Effective combination of arugula vermicompost, chitin and inhibitory bacteria for suppression of the root-knot nematode Meloidogyne javanica and explanation of their beneficial properties based on microbial analysis

PLOS ONE RESEARCH ARTICLE Effective combination of arugula vermicompost, chitin and inhibitory bacteria for suppression of the root-knot nematode Meloidogyne javanica and explanation of their beneficial properties based on microbial analysis a1111111111 a1111111111 a1111111111 a1111111111 a1111111111 OPEN ACCESS Citation: Rostami M, Karegar A, Taghavi SM, Ghasemi-Fasaei R, Ghorbani A (2023) Effective combination of arugula vermicompost, chitin and inhibitory bacteria for suppression of the root-knot nematode Meloidogyne javanica and explanation of their beneficial properties based on microbial analysis. PLoS ONE 18(8): e0289935. https://doi. org/10.1371/journal.pone.0289935 Editor: Raja Aadil Hussain Bhat, ICAR - Directorate of Coldwater Fisheries Research, INDIA Received: December 16, 2022 Accepted: July 28, 2023 Published: August 16, 2023 Peer Review History: PLOS recognizes the benefits of transparency in the peer review process; therefore, we enable the publication of all of the content of peer review and author responses alongside final, published articles. The editorial history of this article is available here: https://doi.org/10.1371/journal.pone.0289935 Copyright: © 2023 Rostami et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Mahsa Rostami1, Akbar Karegar ID1*, S. Mohsen Taghavi1, Reza Ghasemi-Fasaei2, Abozar Ghorbani3¤ 1 Department of Plant Protection, School of Agriculture, Shiraz University, Shiraz, Iran, 2 Department of Soil Science, School of Agriculture, Shiraz University, Shiraz, Iran, 3 Plant Virology Research Centre, School of Agriculture, Shiraz University, Shiraz, Iran ¤ Current address: Nuclear Agriculture Research School, Nuclear Science and Technology Research Institute (NSTRI), Atomic Energy Organization of Iran (AEOI), Karaj, Iran * Abstract Root-knot nematodes (Meloidogyne spp.) are dangerous parasites of many crops worldwide. The threat of chemical nematicides has led to increasing interest in studying the inhibitory effects of organic amendments and bacteria on plant-parasitic nematodes, but their combination has been less studied. One laboratory and four glasshouse experiments were conducted to study the effect on M. javanica of animal manure, common vermicompost, shrimp shells, chitosan, compost and vermicompost from castor bean, chinaberry and arugula, and the combination of arugula vermicompost with some bacteria, isolated from vermicompost or earthworms. The extract of arugula compost and vermicompost, common vermicompost and composts from castor bean and chinaberry reduced nematode egg hatch by 12–32% and caused 13–40% mortality of second-stage juveniles in vitro. Soil amendments with the combination vermicompost of arugula + Pseudomonas. resinovorans + Sphingobacterium daejeonense + chitosan significantly increased the yield of infected tomato plants and reduced nematode reproduction factor by 63.1–76.6%. Comparison of chemical properties showed that arugula vermicompost had lower pH, EC, and C/N ratio than arugula compost. Metagenomics analysis showed that Bacillus, Geodermatophilus, Thermomonas, Lewinella, Pseudolabrys and Erythrobacter were the major bacterial genera in the vermicompost of arugula. Metagenomics analysis confirmed the presence of chitinolytic, detoxifying and PGPR bacteria in the vermicompost of arugula. The combination of arugula vermicompost + chitosan + P. resinovorans + S. daejeonense could be an environmentally friendly approach to control M. javanica. PLOS ONE | https://doi.org/10.1371/journal.pone.0289935 August 16, 2023 1 / 24 PLOS ONE Data Availability Statement: All relevant data are within the paper and its Supporting Information files. Funding: The authors gratefully acknowledge the financial support from Shiraz University. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing interests: The authors declare no conflict of interest Effective combination of arugula vermicompost, chitin and bacteria for suppression of Meloidogyne javanica Introduction Root-knot nematodes (Meloidogyne spp.) are among the most damaging agricultural pests and cause significant economic losses. They specifically attack the root vascular system and cause nutrient deficiencies in the host and disruption of water transport. Visible aboveground symptoms include stunted growth, wilting, chlorosis, and lower crop yields. These parasites have a remarkable ability to infect and multiply in the roots of numerous plant species, which can even lead to crop failure. Conventional approaches to nematode control, such as chemical nematicides, have proven effective to some degree, but are associated with serious environmental and health concerns. Many efforts have been made to direct the management of plant parasitic nematodes towards environmentally friendly methods [1,2]. Increasing awareness of the harmful effects of chemical pesticides on the environment, non-target organisms, and human health has increased the need for alternative, environmentally friendly, and sustainable solutions [3]. In this context, the use of organic amendments, beneficial microorganisms and natural compounds has emerged as a promising strategy for nematode control in agriculture [4]. Among these strategies, the use of organic soil amendments such as compost and vermicompost is an effective method for the control of plant parasitic nematodes that could improve soil quality and plant health [5]. Vermicompost is a soil amendment and a biological control agent against fungi and bacteria that can improve plant growth and resistance to agricultural pests [6]. The liquid extract of vermicompost (vermiwash), which contains proteins, enzymes, vitamins, hormones, bioavailable minerals and decomposing bacteria, can suppress plant pathogens and increase crop productivity [7]. The application of biochar and vermicompost has demonstrated its effectiveness in mitigating the stress caused by the rice root-knot nematode M. graminicola. In particular, the application of 1.2% biochar and 5% vermicompost has shown promising results in controlling the infestation of rice plants [8]. In vitro evaluations of vermicompost and its extracts on tomato root-knot nematodes also showed promising results. As the concentration of vermicompost extract increased, the hatching rate of eggs decreased and the mortality rate of M. incognita second-stage juveniles (J2s) increased significantly. In addition, application of vermicompost in pot experiments with tomato plants resulted in reduction in the number of root knots, indicating its potential as an effective nematode control agent [9]. Different types of vermicompost derived from different plant wastes have dissimilar effects on nematode-infected plants. For exampl (...truncated)