Long-term push–pull cropping system shifts soil and maize-root microbiome diversity paving way to resilient farming system

(2024) 24:92 Jalloh et al. BMC Microbiology https://doi.org/10.1186/s12866-024-03238-z BMC Microbiology Open Access RESEARCH Long‑term push–pull cropping system shifts soil and maize‑root microbiome diversity paving way to resilient farming system Abdul A. Jalloh1,2, Fathiya Mbarak Khamis1, Abdullahi Ahmed Yusuf2,3, Sevgan Subramanian1 and Daniel Munyao Mutyambai1,4* Abstract Background The soil biota consists of a complex assembly of microbial communities and other organisms that vary significantly across farming systems, impacting soil health and plant productivity. Despite its importance, there has been limited exploration of how different cropping systems influence soil and plant root microbiomes. In this study, we investigated soil physicochemical properties, along with soil and maize-root microbiomes, in an agroecological cereal-legume companion cropping system known as push–pull technology (PPT). This system has been used in agriculture for over two decades for insect-pest management, soil health improvement, and weed control in subSaharan Africa. We compared the results with those obtained from maize-monoculture (Mono) cropping system. Results The PPT cropping system changed the composition and diversity of soil and maize-root microbial communities, and led to notable improvements in soil physicochemical characteristics compared to that of the Mono cropping system. Distinct bacterial and fungal genera played a crucial role in influencing the variation in microbial diversity within these cropping systems. The relative abundance of fungal genera Trichoderma, Mortierella, and Bionectria and bacterial genera Streptomyces, RB41, and Nitrospira were more enriched in PPT. These microbial communities are associated with essential ecosystem services such as plant protection, decomposition, carbon utilization, bioinsecticides production, nitrogen fixation, nematode suppression, phytohormone production, and bioremediation. Conversely, pathogenic associated bacterial genus including Bryobacter were more enriched in Mono-root. Additionally, the Mono system exhibited a high relative abundance of fungal genera such as Gibberella, Neocosmospora, and Aspergillus, which are linked to plant diseases and food contamination. Significant differences were observed in the relative abundance of the inferred metabiome functional protein pathways including syringate degradation, L-methionine biosynthesis I, and inosine 5’-phosphate degradation. Conclusion Push–pull cropping system positively influences soil and maize-root microbiomes and enhances soil physicochemical properties. This highlights its potential for agricultural and environmental sustainability. These findings contribute to our understanding of the diverse ecosystem services offered by this cropping system where it is practiced regarding the system’s resilience and functional redundancy. Future research should focus on whether PPT affects the soil and maize-root microbial communities through the release of plant metabolites from the intercrop root exudates or through the alteration of the soil’s nutritional status, which affects microbial enzymatic activities. *Correspondence: Daniel Munyao Mutyambai Full list of author information is available at the end of the article © The Author(s) 2024. Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Jalloh et al. BMC Microbiology (2024) 24:92 Page 2 of 23 Keywords Agroecosystem sustainability, Amplicon sequencing, Cropping system, Ecosystem services, Soil and maize-root microbiomes, Soil health Introduction To feed the growing world population, agricultural intensification in staple food crop production such as maize, wheat, and rice has been increasing, leading to increased food security [1, 2]. However, this intensification has also had negative environmental consequences, including increased greenhouse gas emissions, nutrient leaching, soil erosion, and a decline in biodiversity [3, 4]. Ecological diversification that prioritizes environmental quality and preserves beneficial organisms is needed to mitigate these impacts [5–8]. Diversification involves agronomic practices that improve productivity while maintaining long-term stability and resilience and supporting ecosystem services [9]. Intercropping, where farmers grow two or more crops together in an agricultural field, is one such diversification strategy that has been shown to restore ecosystem services and revitalize soil and its associated biodiversity while improving crop yields [2, 10–13]. One such intercropping system that has gained traction in sub-Saharan Africa (SSA) is the push–pull technology (PPT), that has been adopted by thousands of smallholder farmers in East and Southern Africa [14, 15]. Push–pull is an agroecological companion cropping system where the main crop (maize or sorghum) is intercropped with a leguminous plant (Desmodium spp.) which serves as an insect-repellent (push), while a grass (Napier or Briachiaria) is planted as a border crop to attract stemborers and other herbivores away from the main crop (pull) [16– 18]. The push–pull cropping system being a perennial legume-maize intercrop is likely to impact the soil and maize-root microbial communities strongly. The PPT cropping system utilizes volatile chemical mediated tritrophic interactions where volatile signals emitted by the leguminous plant create an unfavorable environment for oviposition by insect-pests such as Busseola fusca, Chilo partellus, and more recently Spodoptera frugiperda [18– 20]. Desmodium spp. volatiles are also known to recruit the pests’ natural enemies into the cropping system [14, 20]. The trap crop suppresses the larval development of the insect pest upon hatching from the oviposited eggs [13, 14, 16]. Additional ecological benefits of using PPT include reducing the use of synthetic chemical pesticides and controlling the parasitic weed (Striga hermonthica) through the allelopathic effects of the root exudates of the (...truncated)