Enrichment in biodiversity and maturation of the soil food web under conservation agriculture is associated with suppression of rice-parasitic nematodes

Meloidogyne spp. and Hirschmanniella spp. are among the most damaging plant-parasitic nematodes (PPNs). They threaten rice production, the main staple food in Asia. Cropping systems that promote natural biocontrol and plant tolerance to diseases are put forward as sustainable solutions to protect rice from these pests. In particular, cropping systems managed under conservation agriculture (CA) are promising because they improve soil health and functioning. We investigated the effects of two cropping system components in a Cambodian field, (i) CA practices, i.e., no-tillage with a cover crop Stylosanthes guianensis (cv. Nina), versus conventional plow-based tillage with no cover crop, and (ii) using IR504, IR64, Azucena and Zhonghua 11 rice varieties, on PPNs in roots and on communities (bacteria, fungi and nematodes) in the rhizosphere. We used a sequencing approach via amplicon barcoding to target microbial marker genes (16 S and ITS rRNA gene) and a microscopic approach to identify and quantify nematodes in the rhizosphere compartment. The variety had less effect than agricultural practices on the infection by PPNs and on the assembly of the three rhizosphere communities. Under CA, the abundance of PPNs extracted from the roots was reduced by 88%. Soil quality was substantially improved (+83% of total Kjeldahl nitrogen, +34% of available phosphorus, +10% of exchangeable potassium, +110% of soil organic carbon, +30% for the cation exchange capacity), thus providing more basal resources for microbial decomposers, especially fungi (+164% putative saprotrophs). Characterization of the three rhizosphere communities revealed a shift in the structure associated with soil enrichment. Both microbial richness (+3% for bacteria and +38% for fungi) and diversity (Shannon index, +11% for fungi and +5% for nematodes) increased. The relative abundance of taxa was modified by CA with notably more mycorrhizal fungi (+329% Glomeromycota spp.) and fewer Pratylenchidae nematodes (−92% Hirschmanniella spp.) in the rhizosphere. The reassembly of the communities using CA was associated with regulation of PPN populations. The reduction in Meloidogyne spp. abundance in roots (−64%) was correlated with the maturity of the food web (maturity index, +10% under CA) and with the increase in the relative abundance of omnivorous nematodes in the rhizosphere (+68% under CA). Seven years of CA in this field enabled the whole soil food web to mature thus creating a favorable niche for potentially predatory nematodes and microbes antagonistic against PPNs. This study confirms that CA is an alternative to nematicides to limit infection by PPNs in rice cropping systems.