Species Richness, rRNA Gene Abundance, and Seasonal Dynamics of Airborne Plant-Pathogenic Oomycetes

Abstract

Oomycetes, also named Peronosporomycetes, are one of the most important and widespread groups of plant pathogens, leading to significant losses in the global agricultural productivity. They have been studied extensively in ground water, soil, and host plants, but their atmospheric transport vector is not well characterized. In this study, the occurrence of airborne Oomycetes was investigated by Sanger sequencing and quantitative PCR of coarse and fine aerosol particle samples (57 filter pairs) collected over a 1-year period (2006-2007) and full seasonal cycle in Mainz, Germany. In coarse particulate matter, we found 55 different hypothetical species (OTUs), of which 54 were plant pathogens and 29 belonged to the genus Peronospora (downy mildews). In fine particulate matter (<3 μm), only one species of Hyaloperonospora was found in one sample. Principal coordinate analysis of the species composition revealed three community clusters with a dependence on ambient temperature. The abundance of Oomycetes rRNA genes was low in winter and enhanced during spring, summer, and fall, with a dominance of Phytophthora, reaching a maximum concentration of ∼1.6 × 10⁶ rRNA genes per cubic meter of sampled air in summer. The presence and high concentration of rRNA genes in air suggests that atmospheric transport, which can lead to secondary infection, may be more important than currently estimated. This illustrates the need for more current and detailed datasets, as potential seasonal shifts due to changing meteorological conditions may influence the composition of airborne Oomycetes. An insight into the dynamics of airborne plant pathogens and their major drivers should be useful for improved forecasting and management of related plant diseases.

Keywords: Peronosporomycetes; Sanger sequencing; airborne Oomycetes; meteorological parameter; plant pathogen; qPCR analysis; seasonal distribution.

FIGURE 1

Species richness and seasonal dynamics in composition of airborne Oomycetes. (A) Relative proportions of different genera (n.c. = not classified), and (B) heatmap of Bray-Curtis (BC) dissimilarity in OTU composition between all analyzed samples. The BC index can vary between 0, for an identical OTU composition, and 1, for no common OTUs on the samples.

FIGURE 2

Temperature dependency of OTU composition. (A) Principle coordinate analysis (PCoA) of Bray-Curtis dissimilarities, revealing three temperature-dependent clusters with high, intermediate, and low average sampling temperatures. Point shape represents the sampling season, and color represents the average temperature for each aerosol filter pair. (B) Temperature distributions of the clusters (middle band: median, box: the 25 to 75th percentile, whiskers: 95% confidence interval. (C) Relative proportions of different genera within the three clusters (n.c. = not classified).

FIGURE 3

Oomycetes rRNA gene abundance retrieved from qPCR analysis. (A) The gene abundance (rRNA genes m^-3 air) of selected taxa and total Oomycetes in coarse particle filter samples. Error bars represent standard deviation of triplicates. (B) Average seasonal rRNA gene abundance for selected taxa and total Oomycetes. Boxes limit 25 and 75% percentile, median presented as line, and mean values as point inside, connected in line. Error bars present 1 and 99% percentile. Outliers are shown (Student’s two sample t-test p-value < 0.01). (C) Gene abundance of selected taxa and total Oomycetes scaled to maximal taxon-specific values. (D) Gene abundance of selected taxa scaled to gene abundance of total Oomycetes, correlated with gene abundance of the selected taxa. Color codes in all panels: total Oomycetes marked as black squares, Albuginaceae as green inverted triangle, Phytophthora as red circles, Peronospora as orange triangles, and Pythium as blue diamond.