Repressed <i>Beauveria bassiana</i> infections in <scp><i>Delia antiqua</i></scp> due to associated microbiota

Zhou, Fangyuan; Wu, Xiaoqing; Xu, Letian; Guo, Shuhai; Chen, Guanhong; Zhang, Xinjian

doi:10.1002/ps.5084

Cited by 39 publications

(30 citation statements)

References 66 publications

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“…S2a) and mycelial growth ( Fig. S2b) of B. bassiana, which is consistent with previous reports (15). Comparison of metabolomic data from the six bacterial strains and K. oxytoca B313 (Fig.…”

Section: Discussionsupporting

confidence: 91%

“…Ketoisocaproic acid is an intermediate in the metabolism of leucine (29). Taking phylogenetic relationships of the six bacterial species into consideration (15), it seems that these bacteria produce those organic acids mainly through primary metabolization. Those metabolites may be essential in colonization resistance.…”

Section: Discussionmentioning

confidence: 99%

“…Delia antiqua (Meigen) (Diptera: Anthomyiidae) is a devastating pest that feeds on liliaceous crops (12) and can cause a reduction of crop yields by more than half of the total yield (13,14). Previously, we found that six most frequently isolated bacterial symbionts including Citrobacter freundii, Enterobacter ludwigii, Pseudomonas protegens, Serratia plymuthica, Sphingobacterium faecium, and Stenotrophomonas maltophilia protected D. antiqua larvae from Beauveria bassiana infection by inhibiting conidial germination and mycelial growth (15), while the bacterium Klebsiella oxytoca showed no antifungal activity against B. bassiana. Collectively, the D. antiqua-associated bacteriumentomopathogen tripartite interaction system provides an ideal model to investigate whether and which metabolites produced by the bacterial associates prevent fungal infection of D. antiqua larvae.…”

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confidence: 94%

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Symbiotic Bacterium-Derived Organic Acids Protect Delia antiqua Larvae from Entomopathogenic Fungal Infection

Zhou

et al. 2020

mSystems

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Colonization resistance, i.e., the protective effects of associated microbiota for the animal host against pathogen infection, has been studied widely over the last 100 years. However, few molecules mediating colonization resistance have been identified. In the symbiosis formed by Delia antiqua and its associated microbes, six bacteria protect larvae from infection with the entomopathogen Beauveria bassiana, providing an ideal model to investigate the chemical mechanism for colonization resistance. Subsequently using this symbiotic system, we first compared effects of the six bacterial species, and one control bacterium (Klebsiella oxytoca) that showed no antifungal effects, on B. bassiana and its infection of D. antiqua. Second, metabolomic profiles of the six bacteria and K. oxytoca were compared to identify candidate metabolites that may prevent infection. Third, the concentrations of candidate metabolites in situ from axenic and nonaxenic larvae were determined. Finally, effects of artificial metabolite cocktails on B. bassiana and its infection of D. antiqua larvae were determined. Results showed that compared to K. oxytoca, the six bacteria produced a metabolite cocktail showing inhibitory effects on conidial germination, mycelial growth of B. bassiana, and fungal infection. Our work revealed novel molecules that mediate colonization resistance, which could help in developing chemical mechanisms of colonization resistance. Moreover, this work may aid in discovery and expansion of new bioactive antibiotics, promoting development of prophylactic and therapeutic approaches for treating infectious diseases. IMPORTANCE The protection of associated microbiota for their animal hosts against pathogen infection has been studied widely over the last 100 years. However, how those microbes protect the animal host remains unclear. In former studies, body surface microbes of one insect, Delia antiqua, protected the insect larvae from infection with the entomopathogen Beauveria bassiana. By comparing the metabolites produced by microbes that protect the insect and microbes that cannot protect the insect, the question of how the microbes protect the insect is answered. It turns out that body surface bacteria produce a metabolite cocktail that inhibits colonization of B. bassiana and consequently protects the insect. This work reveals novel molecules with antifungal activity, which may aid in discovery and expansion of new prophylactic and therapeutic natural chemicals for treating infectious diseases.

