosphere suggests that specific carbon sources are likely to sustain bacteria, e.g., formate, acetic acid and ethanol.8,65,78 Moreover, it was suggested that bacterial metabolism might also affect cloud or even atmospheric chemistry.65,102 Our results suggest that if dust storms carry viable bacteria, they may be metabolically relevant for atmospheric chemical cycles and may spread these bacteria globally.
In this study, we investigated the links between the surface and atmospheric microbiomes, as well as between different atmospheric microbiomes. We showed that different atmospheric niches display different functional profiles and community structures and that they share a common background dominated by fungi. We also showed that two similar niches, i.e., the dust collected in Israel and over the Red Sea on different, nonsynchronized occasions, were strikingly similar, emphasizing the importance of the source of the dust in determining its composition on a regional and possible global scale. As expected, dust showed high resemblance to soils both in community structure and functional profile, yet the dust samples harbored functional genes that are likely to have been derived from an anthropogenic source.