Summer season and long‐term drought increase the richness of bacteria and fungi in the foliar phyllosphere of Quercus ilex in a mixed Mediterranean forest

Abstract

We explored the changes in richness, diversity and evenness of epiphytic (on the leaf surface) and endophytic (within leaf tissues) bacteria and fungi in the foliar phyllosphere of Quercus ilex, the dominant tree species of Mediterranean forests. Bacteria and fungi were assessed during ontogenic development of the leaves, from the wet spring to the dry summer season in control plots and in plots subjected to drought conditions mimicking those projected for future decades. Our aim was to monitor succession in microbiota during the colonisation of plant leaves and its response to climate change. Ontogeny and seasonality exerted a strong influence on richness and diversity of the microbial phyllosphere community, which decreased in summer in the whole leaf and increased in summer in the epiphytic phyllosphere. Drought precluded the decrease in whole leaf phyllosphere diversity and increased the rise in the epiphytic phyllosphere. Both whole leaf bacterial and fungal richness decreased with the decrease in physiological activity and productivity of the summer season in control trees. As expected, the richness of epiphytic bacteria and fungi increased in summer after increasing time of colonisation. Under summer dry conditions, there was a positive relationship between TRF (terminal restriction fragments) richness and drought, both for whole leaf and epiphytic phyllosphere, and especially for fungal communities. These results demonstrate that changes in climate are likely to significantly alter microbial abundance and composition of the phyllosphere. Given the diverse functions and large number of phyllospheric microbes, the potential functional implications of such community shifts warrant exploration.

Bacterial Communities Associated with Surfaces of Leafy Greens: Shift in Composition and Decrease in Richness over Time

“…This means that the bacterial communities in the phyllosphere of our leafy-green samples changed with the maturation of the plants, and it may indicate that plants exert a selective force on the colonizing bacteria. A few studies have already investigated the impact of leaf age and seasonal effects on phyllosphere communities (14)(15)(16)(17)(18). Our findings are consistent with previous studies.…”

“…The richness and abundance of the spinach phyllosphere bacterial community decrease as the plant leaf matures (18). On the other hand, a study of leaf age and the seasonality of the tree species Quercus ilex in the Mediterranean forest revealed an increase in the richness of epiphytic bacteria with increasing time of colonization (17). With respect to planting 2 in our study, the bacterial richness remained consistent at both sites, and they also had similar microbial profiles that separated them from plantings 1 and 3 ( Fig.…”

“…The introduction of culture-independent methods, in particular, microbial profiling using high-throughput sequencing to study microorganisms, has revealed more complexity and diversity of the phyllosphere microbiota and has dramatically changed the landscape of microbial ecology (5, 7-10). The 454 pyrosequencing platform has been used in different studies of bacterial communities associated with leafy greens (11-15), but Illumina MiSeq has lately been the dominant platform for microbial profiling.Previous studies have shown that the impact of leaf age and seasonal variations on the phyllosphere communities is not clear (14)(15)(16)(17)(18). It can be hypothesized that phyllosphere communities will change with time because of a decline in the nutrient supply when the leaf matures, selection of specific microbiota by different leafy greens, or weather effects.…”

“…Previous studies have shown that the impact of leaf age and seasonal variations on the phyllosphere communities is not clear (14)(15)(16)(17)(18). It can be hypothesized that phyllosphere communities will change with time because of a decline in the nutrient supply when the leaf matures, selection of specific microbiota by different leafy greens, or weather effects.…”

An evolutionary ecology perspective to address forest pathology challenges of today and tomorrow

“…There is already a large body of knowledge showing that the composition and structure of the tree microbiota strongly respond to environmental factors such as temperature, drought, atmospheric CO 2 , or urbanization (Jumpponen and Jones 2010;Compant et al 2010;Peñuelas et al 2012;Cordier et al 2012a;Coince et al 2014;Rico et al 2014). There is also increasing evidence showing that the tree microbiota is influenced by the genetic variability of trees, both at intraspecific (Schweitzer et al 2008;Cordier et al 2012b;Bálint et al 2013) and interspecific (Knief et al 2010;Redford et al 2010;Kembel and Mueller 2014;) levels.…”