Discovery of a new highly pathogenic toxin involved in insect sepsis
ABSTRACT Insect sepsis is a severe consequence that arises from the invasion of the hemocoel by symbionts of entomopathogenic nematodes and bacteria. In the present study, we unveiled the heightened virulence of the entomopathogenic nematode Steinernema feltiae and the entomopathogenic bacteria Xeno...
| Main Authors: | , , , , , , , , |
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| Format: | Article |
| Language: | English |
| Published: |
American Society for Microbiology
2023-12-01
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| Series: | Microbiology Spectrum |
| Subjects: | |
| Online Access: | https://journals.asm.org/doi/10.1128/spectrum.01422-23 |
| _version_ | 1797393597114351616 |
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| author | Yuan Zhang Hao Li Fang Wang Chang Liu Gadi V. P. Reddy Hu Li Zhihong Li Yucheng Sun Zihua Zhao |
| author_facet | Yuan Zhang Hao Li Fang Wang Chang Liu Gadi V. P. Reddy Hu Li Zhihong Li Yucheng Sun Zihua Zhao |
| author_sort | Yuan Zhang |
| collection | DOAJ |
| description | ABSTRACT Insect sepsis is a severe consequence that arises from the invasion of the hemocoel by symbionts of entomopathogenic nematodes and bacteria. In the present study, we unveiled the heightened virulence of the entomopathogenic nematode Steinernema feltiae and the entomopathogenic bacteria Xenorhabdus bovienii, which operate symbiotically, against the wax moth Galleria mellonella. Maximum mortality was observed at 25°C while the optimal infestation efficiency was 20 nematodes per host. After infestation, G. mellonella displayed rapid darkening and softening, accompanied by an escalated esterase activity at 9 h. The X. bovienii, released by S. feltiae, underwent substantial proliferation and discharged toxins that attacked hemocytes, thus triggering extensive hemolysis and sepsis. The host G. mellonella was usually killed within 24 h due to disseminated septicemia. Additionally, X. bovienii infestation led to the upregulation of metabolites like 3-hydroxyanthranilic acid. Strikingly, we identified the perilous actinomycin D, generated through kynurenine metabolites, representing a novel biomarker of insect sepsis. Furthermore, a comprehensive transcriptomic analysis unveiled a noteworthy upregulation of gene expression associated with actinomycin D. Overall, X. bovienii induced apoptosis and sepsis through actinomycin D production, indicating its pivotal role in infestation activity. These findings open up new avenues for studying the mechanism of sepsis and developing innovative biotic pesticides. IMPORTANCE As a current biocontrol resource, entomopathogenic nematodes and their symbiotic bacterium can produce many toxin factors to trigger insect sepsis, having the potential to promote sustainable pest management. In this study, we found Steinernema feltiae and Xenorhabdus bovienii were highly virulent against the insects. After infective juvenile injection, Galleria mellonella quickly turned black and softened with increasing esterase activity. Simultaneously, X. bovienii attacked hemocytes and released toxic components, resulting in extensive hemolysis and sepsis. Then, we applied high-resolution mass spectrometry-based metabolomics and found multiple substances were upregulated in the host hemolymph. We found extremely hazardous actinomycin D produced via 3-hydroxyanthranilic acid metabolites. Moreover, a combined transcriptomic analysis revealed that gene expression of proteins associated with actinomycin D was upregulated. Our research revealed actinomycin D might be responsible for the infestation activity of X. bovienii, indicating a new direction for exploring the sepsis mechanism and developing novel biotic pesticides. |
| first_indexed | 2024-03-09T00:06:07Z |
| format | Article |
| id | doaj.art-50bc84b35c5145158e43408699e129fc |
| institution | Directory Open Access Journal |
| issn | 2165-0497 |
| language | English |
| last_indexed | 2024-03-09T00:06:07Z |
| publishDate | 2023-12-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | Microbiology Spectrum |
