Abstract
Plant-associated microorganisms play a crucial role in plant health and productivity. Belowground microbial diversity is widely reported as a major factor in determining the composition of the plant microbiome. In contrast, much less is known about the role of the atmosphere in relation to the plant microbiome. The current study examined the hypothesis that the atmospheric microbiome influences the composition of fungal communities of the aboveground organs (flowers, fruit, and leaves) of table grape and vice versa. The atmosphere surrounding grape plantings exhibited a significantly higher level of fungal diversity relative to the nearby plant organs and shared a higher number of phylotypes (5,536 OTUs, 40.3%) with the plant than between organs of the same plant. Using a Bayesian source tracking approach, plant organs were determined to be the major source of the atmospheric fungal community (92%). In contrast, airborne microbiota had only a minor contribution to the grape microbiome, representing the source of 15, 4, and 35% of the fungal communities of leaves, flowers, and fruits, respectively. Moreover, data indicate that plant organs and the surrounding atmosphere shared a fraction of each other’s fungal communities, and this shared pool of fungal taxa serves as a two-way reservoir of microorganisms. Microbial association analysis highlighted more positive than negative interactions between fungal phylotypes. Positive interactions were more common within the same environment, while negative interactions appeared to occur more frequently between different environments, i.e., atmosphere, leaf, flower, and fruit. The current study revealed the interplay between the fungal communities of the grape phyllosphere with the surrounding air. Plants were identified as a major source of recruitment for the atmospheric microbiome, while the surrounding atmosphere contributed only a small fraction of the plant fungal community. The results of the study suggested that the plant–air interface modulates the plant recruitment of atmospheric fungi, taking a step forward in understanding the plant holobiont assembly and how the atmosphere surrounding plants plays a role in this process. The impact of plants on the atmospheric microbiota has several biological and epidemiological implications for plants and humans.
Highlights
Microorganisms play a major role in shaping ecosystems, contributing to nutrient cycling, primary production, litter decomposition, and multitrophic interactions (Mahnert et al, 2015; Abdelfattah et al, 2018)
The present study demonstrated that the atmosphere surrounding the grape phyllosphere has a significantly higher level of fungal diversity than the grape phyllosphere composed of flowers, leaves, and fruits
In agreement with these studies, our data indicated that air samples shared a high number of phylotypes (5536 Operational Taxonomic Unit (OTU), 40.3%) with plant organs, and a fraction higher than those shared between organs within the same plant
Summary
Microorganisms play a major role in shaping ecosystems, contributing to nutrient cycling, primary production, litter decomposition, and multitrophic interactions (Mahnert et al, 2015; Abdelfattah et al, 2018). The beneficial effects of the microbiota on plant health include increased tolerance to biotic and abiotic stresses (Eleonora et al, 2015; Unyarat et al, 2016), growth promotion, and increased nutrient intake (van der Heijden et al, 2015). In recognition of these effects, the hologenome theory suggests that the holobiont (host plus symbionts) with its hologenome (host genome plus microbiome) act as a single evolutionary unit (Zilber-Rosenberg and Rosenberg, 2008). Soil is often reported to be a major source of plant microbiota (Bulgarelli et al, 2013; Edwards et al, 2015; Belda et al, 2017; Hassani et al, 2018), the role of the atmosphere as a source for the recruitment and dissemination of the plant microbiota is poorly understood
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