Meloidogyne incognita parasitism is affected by Pseudomonas protegens CHA0 and its effects on tomato-associated microbiota

Abstract Background The multitrophic interactions in plant rhizosphere and endosphere can be beneficial or deleterious for the plant health. The parasitism by root-feeding nematodes is on the negative end of the interaction spectrum, and may be very difficult to control. Biological agents are a prom...

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Main Authors: Olivera Topalović, Enoch Narh Kudjordjie, Sanea Sheikh, Gnimavo Bonaventure Kenou, Frederik Bak, Flemming Ekelund, Mette Vestergård
Format: Article
Language:English
Published: BMC 2025-07-01
Series:Environmental Microbiome
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Online Access:https://doi.org/10.1186/s40793-025-00743-0
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author Olivera Topalović
Enoch Narh Kudjordjie
Sanea Sheikh
Gnimavo Bonaventure Kenou
Frederik Bak
Flemming Ekelund
Mette Vestergård
author_facet Olivera Topalović
Enoch Narh Kudjordjie
Sanea Sheikh
Gnimavo Bonaventure Kenou
Frederik Bak
Flemming Ekelund
Mette Vestergård
author_sort Olivera Topalović
collection DOAJ
description Abstract Background The multitrophic interactions in plant rhizosphere and endosphere can be beneficial or deleterious for the plant health. The parasitism by root-feeding nematodes is on the negative end of the interaction spectrum, and may be very difficult to control. Biological agents are a promising alternative to the environmentally harmful nematicides; however, their efficiency in natural soil often seems to be low due to their limited establishment and dispersal. Thus, understanding how the introduced biological agents interact with nematodes and the surrounding microbiota is necessary to improve sustainable management of root-feeding nematodes. Here, we conducted two experiments to study the effects of Pseudomonas protegens strain CHA0 (CHA0) on the performance of the root-knot nematode Meloidogyne incognita. In the first experiment, we compared M. incognita performance in natural and sterilized soil in the presence and absence of CHA0. In the second experiment, we studied the composition of microbes in the rhizosphere and endosphere of tomato plants grown in native soil in response to M. incognita and CHA0. Results We found that nematode performance, especially nematode reproduction, was significantly increased in native soil amended with CHA0. In addition, we found the highest relative abundance of Pseudomonas in tomato endosphere in response to nematode co-inoculations with CHA0, which suggests that root wounding, caused by nematodes, increased the entrance of inoculated and/or native Pseudomonas spp. As many Pseudomonas spp. are plant growth promoting, this may explain that plant growth was highest in this treatment. Furthermore, the rhizosphere of nematode-inoculated plants was enriched with Flavobacterium, Hydrogenophaga and Variovorax, which are genera generally associated with nematode-suppressive soils. On the other hand, other known nematode-suppressive genera such as Bacillus, Lysobacter, Devosia and Rhizobium were depleted in plants where nematodes were co-inoculated with CHA0, which may explain the higher nematode performance when plants were co-inoculated with CHA0. Conclusions Our findings show that the effect of P. protegens strain CHA0 on M. incognita parasitism is influenced by the multitrophic interactions in the rhizosphere and endosphere of tomato plants. We must understand these interactions thoroughly to optimize sustainable means to mitigate the root-knot nematodes.
