Long-Term Application of Biochar Mitigates Negative Plant–Soil Feedback by Shaping Arbuscular Mycorrhizal Fungi and Fungal Pathogens

Abstract

Negative plant-soil feedback (PSF) arises when localized accumulations of pathogens reduce the growth of conspecifics, whereas positive PSF can occur due to the emergence of mutualists. Biochar, a carbon-rich material produced by the pyrolysis of organic matter, has been shown to modulate soil microbial communities by altering their abundance, diversity, and activity. For this reason, to assess the long-term impact of biochar on soil microbiome dynamics and subsequent plant performance, we conducted a PSF greenhouse experiment using field soil conditioned over 10 years with <i>Vitis vinifera</i> (L.), without (e.g., C) or with biochar at two rates (e.g., B and BB). Subsequently, the conditioned soil was employed in a response phase involving either the same plant species or different species, i.e., <i>Medicago sativa</i> (L.), <i>Lolium perenne</i> (L.), and <i>Solanum lycopersicum</i> (L.). We utilized next-generation sequencing to assess the abundance and diversity of fungal pathogens and arbuscular mycorrhizal fungi (AMF) within each conditioned soil. Our findings demonstrate that biochar application exerted a stimulatory effect on the growth of both conspecifics and heterospecifics. In addition, our results show that untreated soils had a higher abundance of grape-specialized fungal pathogens, mainly <i>Ilyonectria liriodendra</i>, with a relative abundance of 20.6% compared to 2.1% and 5.1% in B and BB, respectively. <i>Cryptovalsa ampelina</i> also demonstrated higher prevalence in untreated soils, accounting for 4.3% compared to 0.4% in B and 0.1% in BB. Additionally, <i>Phaeoacremonium iranianum</i> was exclusively present in untreated soils, comprising 12.2% of the pathogens' population. Conversely, the application of biochar reduced generalist fungal pathogens. For instance, <i>Plenodomus biglobosus</i> decreased from 10.5% in C to 7.1% in B and 2.3% in BB, while <i>Ilyonectria mors-panacis</i> declined from 5.8% in C to 0.5% in B and 0.2% in BB. Furthermore, biochar application was found to enrich the AMF community. Notably, certain species like <i>Funneliformis geosporum</i> exhibited increased relative abundance in biochar-treated soils, reaching 46.8% in B and 70.3% in BB, compared to 40.5% in untreated soils. Concurrently, other AMF species, namely <i>Rhizophagus irregularis</i>, <i>Rhizophagus diaphanus</i>, and <i>Claroideoglomus drummondii</i>, were exclusively observed in soils where biochar was applied. We propose that the alleviation of negative PSF can be attributed to the positive influence of AMF in the absence of strong inhibition by pathogens. In conclusion, our study underscores the potential of biochar application as a strategic agricultural practice for promoting sustainable soil management over the long term.