Frontiers in Microbiology 01 frontiersin.org Olive agroforestry shapes rhizosphere microbiome networks associated with annual crops and impacts the biomass production under low-rainfed conditions Ameni Ben zineb 1 , Karim Barkaoui 2,3 , Fatma Karray 4 , Najla Mhiri 4 , Sami Sayadi 5 , Ahmed Mliki 1 and Mahmoud Gargouri 1 * 1 Laboratory of Plant Molecular Physiology, Centre of Biotechnology of Borj-Cedria, Hammam-Lif, Tunisia, 2 CIRAD, UMR ABSys, Montpellier, France, 3 ABSys, Univ Montpellier, CIHEAM-IAMM, CIRAD, INRAE, Institut Agro, Montpellier, France, 4 Laboratory of Environmental Bioprocesses, Centre of Biotechnology of Sfax, Sfax, Tunisia, 5 Biotechnology Program, Center for Sustainable Development, College of Arts and Sciences, Qatar University, Doha, Qatar Agroforestry (AF) is a promising land-use system to mitigate water defciency, particularly in semi-arid areas. However, the belowground microbes associated with crops below trees remain seldom addressed. This study aimed at elucidating the efects of olive AF system intercropped with durum wheat (Dw), barely (Ba), chickpea (Cp), or faba bean (Fb) on crops biomass and their soil-rhizosphere microbial networks as compared to conventional full sun cropping (SC) under rainfed conditions. To test the hypothesis, we compared the prokaryotic and the fungal communities inhabiting the rhizosphere of two cereals and legumes grown either in AF or SC. We determined the most suitable annual crop species in AF under low-rainfed conditions. Moreover, to deepen our understanding of the rhizosphere network dynamics of annual crops under AF and SC systems, we characterized the microbial hubs that are most likely responsible for modifying the microbial community structure and the variability of crop biomass of each species. Herein, we found that cereals produced signifcantly more above-ground biomass than legumes following in descending order: Ba > Dw > Cp > Fb, suggesting that crop species play a signifcant role in improving soil water use and that cereals are well-suited to rainfed conditions within both types of agrosystems. The type of agrosystem shapes crop microbiomes with the only marginal infuence of host selection. However, more relevant was to unveil those crops recruits specifc bacterial and fungal taxa from the olive-belowground communities. Of the selected soil physicochemical properties, organic matter was the principal driver in shaping the soil microbial structure in the AF system. The co-occurrence network analyses indicated that the AF system generates higher ecological stability than the SC system under stressful climate conditions. Furthermore, legumes’ rhizosphere microbiome possessed a higher resilient capacity than cereals. We also identifed diferent fungal keystones involved in litter decomposition and drought tolerance within AF systems facing the water-scarce condition and TYPE Original Research PUBLISHED 28 October 2022 DOI 10.3389/fmicb.2022.977797 OPEN ACCESS EDITED BY Blanca B. Landa, Institute for Sustainable Agriculture (CSIC), Spain REVIEWED BY Carmen Gómez-Lama Cabanás, Institute for Sustainable Agriculture (CSIC), Spain Elizabeth Temitope Alori, Landmark University, Nigeria Alexandre Barretto De Menezes, National University of Ireland, Ireland *CORRESPONDENCE Mahmoud Gargouri mahmoud.gargouri@cbbc.rnrt.tn SPECIALTY SECTION This article was submitted to Microbe and Virus Interactions with Plants, a section of the journal Frontiers in Microbiology RECEIVED 24 June 2022 ACCEPTED 06 October 2022 PUBLISHED 28 October 2022 CITATION Ben zineb A, Barkaoui K, Karray F, Mhiri N, Sayadi S, Mliki A and Gargouri M (2022) Olive agroforestry shapes rhizosphere microbiome networks associated with annual crops and impacts the biomass production under low-rainfed conditions. Front. Microbiol. 13:977797. doi: 10.3389/fmicb.2022.977797 COPYRIGHT © 2022 Ben zineb, Barkaoui, Karray, Mhiri, Sayadi, Mliki and Gargouri. This is an open- access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.