Apex Predator Nematodes and Meso-Predator Bacteria Consume Their Basal Insect Prey through Discrete Stages of Chemical Transformations

Mucci, Nicholas C.; Jones, Katarina A.; Cao, Mengyi; Wyatt, Michael R.; Foye, Shane; Kauffman, Sarah; Richards, Gregory R.; Taufer, Michela; Chikaraishi, Yoshito; Steffan, Shawn A.; Campagna, Shawn R.; Goodrich-Blair, Heidi

doi:10.1128/msystems.00312-22

Cited by 5 publications

(7 citation statements)

References 89 publications

(133 reference statements)

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Section: Discussionmentioning

confidence: 89%

“…Trp metabolism is crucial for pathogen and host microbiota interactions. Although there has been relatively little research in the field of insects, it has recently been found that in tripartite Xenorhabdus bacterium- Steinernema nematode- Galleria insect symbiosis, the Trp metabolism pathway, especially the Kyn pathway, plays important functions at different stages ( Mucci et al, 2022 ). We discovered that after S. feltiae - X. bovienii were injected into the hemocoel of G. mellonella , the Trp metabolic pathway of the insects was significantly upregulated, especially the 3-HAA content of the Kyn pathway, which was significantly increased in the treated group.…”

Section: Discussionmentioning

confidence: 99%

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Metabonomics reveals that entomopathogenic nematodes mediate tryptophan metabolites that kill host insects

Zhang

Wang²,

Zhao³

2022

Front. Microbiol.

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The entomopathogenic nematode (EPN) Steinernema feltiae, which carries the symbiotic bacterium Xenorhabdus bovienii in its gut, is an important biocontrol agent. This EPN could produce a suite of complex metabolites and toxin proteins and lead to the death of host insects within 24–48 h. However, few studies have been performed on the key biomarkers released by EPNs to kill host insects. The objective of this study was to examine what substances produced by EPNs cause the death of host insects. We found that all densities of nematode suspensions exhibited insecticidal activities after hemocoelic injection into Galleria mellonella larvae. EPN infection 9 h later led to immunosuppression by activating insect esterase activity, but eventually, the host insect darkened and died. Before insect immunity was activated, we applied a high-resolution mass spectrometry-based metabolomics approach to determine the hemolymph of the wax moth G. mellonella infected by EPNs. The results indicated that the tryptophan (Trp) pathway of G. mellonella was significantly activated, and the contents of kynurenine (Kyn) and 3-hydroxyanthranilic acid (3-HAA) were markedly increased. Additionally, 3-HAA was highly toxic to G. mellonella and resulted in corrected mortalities of 62.50%. Tryptophan metabolites produced by EPNs are a potential marker to kill insects, opening up a novel line of inquiry into exploring the infestation mechanism of EPNs.

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Section: Discussionmentioning

confidence: 89%

Section: Discussionmentioning

confidence: 99%

Metabonomics reveals that entomopathogenic nematodes mediate tryptophan metabolites that kill host insects

Zhang

Wang²,

Zhao³

2022

Front. Microbiol.

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“…As part of their symbiotic and entomopathogenic lifecycle, all Xenorhabdus must colonize and be transported by a nematode host, suppress insect immunity, establish a community within and consume the cadaver, and support reproduction of the nematode to ensure future transport [10]. Many will also compete or cooperate with other resident or transient hermaphroditum, currently the most genetically tractable steinernematid [24,120,25].…”

Section: Discussionmentioning

confidence: 99%

“…The resultant insect cadaver is an enclosed nutrient-rich niche that both nematode and bacterium leverage to reproduce proliferatively. Nematode fecundity is enhanced by the consumption of Xenorhabdus [10], and Xenorhabdus defends the niche by secreting bacteriocins, antimicrobials and scavenger deterrents, which antagonize both microbial and invertebrate competitors [11][12][13]. Before their exit from the insect cadaver and entry into the surrounding soil, nascent IJ nematodes are specifically colonized by Xenorhabdus in the anterior intestine and ultimately, the receptacle [14].…”

Section: Introductionmentioning

confidence: 99%

Analyses ofXenorhabdus griffiniaegenomes reveal two distinct sub-species that display intra-species variation due to prophages