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Section: Discussionsupporting

confidence: 91%

Section: Discussionmentioning

confidence: 99%

mentioning

confidence: 94%

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Symbiotic Bacterium-Derived Organic Acids Protect Delia antiqua Larvae from Entomopathogenic Fungal Infection

Zhou

et al. 2020

mSystems

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“…For example, several bacterial species living inside the gut of Delia antiqua confer its larva stronger resistance to Beauveria bassiana infection. 22 Similar results were reported in Leptinotarsa decemlineata 23 and Blattella germanica. 24 Alternatively, gut bacteria synergistically interact with Beauveria bassiana to accelerate the mortality of Anopheles stephensi and Dendroctonus valens.…”

Section: Introductionsupporting

confidence: 77%

Temporospatial modulation of Lymantria dispar immune system against an entomopathogenic fungal infection

Bai

et al. 2020

Pest Management Science

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BACKGROUND: Lymantria dispar is an economically impactful forest pest worldwide. The entomopathogenic fungi Beauveria bassiana shows great promise in pest management due to its high lethality in Lymantria dispar. A complete understanding of the immune interactions between the pest and the pathogenic fungus is essential to actualizing biological pest management. RESULTS: Following the infection of Lymantria dispar by Beauveria bassiana spores, we performed a time-course analysis of transcriptome in Lymantria dispar fat bodies and hemocytes to explore host immune response. A total of 244 immunity-related genes including pattern recognition receptors, extracellular signal modulators, immune pathways (Toll, IMD, JNK and JAK/ STAT), and response effectors were identified. We observed contrasting tissue and time-specific differences in the expression of immune genes. At the early stage of infection, several recognition receptors and effector genes were activated, while the signal modulation and effector genes were suppressed at later stages. Further enzyme activity-based assays coupled with gene expression analysis of prophenoloxidase revealed a significant upregulation of phenoloxidase activity at 48-and 72-h postinfection. Moreover, fungal infection led to dysbiosis in gut microbiota that seems to be partially attributed to reduced gut hydrogen peroxide (H 2 O 2) amount, which indicates a significant impact of fungal infection on host gut microbes. CONCLUSION: Our study provides a comprehensive sequence resource and crucial new insights about an economically important forest pest. Specifically, we elucidate the complicated multipartite interaction between host and fungal pathogen and contribute to a better understanding of Lymantria dispar anti-fungal immunity, resulting in better tools for biological pest control.

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“…This occurs due to tissue damage [ 1 ] and deregulation of host immune reactions in response to the pathogenic fungi [ 2 , 3 ]. Direct and indirect interactions between fungi and bacteria may lead to both antagonistic and synergistic effects on survival [ 2 , 4 , 5 , 6 ]. In addition, interrelations between fungi and bacteria in insect hosts may be mediated by complex environmental factors, such as temperature, chemicals, or parasitoids, that have an influence on the outcome of the disease [ 7 , 8 ].…”

Section: Introductionmentioning

confidence: 99%

Interplay between Fungal Infection and Bacterial Associates in the Wax Moth Galleria mellonella under Different Temperature Conditions

Kryukov

Kosman

Tomilova

et al. 2020

JoF

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Various insect bacterial associates are involved in pathogeneses caused by entomopathogenic fungi. The outcome of infection (fungal growth or decomposition) may depend on environmental factors such as temperature. The aim of this study was to analyze the bacterial communities and immune response of Galleria mellonella larvae injected with Cordyceps militaris and incubated at 15 °C and 25 °C. We examined changes in the bacterial CFUs, bacterial communities (Illumina MiSeq 16S rRNA gene sequencing) and expression of immune, apoptosis, ROS and stress-related genes (qPCR) in larval tissues in response to fungal infection at the mentioned temperatures. Increased survival of larvae after C. militaris injection was observed at 25 °C, although more frequent episodes of spontaneous bacteriosis were observed at this temperature compared to 15 °C. We revealed an increase in the abundance of enterococci and enterobacteria in the midgut and hemolymph in response to infection at 25 °C, which was not observed at 15 °C. Antifungal peptide genes showed the highest expression at 25 °C, while antibacterial peptides and inhibitor of apoptosis genes were strongly expressed at 15 °C. Cultivable bacteria significantly suppressed the growth of C. militaris. We suggest that fungi such as C. militaris may need low temperatures to avoid competition with host bacterial associates.

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Repressed Beauveria bassiana infections in Delia antiqua due to associated microbiota

Abstract: Bacteria associated with larvae, including C. freundii, E. ludwigii, P. protegens, S. plymuthica, S. faecium and S. maltophilia, can inhibit B. bassiana infection. Removing the microbiota can suppress larval resistance to fungal infection. © 2018 Society of Chemical Industry.

Cited by 39 publications

References 66 publications

Symbiotic Bacterium-Derived Organic Acids Protect Delia antiqua Larvae from Entomopathogenic Fungal Infection

Symbiotic Bacterium-Derived Organic Acids Protect Delia antiqua Larvae from Entomopathogenic Fungal Infection

Temporospatial modulation of Lymantria dispar immune system against an entomopathogenic fungal infection

Interplay between Fungal Infection and Bacterial Associates in the Wax Moth Galleria mellonella under Different Temperature Conditions

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