Combining permanent aerobiological networks and molecular analyses for large‐scale surveillance of forest fungal pathogens: A proof‐of‐concept

Abstract

Forest disease management relies principally on a preventive approach in which epidemiological surveillance plays a crucial role. However, efficient and cost-effective surveillance methods are not currently available for large spatial scales. Nevertheless, aerobiological networks have been set up for several decades in many countries to monitor pollen dispersal and provide real-time assessments of allergenic risk. Here, we suggest that the same approach could be used for the surveillance of forest pathogens. Using molecular methods, we analysed samples from 12 sites of the French aerobiological network, at different dates. Both metabarcoding by high-throughput sequencing (using two markers and two different bioinformatics approaches) and real-time PCR targeting eight important forest pathogens were conducted. To validate the approach, temporal and spatial trends of spore detection were compared with field disease data. The metabarcoding approach demonstrated that many fungal plant pathogens could be found in aerobiological samples. Moreover, five of the eight targeted forest pathogens were detected by real-time PCR, with temporal and spatial trends of spore capture consistent with field data. In particular, Hymenoscyphus fraxineus was detected at high frequency in aerobiological samples in the areas where ash dieback has been present for the longest period of time, and at lower frequency in areas with more recent invasion. Spore detection of seasonal pathogens showed a temporal pattern similar to that of disease reports. Overall, our study provides a proof of concept that permanent aerobiological networks combined with molecular methods may provide a useful tool for large-scale surveillance of forest pathogens.

Using a systematic approach to synthesize existing knowledge on Gymnopus fusipes (syn. Collybia fusipes), the cause of Collybia root rot

“…Much of the research concerning G. fusipes has been focused in Europe, with molecular‐based identification confirming the presence in France (Aguayo et al, 2021), Germany (Schmidt et al, 2012) and Belgium (Chandelier et al, 2021). Studies that isolated G. fusipes have been concentrated in France (Marçais et al, 1998, 1999, 2000b; Marçais & Caël, 2001), the UK (Boddy & Thompson, 1983; Campbell, 1939; Denman et al, 2017; Gibbs & Greig, 1990) and Poland (Przybyl, 1994).…”

“…Gymnopus fusipes is widespread where the environment is suitable, and although sometimes documented as a typical member of the oak associated fungal community (Watling, 2014), G. fusipes is actually categorized as a forest pathogen (Aguayo et al, 2021; Chandelier et al, 2021). Gymnopus fusipes is most often found on tree stumps or at the base of living trees (Sardariu, 2013; Tortic & Lisiewska, 1978); however, macroscopic identifications have suggested that G. fusipes may also occur in soil (Ambrosio et al, 2018) and leaf litter (Diamandis & Perlerou, 2001), although this finding may result from the stipe of the fruiting body being attached to a suitable organic matter substrate below the ground level, such as decaying wood or root tissue (Campbell, 1939).…”

Comparison of intercept trap fluids and aerial spore collectors to survey fungal spores

“…Similarly, other studies used crushed insect specimens to extract bacterial DNA for metabarcoding (Malacrino et al, 2017;Ravenscraft et al, 2019). Many metabarcoding studies have used classical aerial spore collecting devices, such as active rotating-arm devices (Botella et al, 2019), sticky Ionic traps (Redondo et al, 2020), Hirst-type spore traps (Dananché et al, 2017;Aguayo et al, 2021), Burkard volumetric spore traps (Nicolaisen et al, 2017), or passive collecting devices such as rainwater traps (Castaño et al, 2019;Crandall et al, 2020). This is the first comprehensive study to compare insect trap fluids and classical spore collecting devices.…”

Fungal Spores in Insect Trapping Fluids: Simultaneous Sampling for Insects and Pathogens

“…Similarly, other studies used crushed insect specimens to extract bacterial DNA for metabarcoding (Ravenscraft et al, 2019;Malacrino et al, 2017). Many metabarcoding studies have used classical aerial spore collecting devices such as active rotating-arm devices (Botella et al, 2019), sticky Ionic traps (Redondo et al, 2020), Hirst-type spore traps (Dananché et al, 2017;Aguayo et al, 2021), Burkard volumetric spore traps (Nicolaisen et al, 2017) or passive collecting devices such as rainwater traps (Crandall et al, 2020;Castano et al, 2019). This is the rst comprehensive study to compare insect trap uids and classical spore collecting devices.…”