The role for non-pathogenic microorganisms in PSF
Many microbial OTUs were indicators of negative PSF in our system (Fig.
2), which is consistent with many other studies showing accumulation of
soilborne detrimental organisms by plants (e.g., Mangan et al. ,
2010; Bagchi et al. , 2014; Laliberté et al. , 2015).
However, our results also suggest that non-pathogenic soil
microorganisms are an overlooked group of soil biota that may drive
negative PSF and plant coexistence. Soil microorganisms are known to be
efficient competitors for mineral nutrients, especially N (Liu et
al. , 2016). They have high nutrient uptake capacity and high demand for
it (Kuzyakov & Xu, 2013). Denitrifying prokaryotes efficiently compete
against roots for NO3- when roots
deplete soil O2 through respiration (Philippot et
al. , 2002, 2009). Nitrifiers, on the other hand, compete with roots for
NH4+, which they require as an energy
source (Prosser, 1990). Knowing that N mineralization rates in
unfertilized grasslands are expected to be insufficient to meet both
microbial and plant demand (Woodmansee et al. , 1981),
exploitation competition between plant and soil microorganisms is
expected to be intense in our N-poor natural grassland. As a result, a
plant that accumulates microbial competitors for N in its rhizosphere
may suffer from negative PSF.
Our evidence that non-pathogenic microbes can cause negative PSF should
also lead to reconsideration of the intended target of a variety of root
exudates. For example, antimicrobial compounds secreted by plants (e.g.,
quinones, terpenoids, flavonoids) (Brigham et al. , 1999; Bais,
2006) may target soil microorganisms broadly. Not strictly soilborne
pathogens. Bromus, for example, has specifically been found to
produce surprisingly high amounts of polyphenol oxidase in its
rhizosphere (Holzapfel et al. , 2010), a class of enzymes known to
degrade mycotoxins (e.g., Alberts et al. , 2009). Plants are also
known to interfere broadly with soil microbial growth by exuding
protons, phenolics, glucanases or chitinase (Weisskoppf et al. ,
2006). Conversely, many non-pathogenic microorganisms have been
demonstrated to inhibit plant nutrient uptake through inhibition of
mycorrhiza formation (Duponnois & Garbaye, 1991), or degradation of
nutrient-mobilizing compounds secreted by plants (e.g., organic acids)
(Marschner et al. , 2011). Taken collectively, all these
mechanisms bring compelling evidence to the idea that plants are
involved in antagonistic interactions with soil microorganisms broadly,
not only the ones that are trying to colonize their tissues (i.e.,
pathogens).
Positive PSF were also common in our system, especially forBromus (Fig. 1). These were not linked to mutualistic/symbiotic
OTUs (Fig. 2), even though these guilds were well represented in our
microbial metacommunity (which included Bacillus spp.,Pseudomonas spp., arbuscular mycorrhizal fungi, dark septate
endophytes, etc.). This could be explained by the fact that the impact
of belowground symbionts on plants tend oscillate along a
mutualism-parasitism continuum, which is contingent upon the abiotic
environment (Johnson et al. , 1997; Hirsch, 2004). More generally,
this shows how positive PSF must be interpreted beyond the idea of
mutualistic symbiont accumulation. Our indicator OTUs for positive PSF
were non-symbiotic nutrient cyclers (fungal saprotrophs, prokaryotic
nitrifiers, etc.), showing that plants can benefit from microorganisms
contributing to nutrient cycling more broadly, and not necessarily in a
symbiotic manner. We should also keep in mind that mutualistic guilds
(e.g., arbuscular mycorrhizal fungi) can drive negative PSF (Bever,
1999, 2002; Chagnon et al. , unpublished data ).