| spelling | doaj.art-50bc84b35c5145158e43408699e129fc2023-12-12T13:17:19ZengAmerican Society for MicrobiologyMicrobiology Spectrum2165-04972023-12-0111610.1128/spectrum.01422-23Discovery of a new highly pathogenic toxin involved in insect sepsisYuan Zhang0Hao Li1Fang Wang2Chang Liu3Gadi V. P. Reddy4Hu Li5Zhihong Li6Yucheng Sun7Zihua Zhao8MARA Key Laboratory of Surveillance and Management for Plant Quarantine Pests, College of Plant Protection, China Agricultural University , Beijing, ChinaMARA Key Laboratory of Surveillance and Management for Plant Quarantine Pests, College of Plant Protection, China Agricultural University , Beijing, ChinaInstitute of Plant Protection, Ningxia Academy of Agricultural and Forestry Sciences , Yinchuan, ChinaInstitute of Plant Protection, Ningxia Academy of Agricultural and Forestry Sciences , Yinchuan, ChinaDepartment of Entomology, Lousiana State University , Baton Rouge, Los Angeles, USAMARA Key Laboratory of Surveillance and Management for Plant Quarantine Pests, College of Plant Protection, China Agricultural University , Beijing, ChinaMARA Key Laboratory of Surveillance and Management for Plant Quarantine Pests, College of Plant Protection, China Agricultural University , Beijing, ChinaInstitute of Zoology, Chinese Academy of Sciences , Beijing, ChinaMARA Key Laboratory of Surveillance and Management for Plant Quarantine Pests, College of Plant Protection, China Agricultural University , Beijing, ChinaABSTRACT Insect sepsis is a severe consequence that arises from the invasion of the hemocoel by symbionts of entomopathogenic nematodes and bacteria. In the present study, we unveiled the heightened virulence of the entomopathogenic nematode Steinernema feltiae and the entomopathogenic bacteria Xenorhabdus bovienii, which operate symbiotically, against the wax moth Galleria mellonella. Maximum mortality was observed at 25°C while the optimal infestation efficiency was 20 nematodes per host. After infestation, G. mellonella displayed rapid darkening and softening, accompanied by an escalated esterase activity at 9 h. The X. bovienii, released by S. feltiae, underwent substantial proliferation and discharged toxins that attacked hemocytes, thus triggering extensive hemolysis and sepsis. The host G. mellonella was usually killed within 24 h due to disseminated septicemia. Additionally, X. bovienii infestation led to the upregulation of metabolites like 3-hydroxyanthranilic acid. Strikingly, we identified the perilous actinomycin D, generated through kynurenine metabolites, representing a novel biomarker of insect sepsis. Furthermore, a comprehensive transcriptomic analysis unveiled a noteworthy upregulation of gene expression associated with actinomycin D. Overall, X. bovienii induced apoptosis and sepsis through actinomycin D production, indicating its pivotal role in infestation activity. These findings open up new avenues for studying the mechanism of sepsis and developing innovative biotic pesticides. IMPORTANCE As a current biocontrol resource, entomopathogenic nematodes and their symbiotic bacterium can produce many toxin factors to trigger insect sepsis, having the potential to promote sustainable pest management. In this study, we found Steinernema feltiae and Xenorhabdus bovienii were highly virulent against the insects. After infective juvenile injection, Galleria mellonella quickly turned black and softened with increasing esterase activity. Simultaneously, X. bovienii attacked hemocytes and released toxic components, resulting in extensive hemolysis and sepsis. Then, we applied high-resolution mass spectrometry-based metabolomics and found multiple substances were upregulated in the host hemolymph. We found extremely hazardous actinomycin D produced via 3-hydroxyanthranilic acid metabolites. Moreover, a combined transcriptomic analysis revealed that gene expression of proteins associated with actinomycin D was upregulated. Our research revealed actinomycin D might be responsible for the infestation activity of X. bovienii, indicating a new direction for exploring the sepsis mechanism and developing novel biotic pesticides.https://journals.asm.org/doi/10.1128/spectrum.01422-23SteinernemaXenorhabdusphenotypic variationapoptosisKyn pathwayactinomycin D |
| spellingShingle | Yuan Zhang Hao Li Fang Wang Chang Liu Gadi V. P. Reddy Hu Li Zhihong Li Yucheng Sun Zihua Zhao Discovery of a new highly pathogenic toxin involved in insect sepsis Microbiology Spectrum Steinernema Xenorhabdus phenotypic variation apoptosis Kyn pathway actinomycin D |
| title | Discovery of a new highly pathogenic toxin involved in insect sepsis |
| title_full | Discovery of a new highly pathogenic toxin involved in insect sepsis |
| title_fullStr | Discovery of a new highly pathogenic toxin involved in insect sepsis |
| title_full_unstemmed | Discovery of a new highly pathogenic toxin involved in insect sepsis |
| title_short | Discovery of a new highly pathogenic toxin involved in insect sepsis |
| title_sort | discovery of a new highly pathogenic toxin involved in insect sepsis |
| topic | Steinernema Xenorhabdus phenotypic variation apoptosis Kyn pathway actinomycin D |
| url | https://journals.asm.org/doi/10.1128/spectrum.01422-23 |
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