Since the origin of fungi, estimated between 760 million and 1.06 billion years ago
(Lücking et al., 2009), fungi and bacteria have been interacting with each other and
have colonized almost all explored niches on earth, including nutrient poor environments.
Although these two microbial groups often interact in nature and form complex microbial
consortia, fungi and bacteria have been mostly studied separately (Frey-Klett et al.,
2011). Nonetheless, it is well accepted that fungal-bacterial interactions have essential
roles for ecosystem functioning, host health and are also highly relevant in the context
of food industry and biotechnology (Frey-Klett et al., 2011). It is likely that these
two microbial kingdoms have evolved sophisticated strategies to sense each other in
order to compete or cooperate within specific environmental niches. Fungal–bacterial
interactions are mediated by different mechanisms, ranging from contact-dependent
to long-distance signaling processes. Although different degrees of specificity have
been observed (spanning along the mutualism-antagonism continuum), the molecular basis
governing fungal-bacterial interactions remains poorly understood.
Recent evidence indicates that low molecular weight metabolites such as Volatile Organic
Compounds (VOCs) can be produced by taxonomically diverse groups of microorganisms
and play important roles for long distance microbe-microbe interactions (Effmert et
al., 2012; Schmidt et al., 2015). Microbial VOCs were mainly studied from the bacterial
point of view, acting as infochemical molecules in soil or protecting plants against
pathogenic fungi and oomycetes (Garbeva et al., 2014; Cordovez et al., 2015; De Vrieze
et al., 2015). However, still very little is known regarding the chemical diversity
of VOCs produced by filamentous microbes (fungi and oomycetes) as well as their ecological
role for fungal-bacterial interactions. The work of Schmidt et al. (2016) is an important
contribution to the field that nicely illustrates the complexity of the molecular
dialogue likely taking place among soil microbes. Particularly, they address the following
questions: (1) Are soil bacteria able to sense VOCs produced by microbial eukaryotes
and modify their behaviors in response to them? (2) What is the effect of those VOCs
on bacterial fitness and survival? (3) Does the nutritional status matters?
By using GC-Q-TOF analysis, Schmidt et al. identified hundreds of VOCs produced in
vitro by five soil/rhizospheric fungi (Mucor hiemalis, Rhizoctonia solani, Verticillium
dahliae, Fusarium culmorum, Trichoderma sp.) and one oomycete (Pythium ultimum) and
demonstrated that each microbe has its own chemical signature and that the growth
stage and the nutritional status (rich vs. poor media) have a strong effect on VOCs
emission. This result suggests that VOCs production by soil filamentous microbes is
tightly controlled in time and in space according to soil nutritional constraints.
Since organic carbon is the most important factor limiting microbial growth in soil
(Demoling et al., 2007) and that production of particular terpene volatiles is enhanced
under nutrient-poor conditions, it is tempting to speculate that fungal terpenes play
an important role for microbe-microbe communication in soils.
Beyond the characterization of the volatile blends produced by these filamentous microbes,
Schmidt and collaborators also tested their antibacterial activities as well as their
effect on bacterial traits such as growth, motility or biofilm formation. They found
that microbial VOCs emitted by particular fungi/oomycetes strongly affect motility
of two bacterial isolates (Collimonas pratensis and Serratia plymuthica) while the
other traits remain unaltered. This suggests that similar to bacterial VOCs that have
been shown to alter specific fungal/oomycetal traits (Tyc et al., 2014; De Vrieze
et al., 2015; Sharifi and Ryu, 2016), VOCs produced by fungi/oomycetes can be in turn
sensed by bacteria, therefore modulating their ability to move (Figure 1). These results
shed new lights into one possible mechanism used by particular soil and rhizospheric
fungi/oomycetes to attract or repel bacterial neighbors under specific nutritional
conditions. Since motility is an important trait of the bacterial root microbiota
(van Overbeek and Saikkonen, 2016), it would be interesting to test whether particular
rhizospheric fungi can alter endosphere colonization by specific bacteria taxa via
long distance VOCs emission at the root/soil interface.
Figure 1
Role of volatile organic compounds (VOCs) in fungal-bacterial interactions. Soil fungi
and or oomycetes secrete particular volatile blends that are influenced by the growth
stage and the nutritional status of the microbe. As described by Schmidt et al. (2016),
some of these VOCs (i.e., terpenes) can either promote or inhibit the motility of
specific bacteria. In turn, it is well documented that soil bacteria can also produce
VOCs that alter the growth and the reproductive fitness of soil or rhizospheric fungi/oomycetes.
VOCs effect on bacterial motility is highlighted with the following symbols: + (positive),
− (negative), = (no effect). These reciprocal interactions mediated by VOCs are likely
important for structuring microbial communities at long distance.
Interestingly, Schmidt and collaborators also found that the soil fungus F. culmorum
affects differently swimming motility of C. pratensis (reduction) and S. plymuthica
(induction), likely due to the production of a unique terpene blend. To validate the
potential role of terpenes on bacterial motility, they tested the activity of four
pure synthetic terpenes (having mass spectra and retention indices similar with to
those found in the F. culmorum volatile profile) on bacterial motility. They showed
that all four tested terpenes could indeed affect motility (either swarming or swimming)
of at least one of the two tested bacteria. Remarkably, the same terpene molecule
can affect differently the motility of C. pratensis (Betaproteobacteria) and S. plymuthica
(Gammaproteobacteria), indicating that taxonomically unrelated bacteria have evolved
the ability to sense and differentially respond to specific terpene signatures. Their
work is an open eye illustrating the complexity of the soil volatilome and its potential
importance for structuring microbial communities in nature (Figure 1).
Funding
The Max Planck Society and the European Research Council.
Author contributions
The author confirms being the sole contributor of this work and approved it for publication.
Conflict of interest statement
The author declares that the research was conducted in the absence of any commercial
or financial relationships that could be construed as a potential conflict of interest.