Transient colonization by Priestia megaterium B1L5 alters the structure of the rhizosphere microbiome towards potential plant beneficial bacterial groups in apple plantlets

Abstract Background Plant growth-promoting bacteria (PGPB) can beneficially modulate rhizosphere microbial communities, potentially improving plant health and reducing disease incidence. Limited research exists on the influence of PGPB inoculation on the rhizosphere microbial communities of apple pl...

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Main Authors: Fatma M. Mahmoud, Holger Edelmann, Yang Si, Lea Endrejat, Karin Pritsch, Caroline Gutjahr, Armin Ehrenreich, Traud Winkelmann, Jana Barbro Winkler, Jörg‑Peter Schnitzler, Michael Schloter
Format: Article
Language:English
Published: BMC 2025-08-01
Series:Environmental Microbiome
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Online Access:https://doi.org/10.1186/s40793-025-00762-x
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author Fatma M. Mahmoud
Holger Edelmann
Yang Si
Lea Endrejat
Karin Pritsch
Caroline Gutjahr
Armin Ehrenreich
Traud Winkelmann
Jana Barbro Winkler
Jörg‑Peter Schnitzler
Michael Schloter
author_facet Fatma M. Mahmoud
Holger Edelmann
Yang Si
Lea Endrejat
Karin Pritsch
Caroline Gutjahr
Armin Ehrenreich
Traud Winkelmann
Jana Barbro Winkler
Jörg‑Peter Schnitzler
Michael Schloter
author_sort Fatma M. Mahmoud
collection DOAJ
description Abstract Background Plant growth-promoting bacteria (PGPB) can beneficially modulate rhizosphere microbial communities, potentially improving plant health and reducing disease incidence. Limited research exists on the influence of PGPB inoculation on the rhizosphere microbial communities of apple plants, particularly in soils affected by apple replant disease (ARD). Here, we evaluated the capacity of GFP-labelled Priestia megaterium B1 (designated as P. megaterium B1L5) to colonize the roots of apple plantlets grown in two soils: ARD-affected soil and ARD-unaffected grass soil. We investigated its influence on plant growth in ARD-affected soil and its potential to mitigate ARD-related symptoms. We also assessed how its inoculation modulates the rhizosphere microbial communities, with emphasis on changes that may support plant health, particularly in ARD-affected soils. Results P. megaterium B1L5 successfully colonized apple roots in both soils 6 days post-inoculation (dpi), but was not detectable at 33 dpi. In ARD-affected soil, plants inoculated with vegetative cells or spores displayed a lower proportion of blackened root tips compared to uninoculated controls. Beta diversity and PERMANOVA analyses demonstrated a significant influence of inoculation on the bacterial communities in both soils at 6 and 33 dpi (p = 0.001). Furthermore, inoculation enriched the rhizosphere of apple plantlets with potential plant-beneficial bacteria, such as Luteimonas, Lysobacter, Pseudomonas, Sphingomonas, Sphingobacterium, Rhodanobacter, Pedobacter and Flavobacterium. In contrast, fungal communities remained largely unaffected by inoculation. Most bacterial and fungal shifts observed in the rhizosphere of inoculated plantlets at 33 dpi did not exhibit similar patterns in uninoculated controls over time, indicating that these shifts were largely driven by the inoculum rather than by plant development or natural microbial succession. Conclusions Our results highlight the capacity of P. megaterium B1L5’s to transiently colonize apple plant roots across different soil environments. The observed tendency toward reduced root tip blackening in inoculated plants grown in ARD-affected plants reflects its potential for alleviating stress associated with ARD. Additionally, inoculation with P. megaterium B1L5 promoted beneficial shifts in the rhizosphere microbiome by enriching bacterial taxa commonly linked to plant health. These findings indicate that P. megaterium B1L5 presents a candidate for ARD mitigation, however its long-term efficacy and practical application should be further evaluated.
