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 ).