Linking soil's volatilome to microbes and plant roots highlights the importance of microbes as emitters of belowground volatile signals

Abstract

Summary Plants and microbes release a plethora of volatiles that act as signals in plant–microbe interactions. Characterizing soil's volatilome and microbiome might shed light on the nature of relevant volatile signals and on their emitters. This hypothesis was tested by characterizing plant cover, soil's volatilome, nutrient content and microbiomes in three grasslands of the Swiss Jura Mountains. The fingerprints of soil's volatiles were generated by solid‐phase micro‐extraction gas chromatography/mass spectrometry, whereas high‐throughput sequencing was used to create a snapshot of soil's microbial communities. A high similarity was observed in plant communities of two out of three sites, which was mirrored by the soil's volatilome. Multiple factor analysis evidenced a strong association among soil's volatilome, plant and microbial communities. The proportion of volatiles correlated to single bacterial and fungal taxa was higher than for plants. This suggests that those organisms might be major contributors to the volatilome of grassland soils. These findings illustrate that key volatiles in grassland soils might be emitted by a handful of organisms that include specific plants and microbes. Further work will be needed to unravel the structure of belowground volatiles and understand their implications for plant health and development.

Linking Plant Secondary Metabolites and Plant Microbiomes: A Review

“…Together, these studies show that the plant VOC-microbiome interactions are widespread and are of great ecological interests. A recent review provided an excellent account of the interaction between the phyllosphere or rhizosphere microbiomes and plant VOC emissions ( Schenkel et al, 2019 ).…”

“…Similar observations were made in Penstemon digitalis ( Burdon et al, 2018 ), Arabidopsis thaliana ( Raza et al, 2020 ), Brassica rapa ( Helletsgruber et al, 2017 ), petunia ( Boachon et al, 2019b ), and Atractylodes lancea ( Zhou et al, 2018 ). A recent review provided an excellent summary on the effects of plant microbiomes on plant VOC emissions ( Schenkel et al, 2019 ).…”

The soil crisis: the need to treat as a global health problem and the pivotal role of microbes in prophylaxis and therapy

“…This attraction of Streptomyces of arthropods is specific, as insects and arachnids do not respond to geosmin. Signalling between soil organisms via volatiles is pervasive (Audrain et al, 2015;Schulz-Bohm et al, 2017;Tyc et al, 2017;Hammerbacher et al, 2019;Schenkel et al, 2019;Camarena-Pozos et al, 2021;Weisskopf, et al, 2021). However, soil compaction through use of heavy machinery, and flooding events, reduce air spaces and channels in soil, and hence reduce the diffusive flow of signalling volatiles.…”

“…As already mentioned, soil microbes have been successfully mined for many diverse applications that include symbiotic and non-symbiotic N 2 -fixation, protection of and acquisition of soil minerals by plant roots through mycorrhizal fungi, protection from pathogens by antibiotic producing bacteria, like Pseudomonas (van Peer et al, 1991;Roca et al, 2013) andBacillus (Perez-Garcia et al, 2011;Chen et al, 2020b), protection from insect pests by entomopathogenic bacteria and fungi, like Pseudomonas (e.g. Ruffner et al, 2012), Bt toxin-producing Bacillus thuringiensis (Federici, 2005) and fungi, like Beauveria bassiana (Ownley et al, 2004), increasing root growth by production of plant hormones, inducing systemic resistance by production of volatile signals, increasing tolerance of stresses (de Zelicourt et al, 2013), degradation and immobilization of soil pollutants, restoration of soil functionality after fire damage (Pizarro-Tobias et al, 2015;Schenkel et al, 2019;Steindorff et al, 2021), etc. Many of these, and other, microbial activities can be exploited in applications designed to replace or reduce the use of agrochemicals.…”

Spotlight on how microbes influence their host's behavior

“…This is demonstrated in this special issue by a combination of metabolomics and metagenomics being used to characterize the seaweed microbiota and identify a positive correlation between select microbial taxa and the occurrence of metabolites of relevance to the host's defence (Paix et al, 2019). A combination of metabolomics and metagenomics was also applied to terrestrial ecosystems, in a study showing that soil microbes rather than roots are the main contributors to the emission of volatile organic compounds in grassland soils (Schenkel et al, 2019).…”