Heppert,

Awori,

Cao

et al. 2024

Preprint

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Nematodes of the genus Steinernema and their Xenorhabdus bacterial symbionts are lethal entomopathogens that are useful in the biocontrol of insect pests, as sources of diverse natural products, and as research models for mutualism and parasitism. Xenorhabdus play a central role in all aspects of the Steinernema lifecycle, and a deeper understanding of their genomes therefore has the potential to spur advances in each of these applications. Results: Here, we report a comparative genomics analysis of Xenorhabdus griffiniae, including the symbiont of Steinernema hermaphroditum nematodes, for which genetic and genomic tools are being developed. We sequenced and assembled circularized genomes for three Xenorhabdus strains: HGB2511, ID10 and TH1. We then determined their relationships to other Xenorhabdus and delineated their species via phylogenomic analyses, concluding that HGB2511 and ID10 are Xenorhabdus griffiniae while TH1 is a novel species. These additions to the existing X. griffiniae landscape further allowed for the identification of two subspecies within the clade. Consistent with other Xenorhabdus, the analysed X. griffiniae genomes each encode a wide array of antimicrobials and virulence-related proteins. Comparative genomic analyses, including the creation of a pangenome, revealed that a large amount of the intraspecies variation in X. griffiniae is contained within the mobilome and attributable to prophage loci. In addition, CRISPR arrays, secondary metabolite potential and toxin genes all varied among strains within the X. griffiniae species. Conclusions: Our findings suggest that phage-related genes drive the genomic diversity in closely related Xenorhabdus symbionts, and that these may underlie some of the traits most associated with the lifestyle and survival of entomopathogenic nematodes and their bacteria: virulence and competition. This study establishes a broad knowledge base for further exploration of not only the relationships between X. griffiniae species and their nematode hosts but also the molecular mechanisms that underlie their entomopathogenic lifestyle.

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“…Once invading an insect, IJ releases its symbiotic bacteria, and both partners kill the insect. Xenorhabdus bacteria replicate using the nutrient from the insect cadaver and the bacteria serve as food for the nematodes (Mucci et al, 2022), supporting their reproductive development (juveniles J1-J4 and adults). The depletion of nutrients and nematode overcrowding within the dead insect, causing accumulation of pheromone, could induce IJ development, and promote IJs disperse from the insect cadaver into the soil to seek for a new insect prey (Kaplan et al, 2012; Popiel et al, 1989) (Fig.…”

Section: Introductionmentioning

confidence: 99%

CRISPR-Cas9 genome editing inSteinernemaentomopathogenic nematodes

Cao

2023

Preprint

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Molecular tool development in traditionally non-tractable animals opens new avenues to study gene functions in the relevant ecological context. Entomopathogenic nematodes (EPN)Steinernemaand their symbiotic bacteria ofXenorhabdusspp are a valuable experimental system in the laboratory and are applicable in the field to promote agricultural productivity. The infective juvenile (IJ) stage of the nematode packages mutualistic symbiotic bacteria in the intestinal pocket and invades insects that are agricultural pests. The lack of consistent and heritable genetics tools in EPN targeted mutagenesis severely restricted the study of molecular mechanisms underlying both parasitic and mutualistic interactions. Here, I report a protocol for CRISPR-Cas9 based genome-editing that is successful in two EPN species,S. carpocapsaeandS. hermaphroditum. I adapted a gonadal microinjection technique inS. carpocapsae, which created on-target modifications of a homologueSc-dpy-10(cuticular collagen) by homology-directed repair. A similar delivery approach was used to introduce various alleles inS. hermaphroditumincludingSh-dpy-10andSh-unc-22(a muscle gene), resulting in visible and heritable phenotypes of dumpy and twitching, respectively. Using conditionally dominant alleles ofSh-unc-22as a co-CRISPR marker, I successfully modified a second locus encoding Sh-Daf-22 (a homologue of human sterol carrier protein SCPx), predicted to function as a core enzyme in the biosynthesis of nematode pheromone that is required for IJ development. As a proof of concept,Sh-daf-22null mutant showed IJ developmental defectsin vivo(in insecta). This research demonstrates thatSteinernemaspp are highly tractable for targeted mutagenesis and has great potential in the study of gene functions under controlled laboratory conditions within the relevant context of its ecological niche.

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Apex Predator Nematodes and Meso-Predator Bacteria Consume Their Basal Insect Prey through Discrete Stages of Chemical Transformations

Cited by 5 publications

References 89 publications

Metabonomics reveals that entomopathogenic nematodes mediate tryptophan metabolites that kill host insects

Metabonomics reveals that entomopathogenic nematodes mediate tryptophan metabolites that kill host insects

Analyses ofXenorhabdus griffiniaegenomes reveal two distinct sub-species that display intra-species variation due to prophages

CRISPR-Cas9 genome editing inSteinernemaentomopathogenic nematodes

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