Bacteria isolated from the cuticle of plant-parasitic nematodes attached to and antagonized the root-knot nematode Meloidogyne hapla

Topalović, Olivera; Elhady, Ahmed; Hallmann, Johannes; Richert-Pöggeler, Katja; Heuer, Holger

doi:10.1038/s41598-019-47942-7

Cited by 52 publications

(33 citation statements)

References 54 publications

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“…The interaction between the virulence of M. incognita and the microbial diversity in the various niches M. incognita occupy has been studied in the context of biological control, revealing complex relationships, which efficacy diminishes with the transfer from lab to field ( 20 ). In this field of research, common themes include the isolation of Meloidogyne pathogens from the cuticles of J2s ( 21 – 23 ) and the identification of soil microbes and bacterial volatile compounds with antagonistic effects ( 24 , 25 ) from key taxa, including Rhizobia ( 26 ), Trichoderma and Pseudomonas ( 27 , 28 ), Pasteuria ( 29 ), Pochonia ( 30 , 31 ), and some mycorrhiza ( 31 – 33 ).…”

Section: Introductionmentioning

confidence: 99%

Bacterial Community Structure Dynamics in Meloidogyne incognita -Infected Roots and Its Role in Worm-Microbiome Interactions

Yergaliyev

Alexander-Shani

Dimerets

et al. 2020

mSphere

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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.

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Section: Introductionmentioning

confidence: 99%

Bacterial Community Structure Dynamics in Meloidogyne incognita -Infected Roots and Its Role in Worm-Microbiome Interactions

Yergaliyev

Alexander-Shani

Dimerets

et al. 2020

mSphere

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“…In a previous study, the rhizosphere microbial communities of maize, but not tomato, protected plants better against nematode attack than the microbial community from bulk soil [11]. As cuticle-attached microbes can affect root invasion of nematodes [16,[29][30][31], we investigated whether shifts in soil microbial communities induced by different plant species led to a different set of microbes that attach to the phytonematode species P. penetrans. DGGE fingerprints of fungal ITS fragments and bacterial 16S rRNA genes showed that the plant species determined, which microbes attached to the cuticle.…”

Section: Discussionmentioning

confidence: 96%

Plants Specifically Modulate the Microbiome of Root-lesion Nematodes in the Rhizosphere, Affecting Their Fitness

Elhady

Topalović

Heuer

2021

Preprint

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Plant-parasitic nematodes are a major constraint for agricultural production. They significantly impede crop yield. To complete their parasitism, they need to locate, disguise, and interact with plant signals exuded in the rhizosphere of the host plant. A specific subset of the soil microbiome can attach to the surface of nematodes in a specific manner. We hypothesized that host plants recruit species of microbes as helpers against attacking nematode species, and that these helpers differ among plant species. We investigated to what extend the attached microbial species are determined by plant species, their root exudates, and how these microbes affect nematodes. We conditioned the soil microbiome in the rhizosphere of different plant species, then employed culture-independent and culture-dependent methods to study the microbial attachment to the cuticle of the phytonematode Pratylenchus penetrans. Community fingerprints of nematode-attached fungi and bacteria showed that the plant species govern the microbiome associated with nematode cuticle. Bacteria isolated from the cuticle belonged to Actinobacteria, Alphaproteobacteria, Betaproteobacteria, Gammaproteobacteria, Sphingobacteria, and Firmicutes. The isolates Microbacterium sp. i.14, Lysobacter capsici i.17, and Alcaligenes sp. i.37 showed the highest attachment rates to the cuticle. The isolates Bacillus cereus i.24 and L. capsici i.17 significantly antagonized P. penetrans after attachment. Significantly more bacteria attached to P. penetrans in microbiome suspensions from bulk soil or oat rhizosphere compared to Ethiopian mustard rhizosphere. However, the latter caused a better suppression of the nematode. Conditioning the cuticle of P. penetrans with root exudates significantly decreased the number of Microbacterium sp. i.14 attaching to the cuticle, suggesting induced changes of the cuticle structure. These findings will lead to a more knowledge-driven exploitation of microbial antagonists of plant-parasitic nematodes for plant protection.

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“…Research has succeeded to isolate, screen, and utilize BCAs against PPNs (e.g., Askary and Martinelli 2015; Abd-Elgawad and Askary 2018), but additional efforts should offer technologies that are truly transformational and result in significant penetration to the bionematicides market. Topalović et al (2019) used molecular tools to reveal the bacteria with the highest affinity to attach to Meloidogyne hapla-J 2 and could elucidate the dynamics and speed of the bacterial adhesion to nematode cuticle during the biocontrol process. They reported that most of the tested bacterial attackers significantly decreased the nematode penetration into the root system, demonstrating their biocontrol role in soil suppressiveness against M. hapla on tomato plants.…”

Section: Genetic Improvement For Better and Broader Ppn Control Molecmentioning

confidence: 99%

Factors affecting success of biological agents used in controlling the plant-parasitic nematodes

Abd-Elgawad

Askary

2020

Egypt J Biol Pest Control

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Biological control agents (BCAs) are increasingly used against various plant-parasitic nematode (PPN) pests and offer a favorable alternative to hazardous chemical nematicides. Yet, their lack of efficacy, inconsistent field performance, and/or unfavorable economic factors have generally relegated them to a relatively small sector of pesticide market. Efficacy and biocontrol success can be boosted via holistic grasping of soil biological and ecological factors. Therefore, such factors were highlighted to give better directions for their use. Main points discussed currently are considered to affect the transmission success of these BCAs so that their use must be a way forward in crop protection/pest management. These included improved sampling, grasping BCAs interactions with soil biota and ecology, cost-effective use of BCAs, genetic manipulation for better PPN control, grower acceptance and awareness-raising of BCA techniques, and commercial application.

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Bacteria isolated from the cuticle of plant-parasitic nematodes attached to and antagonized the root-knot nematode Meloidogyne hapla

Cited by 52 publications

References 54 publications

Bacterial Community Structure Dynamics in Meloidogyne incognita -Infected Roots and Its Role in Worm-Microbiome Interactions

Bacterial Community Structure Dynamics in Meloidogyne incognita -Infected Roots and Its Role in Worm-Microbiome Interactions

Plants Specifically Modulate the Microbiome of Root-lesion Nematodes in the Rhizosphere, Affecting Their Fitness

Factors affecting success of biological agents used in controlling the plant-parasitic nematodes

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