Maturation of the soil food web under conservation agriculture is associated with a reduction of rice-parasitic nematodes

Meloidogyne spp. and Hirschmanniella spp. are among the world's most damaging plant-parasitic nematodes. They threaten the production of rice, the main staple food in Asia. Looking for sustainable solutions to protect rice from these pests, cropping systems that promote biocontrol and plant resilience are brought forward. In particular, cropping systems managed within conservation agriculture (CA) are promising because they improve soil health and functioning. In this study, we investigated the effect of two components of the cropping system, (i) the agricultural practices (conservation agriculture, i.e. no-tillage cropping system with Stylosanthes guianensis (variety Nina) as cover crops, versus conventional plough-based tillage without cover crop) and (ii) the rice variety (IR504, IR64, Azucena and Zhonghua) on plant-parasitic nematodes in roots and rhizosphere communities. We used a molecular approach by amplicon barcoding to target microbial marker genes (16S and ITS rRNA gene) and a microscopic approach to identify and quantify nematodes in the rhizosphere compartment. The effect of the variety had a lower print than the effect of the agricultural practices on the infective nematodes and on the three rhizosphere communities. within CA, the abundance of plant-parasitic nematodes extracted from the roots was reduced by 88%. Soil quality was substantially improved (+83% of TKN, +34% of available P, +10% of exchangeable K, +110% of SOC, +30% for the CEC), providing more basal resources for the microbial decomposers, especially fungi (+164% putative saprotrophs). A characterization of the three rhizosphere communities (bacteria, fungi and nematodes) showed a shift in the structures that was associated with the soil enrichment. Microbial richness was increased (+3% for bacteria and +38% for fungi) and diversity (Shannon's index) was increased for fungi (+11%) and nematodes (+5%). Relative abundances of taxa and trophic guilds were modified with notably more mycorrhizal fungi (+329% Glomeromycota spp.) and less Pratylenchidae nematodes (-92% Hirschmanniella spp.) in the rhizosphere. This reassembly of the communities within CA was associated with a regulation of plant-parasitic nematodes populations. The reduction of Meloidogyne spp. abundance in roots (-64%) was correlated with the maturation of the food web (maturity index, +9% within conservation agriculture) and the increase of omnivorous nematodes relative abundance in the rhizosphere (+68% within conservation agriculture). Seven years of conservation agriculture in this field allowed the maturation of the whole soil food web and built a favorable niche for potentially predatory nematodes and microbial antagonists to plant-parasitic nematodes. This study emphasizes that conservation agriculture represents an alternative system to limit the infection by plant-parasitic nematodes in rice cropping systems.