Bacterial Community Structure Dynamics in <italic toggle="yes">Meloidogyne incognita</italic>-Infected Roots and Its Role in Worm-Microbiome Interactions

ABSTRACT Plant parasitic nematodes such as Meloidogyne incognita have a complex life cycle, occurring sequentially in various niches of the root and rhizosphere. They are known to form a range of interactions with bacteria and other microorganisms that can affect their densities and virulence. High-...

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Autores principales: Timur M. Yergaliyev, Rivka Alexander-Shani, Hana Dimerets, Shimon Pivonia, David McK. Bird, Shimon Rachmilevitch, Amir Szitenberg
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Publicado: American Society for Microbiology 2020
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spelling oai:doaj.org-article:93e911e166964ec5b26428c493c61c612021-11-15T15:30:50ZBacterial Community Structure Dynamics in <italic toggle="yes">Meloidogyne incognita</italic>-Infected Roots and Its Role in Worm-Microbiome Interactions10.1128/mSphere.00306-202379-5042https://doaj.org/article/93e911e166964ec5b26428c493c61c612020-08-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSphere.00306-20https://doaj.org/toc/2379-5042ABSTRACT Plant parasitic nematodes such as Meloidogyne incognita have a complex life cycle, occurring sequentially in various niches of the root and rhizosphere. They are known to form a range of interactions with bacteria and other microorganisms that can affect their densities and virulence. High-throughput sequencing can reveal these interactions in high temporal and geographic resolutions, although thus far we have only scratched the surface. In this study, we have carried out a longitudinal sampling scheme, repeatedly collecting rhizosphere soil, roots, galls, and second-stage juveniles from 20 plants to provide a high-resolution view of bacterial succession in these niches, using 16S rRNA metabarcoding. Our findings indicate that a structured community develops in the root, in which gall communities diverge from root segments lacking a gall, and that this structure is maintained throughout the crop season. We describe the successional process leading toward this structure, which is driven by interactions with the nematode and later by an increase in bacteria often found in hypoxic and anaerobic environments. We present evidence that this structure may play a role in the nematode’s chemotaxis toward uninfected root segments. Finally, we describe the J2 epibiotic microenvironment as ecologically deterministic, in part, due to the active bacterial attraction of second-stage juveniles. IMPORTANCE The study of high-resolution successional processes within tightly linked microniches is rare. Using the power and relatively low cost of metabarcoding, we describe the bacterial succession and community structure in roots infected with root-knot nematodes and in the nematodes themselves. We reveal separate successional processes in galls and adjacent non-gall root sections, which are driven by the nematode’s life cycle and the progression of the crop season. With their relatively low genetic diversity, large geographic range, spatially complex life cycle, and the simplified agricultural ecosystems they occupy, root-knot nematodes can serve as a model organism for terrestrial holobiont ecology. This perspective can improve our understanding of the temporal and spatial aspects of biological control efficacy.Timur M. YergaliyevRivka Alexander-ShaniHana DimeretsShimon PivoniaDavid McK. BirdShimon RachmilevitchAmir SzitenbergAmerican Society for MicrobiologyarticleMeloidogyne incognitabacterial successionmicrobiomeplant-microbe interactionsroot knot nematodeMicrobiologyQR1-502ENmSphere, Vol 5, Iss 4 (2020)
institution DOAJ
collection DOAJ
language EN
topic Meloidogyne incognita
bacterial succession
microbiome
plant-microbe interactions
root knot nematode
Microbiology
QR1-502
spellingShingle Meloidogyne incognita
bacterial succession
microbiome
plant-microbe interactions
root knot nematode
Microbiology
QR1-502
Timur M. Yergaliyev
Rivka Alexander-Shani
Hana Dimerets
Shimon Pivonia
David McK. Bird
Shimon Rachmilevitch
Amir Szitenberg
Bacterial Community Structure Dynamics in <italic toggle="yes">Meloidogyne incognita</italic>-Infected Roots and Its Role in Worm-Microbiome Interactions
description ABSTRACT Plant parasitic nematodes such as Meloidogyne incognita have a complex life cycle, occurring sequentially in various niches of the root and rhizosphere. They are known to form a range of interactions with bacteria and other microorganisms that can affect their densities and virulence. High-throughput sequencing can reveal these interactions in high temporal and geographic resolutions, although thus far we have only scratched the surface. In this study, we have carried out a longitudinal sampling scheme, repeatedly collecting rhizosphere soil, roots, galls, and second-stage juveniles from 20 plants to provide a high-resolution view of bacterial succession in these niches, using 16S rRNA metabarcoding. Our findings indicate that a structured community develops in the root, in which gall communities diverge from root segments lacking a gall, and that this structure is maintained throughout the crop season. We describe the successional process leading toward this structure, which is driven by interactions with the nematode and later by an increase in bacteria often found in hypoxic and anaerobic environments. We present evidence that this structure may play a role in the nematode’s chemotaxis toward uninfected root segments. Finally, we describe the J2 epibiotic microenvironment as ecologically deterministic, in part, due to the active bacterial attraction of second-stage juveniles. IMPORTANCE The study of high-resolution successional processes within tightly linked microniches is rare. Using the power and relatively low cost of metabarcoding, we describe the bacterial succession and community structure in roots infected with root-knot nematodes and in the nematodes themselves. We reveal separate successional processes in galls and adjacent non-gall root sections, which are driven by the nematode’s life cycle and the progression of the crop season. With their relatively low genetic diversity, large geographic range, spatially complex life cycle, and the simplified agricultural ecosystems they occupy, root-knot nematodes can serve as a model organism for terrestrial holobiont ecology. This perspective can improve our understanding of the temporal and spatial aspects of biological control efficacy.
format article
author Timur M. Yergaliyev
Rivka Alexander-Shani
Hana Dimerets
Shimon Pivonia
David McK. Bird
Shimon Rachmilevitch
Amir Szitenberg
author_facet Timur M. Yergaliyev
Rivka Alexander-Shani
Hana Dimerets
Shimon Pivonia
David McK. Bird
Shimon Rachmilevitch
Amir Szitenberg
author_sort Timur M. Yergaliyev
title Bacterial Community Structure Dynamics in <italic toggle="yes">Meloidogyne incognita</italic>-Infected Roots and Its Role in Worm-Microbiome Interactions
title_short Bacterial Community Structure Dynamics in <italic toggle="yes">Meloidogyne incognita</italic>-Infected Roots and Its Role in Worm-Microbiome Interactions
title_full Bacterial Community Structure Dynamics in <italic toggle="yes">Meloidogyne incognita</italic>-Infected Roots and Its Role in Worm-Microbiome Interactions
title_fullStr Bacterial Community Structure Dynamics in <italic toggle="yes">Meloidogyne incognita</italic>-Infected Roots and Its Role in Worm-Microbiome Interactions
title_full_unstemmed Bacterial Community Structure Dynamics in <italic toggle="yes">Meloidogyne incognita</italic>-Infected Roots and Its Role in Worm-Microbiome Interactions
title_sort bacterial community structure dynamics in <italic toggle="yes">meloidogyne incognita</italic>-infected roots and its role in worm-microbiome interactions
publisher American Society for Microbiology
publishDate 2020
url https://doaj.org/article/93e911e166964ec5b26428c493c61c61
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