Disentangling shifts in the soil microbiome of potatoes infected with Rhizoctonia solani AG 3-PT in two contrasting regions of South Africa

Abstract

Potato (Solanum tuberosum L.) is a widely consumed and economically important vegetable crop that ensures food security to many communities worldwide. The fungus Rhizoctonia solani AG 3-PT is one of the most devastating pathogens causing several potato diseases in South Africa and globally. The removal of various fungicides from the market and strict regulations on the use of synthetic chemicals makes disease management difficult. Therefore, alternative and environmentally safe control measures, such as biological control agents (BCAs), are being considered to improve the soil and plant health of important crops. Next-Generation Sequencing (NGS) methods, such as amplicon sequencing, enable detailed structural characterisations and possible interactions of the soil microbial communities as a whole, without the need for microbial culturing. The objective of this study was to investigate the changes in soil fungal and bacterial communities in response to R. solani AG 3-PT infection for the identification of key microbial indicators that show potential disease-suppressive activity. To identify key microbial indicators of disease suppression against R. solani AG 3-PT, a greenhouse pot trial experiment was conducted using soil from two contrasting potato production regions in South Africa, namely the KwaZulu-Natal and the Sandveld. High-throughput sequencing of fungal ITS and bacterial 16S rRNA was used to characterize the fungal and bacterial community composition in the soils, respectively, with and without artificial inoculation with R. solani AG 3-PT. Results indicated that the R. solani AG 3-PT caused dysbiosis in the potato soil microbiome in both soils, leading to a shift in the fungal and bacterial community composition. However, soil microbial extracellular enzyme activities revealed that only the KwaZulu-Natal soil exhibited potential functional changes. Furthermore, the results from the disease assessment showed that the KwaZulu-Natal soil showed an overall lower disease index as compared to the Sandveld soil. These findings highlight the fact that the KwaZulu-Natal soil demonstrates a more robust soil microbiome with the potential to suppress R. solani AG 3-PT as compared to the Sandveld soil. Differentially abundant fungal and bacterial taxa in R. solani AG 3-PT inoculated soils suggest a promising potential for disease-suppressive microbial indicators against the pathogen. Network analysis further provided insight into the presence of key microbial taxa involved in the microbial community shifts, which could support their role in the suppression of R. solani AG 3-PT. The utilization of high-throughput amplicon sequencing and advanced bioinformatic methods in this study, shed light on the intricate shifts in the soil microbiome upon R. solani AG 3-PT infection of potatoes. Moreover, this study provides a comprehensive framework for identifying potential disease-suppressive microbes and/or microbial groups against R. solani AG 3-PT that can facilitate future studies investigating potential biocontrol agents. The identification of these key microbial indicators against Rhizoctonia diseases will contribute to the development of environmentally sustainable potato production systems, which are particularly important considering the implementation of the European Green Deal.