Soil microbial community differences drive variation in Pinus sylvestris physiology, productivity, and responses to elevated CO2.

BACKGROUND: Soil microbial communities can affect plant nutrient uptake, productivity, and may even confer resistance to global change. Elevated atmospheric CO2 is widely expected to stimulate plant productivity; however, this will depend on the availability of growth limiting nutrients such as nitrogen. Soil microbial communities are the main mediators of soil nitrogen cycling and should therefore play a key role in influencing plant responses to elevated CO2. RESULTS: To test this, we conducted a controlled, growth chamber experiment with Pinus sylvestris to evaluate how soil microbiome variation influences plant physiology, productivity, and responses to elevated CO₂ (eCO₂; 800 ppm versus 400 ppm in the ambient treatment). Field soils were collected from six forests with varying tree growth rates and were used as an inoculant source, either sterilized or living, into a common growth medium seeded with P. sylvestris. After seven months of growth, we measured plant carbon assimilation, photosynthetic nitrogen use efficiency, above- and belowground productivity, and we measured soil microbial biodiversity using DNA metabarcoding. Our findings demonstrate that seedling productivity was stimulated under eCO2 conditions and that this was supported by improved plant photosynthetic nitrogen use efficiency, but only in the presence of living versus sterilized soil inoculant. The magnitude of this response was also dependent on the forest soil microbial inoculant source and was linked to a 70% increase in bacterial species richness, increased relative abundances of bacteria known to have positive effects on plant growth (e.g., Lactobacillus, Bacillus, Flavobacterium), and with a concomitant shift in saprotrophic fungal community composition and root growth. Variation in inorganic nitrogen cycling which favored the accumulation of nitrate under eCO2 was also correlated with a twofold reduction in photosynthetic nitrogen use efficiency, suggesting a decoupling of nitrogen availability and assimilation efficiency with distinct implications for plant growth responses to elevated CO2. CONCLUSIONS: Our results show that soil microbial community variation directly affects P. sylvestris physiology, productivity, and responses to eCO2, and may enhance plant growth through improved nitrogen use efficiency. Surprisingly, growth with different microbial communities even more strongly impacted plant productivity than a doubling of atmospheric CO2 concentrations. The soil microbiome therefore plays a key role in supporting plant nutrition and growth under ambient and eCO2 conditions, and in turn, may confer increased forest resistance to climate change.