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spelling doaj-art-643f2f0a1bac4a75b36a2e7a0155e0e32025-08-20T04:02:41ZengBMCEnvironmental Microbiome2524-63722025-08-0120112210.1186/s40793-025-00762-xTransient colonization by Priestia megaterium B1L5 alters the structure of the rhizosphere microbiome towards potential plant beneficial bacterial groups in apple plantletsFatma M. Mahmoud0Holger Edelmann1Yang Si2Lea Endrejat3Karin Pritsch4Caroline Gutjahr5Armin Ehrenreich6Traud Winkelmann7Jana Barbro Winkler8Jörg‑Peter Schnitzler9Michael Schloter10Research Unit for Comparative Microbiome Analysis, Helmholtz Munich, German Research Center for Environmental HealthChair of Microbiology, TUM School of Life Sciences, Technical University of MunichPlant Genetics, TUM School of Life Sciences, Technical University of MunichResearch Unit for Comparative Microbiome Analysis, Helmholtz Munich, German Research Center for Environmental HealthResearch Unit for Environmental Simulations, Helmholtz Munich, German Research Center for Environmental HealthPlant Genetics, TUM School of Life Sciences, Technical University of MunichChair of Microbiology, TUM School of Life Sciences, Technical University of MunichInstitute of Plant Genetics, Leibniz University HannoverResearch Unit for Environmental Simulations, Helmholtz Munich, German Research Center for Environmental HealthResearch Unit for Environmental Simulations, Helmholtz Munich, German Research Center for Environmental HealthResearch Unit for Comparative Microbiome Analysis, Helmholtz Munich, German Research Center for Environmental HealthAbstract Background Plant growth-promoting bacteria (PGPB) can beneficially modulate rhizosphere microbial communities, potentially improving plant health and reducing disease incidence. Limited research exists on the influence of PGPB inoculation on the rhizosphere microbial communities of apple plants, particularly in soils affected by apple replant disease (ARD). Here, we evaluated the capacity of GFP-labelled Priestia megaterium B1 (designated as P. megaterium B1L5) to colonize the roots of apple plantlets grown in two soils: ARD-affected soil and ARD-unaffected grass soil. We investigated its influence on plant growth in ARD-affected soil and its potential to mitigate ARD-related symptoms. We also assessed how its inoculation modulates the rhizosphere microbial communities, with emphasis on changes that may support plant health, particularly in ARD-affected soils. Results P. megaterium B1L5 successfully colonized apple roots in both soils 6 days post-inoculation (dpi), but was not detectable at 33 dpi. In ARD-affected soil, plants inoculated with vegetative cells or spores displayed a lower proportion of blackened root tips compared to uninoculated controls. Beta diversity and PERMANOVA analyses demonstrated a significant influence of inoculation on the bacterial communities in both soils at 6 and 33 dpi (p = 0.001). Furthermore, inoculation enriched the rhizosphere of apple plantlets with potential plant-beneficial bacteria, such as Luteimonas, Lysobacter, Pseudomonas, Sphingomonas, Sphingobacterium, Rhodanobacter, Pedobacter and Flavobacterium. In contrast, fungal communities remained largely unaffected by inoculation. Most bacterial and fungal shifts observed in the rhizosphere of inoculated plantlets at 33 dpi did not exhibit similar patterns in uninoculated controls over time, indicating that these shifts were largely driven by the inoculum rather than by plant development or natural microbial succession. Conclusions Our results highlight the capacity of P. megaterium B1L5’s to transiently colonize apple plant roots across different soil environments. The observed tendency toward reduced root tip blackening in inoculated plants grown in ARD-affected plants reflects its potential for alleviating stress associated with ARD. Additionally, inoculation with P. megaterium B1L5 promoted beneficial shifts in the rhizosphere microbiome by enriching bacterial taxa commonly linked to plant health. These findings indicate that P. megaterium B1L5 presents a candidate for ARD mitigation, however its long-term efficacy and practical application should be further evaluated.https://doi.org/10.1186/s40793-025-00762-xApple replant disease (ARD)Plant growth-promoting bacteria (PGPB)GFP-labelled mutantRoot colonizationRhizosphere microbial communityMetabarcoding
spellingShingle Fatma M. Mahmoud
Holger Edelmann
Yang Si
Lea Endrejat
Karin Pritsch
Caroline Gutjahr
Armin Ehrenreich
Traud Winkelmann
Jana Barbro Winkler
Jörg‑Peter Schnitzler
Michael Schloter
Transient colonization by Priestia megaterium B1L5 alters the structure of the rhizosphere microbiome towards potential plant beneficial bacterial groups in apple plantlets
Environmental Microbiome
Apple replant disease (ARD)
Plant growth-promoting bacteria (PGPB)
GFP-labelled mutant
Root colonization
Rhizosphere microbial community
Metabarcoding
title Transient colonization by Priestia megaterium B1L5 alters the structure of the rhizosphere microbiome towards potential plant beneficial bacterial groups in apple plantlets
title_full Transient colonization by Priestia megaterium B1L5 alters the structure of the rhizosphere microbiome towards potential plant beneficial bacterial groups in apple plantlets
title_fullStr Transient colonization by Priestia megaterium B1L5 alters the structure of the rhizosphere microbiome towards potential plant beneficial bacterial groups in apple plantlets
title_full_unstemmed Transient colonization by Priestia megaterium B1L5 alters the structure of the rhizosphere microbiome towards potential plant beneficial bacterial groups in apple plantlets
title_short Transient colonization by Priestia megaterium B1L5 alters the structure of the rhizosphere microbiome towards potential plant beneficial bacterial groups in apple plantlets
title_sort transient colonization by priestia megaterium b1l5 alters the structure of the rhizosphere microbiome towards potential plant beneficial bacterial groups in apple plantlets
topic Apple replant disease (ARD)
Plant growth-promoting bacteria (PGPB)
GFP-labelled mutant
Root colonization
Rhizosphere microbial community
Metabarcoding
url https://doi.org/10.1186/s40793-025-00762-x
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