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spelling doaj-art-e39d042a47a8498a873d8a20fa5ee90d2025-08-20T04:01:35ZengBMCEnvironmental Microbiome2524-63722025-07-0120111210.1186/s40793-025-00743-0Meloidogyne incognita parasitism is affected by Pseudomonas protegens CHA0 and its effects on tomato-associated microbiotaOlivera Topalović0Enoch Narh Kudjordjie1Sanea Sheikh2Gnimavo Bonaventure Kenou3Frederik Bak4Flemming Ekelund5Mette Vestergård6Department of Biology, Section of Terrestrial Ecology, University of CopenhagenDepartment of Agroecology, Section for Plant Pathology and Microbiology, Aarhus UniversityDepartment of Biology, Section of Terrestrial Ecology, University of CopenhagenDepartment of Agroecology, Section for Plant Pathology and Microbiology, Aarhus UniversityDepartment of Plant and Environmental Sciences, University of CopenhagenDepartment of Biology, Section of Terrestrial Ecology, University of CopenhagenDepartment of Agroecology, Section for Plant Pathology and Microbiology, Aarhus UniversityAbstract Background The multitrophic interactions in plant rhizosphere and endosphere can be beneficial or deleterious for the plant health. The parasitism by root-feeding nematodes is on the negative end of the interaction spectrum, and may be very difficult to control. Biological agents are a promising alternative to the environmentally harmful nematicides; however, their efficiency in natural soil often seems to be low due to their limited establishment and dispersal. Thus, understanding how the introduced biological agents interact with nematodes and the surrounding microbiota is necessary to improve sustainable management of root-feeding nematodes. Here, we conducted two experiments to study the effects of Pseudomonas protegens strain CHA0 (CHA0) on the performance of the root-knot nematode Meloidogyne incognita. In the first experiment, we compared M. incognita performance in natural and sterilized soil in the presence and absence of CHA0. In the second experiment, we studied the composition of microbes in the rhizosphere and endosphere of tomato plants grown in native soil in response to M. incognita and CHA0. Results We found that nematode performance, especially nematode reproduction, was significantly increased in native soil amended with CHA0. In addition, we found the highest relative abundance of Pseudomonas in tomato endosphere in response to nematode co-inoculations with CHA0, which suggests that root wounding, caused by nematodes, increased the entrance of inoculated and/or native Pseudomonas spp. As many Pseudomonas spp. are plant growth promoting, this may explain that plant growth was highest in this treatment. Furthermore, the rhizosphere of nematode-inoculated plants was enriched with Flavobacterium, Hydrogenophaga and Variovorax, which are genera generally associated with nematode-suppressive soils. On the other hand, other known nematode-suppressive genera such as Bacillus, Lysobacter, Devosia and Rhizobium were depleted in plants where nematodes were co-inoculated with CHA0, which may explain the higher nematode performance when plants were co-inoculated with CHA0. Conclusions Our findings show that the effect of P. protegens strain CHA0 on M. incognita parasitism is influenced by the multitrophic interactions in the rhizosphere and endosphere of tomato plants. We must understand these interactions thoroughly to optimize sustainable means to mitigate the root-knot nematodes.https://doi.org/10.1186/s40793-025-00743-0Root-feeding nematodesMeloidogynePseudomonas16S rRNA geneITS regionPlant growth
spellingShingle Olivera Topalović
Enoch Narh Kudjordjie
Sanea Sheikh
Gnimavo Bonaventure Kenou
Frederik Bak
Flemming Ekelund
Mette Vestergård
Meloidogyne incognita parasitism is affected by Pseudomonas protegens CHA0 and its effects on tomato-associated microbiota
Environmental Microbiome
Root-feeding nematodes
Meloidogyne
Pseudomonas
16S rRNA gene
ITS region
Plant growth
title Meloidogyne incognita parasitism is affected by Pseudomonas protegens CHA0 and its effects on tomato-associated microbiota
title_full Meloidogyne incognita parasitism is affected by Pseudomonas protegens CHA0 and its effects on tomato-associated microbiota
title_fullStr Meloidogyne incognita parasitism is affected by Pseudomonas protegens CHA0 and its effects on tomato-associated microbiota
title_full_unstemmed Meloidogyne incognita parasitism is affected by Pseudomonas protegens CHA0 and its effects on tomato-associated microbiota
title_short Meloidogyne incognita parasitism is affected by Pseudomonas protegens CHA0 and its effects on tomato-associated microbiota
title_sort meloidogyne incognita parasitism is affected by pseudomonas protegens cha0 and its effects on tomato associated microbiota
topic Root-feeding nematodes
Meloidogyne
Pseudomonas
16S rRNA gene
ITS region
Plant growth
url https://doi.org/10.1186/s40793-025-00743-0
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