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. 2018 Dec;12(12):2967-2980.
doi: 10.1038/s41396-018-0229-3. Epub 2018 Aug 2.

Contrasting Distribution Patterns Between Aquatic and Terrestrial Phytophthora Species Along a Climatic Gradient Are Linked to Functional Traits

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Free PMC article

Contrasting Distribution Patterns Between Aquatic and Terrestrial Phytophthora Species Along a Climatic Gradient Are Linked to Functional Traits

Miguel A Redondo et al. ISME J. .
Free PMC article

Abstract

Diversity of microbial organisms is linked to global climatic gradients. The genus Phytophthora includes both aquatic and terrestrial plant pathogenic species that display a large variation of functional traits. The extent to which the physical environment (water or soil) modulates the interaction of microorganisms with climate is unknown. Here, we explored the main environmental drivers of diversity and functional trait composition of Phytophthora communities. Communities were obtained by a novel metabarcoding setup based on PacBio sequencing of river filtrates in 96 river sites along a geographical gradient. Species were classified as terrestrial or aquatic based on their phylogenetic clade. Overall, terrestrial and aquatic species showed contrasting patterns of diversity. For terrestrial species, precipitation was a stronger driver than temperature, and diversity and functional diversity decreased with decreasing temperature and precipitation. In cold and dry areas, the dominant species formed resistant structures and had a low optimum temperature. By contrast, for aquatic species, temperature and water chemistry were the strongest drivers, and diversity increased with decreasing temperature and precipitation. Within the same area, environmental filtering affected terrestrial species more strongly than aquatic species (20% versus 3% of the studied communities, respectively). Our results highlight the importance of functional traits and the physical environment in which microorganisms develop their life cycle when predicting their distribution under changing climatic conditions. Temperature and rainfall may be buffered differently by water and soil, and thus pose contrasting constrains to microbial assemblies.

Conflict of interest statement

The authors declare that they have no conflict of interest.

Figures

Fig. 1
Fig. 1
Association between climatic score, mean annual temperature, and total annual precipitation. The mean annual temperature and the total annual precipitation correspond to the average of the last 20 years. Climatic score corresponds to the score of each sampling site on the first axis of a principal component analysis, which included the average values of both mean annual temperature and total annual precipitation of the last 20 years
Fig. 2
Fig. 2
Association between species richness and functional richness for simulated a terrestrial and b aquatic Phytophthora communities. The lines correspond to the average (solid black line) and the 90% quantile (dotted lines) of the 5000 simulations of functional richness for each number of species richness. Solid black circles correspond to communities with significantly lower functional richness than the null-model simulated communities (one-tailed t-test, P < 0.05). Some communities had the same value of functional richness, and therefore some solid dots are overlapped
Fig. 3
Fig. 3
Distribution of terrestrial communities dominated by different trait values of a clade, b infected tissue, c asexual survival structures, and d reproductive mode, along a climatic gradient. Of the nine traits investigated, only the four traits with the highest R2 values are shown. Trait dominance was determined using the community-weighted mean (CWM) values of traits. A community climatic score with a value of 0 corresponds to the average temperature and precipitation values of all the sampling sites. In total, 164 terrestrial communities were included in the analysis. Error bars represent SE. Different lowercase letters above or below the error bars indicate significant differences at P < 0.05 when subjected to a protected Fisher least square differences (LSD) test. Higher values of community climatic score indicates wetter and warmer places, as showed in Figure 1
Fig. 4
Fig. 4
Community optimum temperature of a terrestrial and b aquatic Phytophthora communities along the climatic gradient. The community optimum temperature corresponds to the weighted mean of the optimum temperature for the species that comprise the community. A community climatic score with a value of 0 corresponds to the average temperature and precipitation values of all the sampling sites. Each circle corresponds to a community. Solid circles represent communities obtained in 2013; empty circles represent communities obtained in 2014. In total, 164 terrestrial and 192 aquatic communities were included in the analysis
Fig. 5
Fig. 5
The association between climatic scores and functional traits at the species level for terrestrial Phytophthora species. a Association between the optimum temperature for the species and the species climatic score. The R2 and P-value (P) is based on a linear regression weighted by the proportion of total reads for each of the species. b Association between the climatic score and the asexual survival structures of terrestrial Phytophthora species detected at more than one location during the survey. The mean climatic score of species that form asexual structures was significantly higher than that of species that did not form structures (P = 0.02, Welch t-test). A climatic score with a value of 0 corresponds to the average temperature and precipitation values of all the sampling sites in the survey. In total, 21 Phytophthora species were included in this analysis: bra P. brassicae, cic P. cichorii, por P. porri, gal P. gallica, eur P. europaea, syr P. syringae, fra P. fragariae, plu P. plurivora, pse P. pseudosyringae, soj P. sojae, aln P. alni (species complex), uli P. uliginosa, san P. sansomeana, cam P. cambivora, ira P. iranica, pis P. pisi, dre P. drechsleri, fraf P. fragariaefolia, tri P. trifolii, cry P. cryptogea

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