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Transcriptional response of Musca domestica larvae to bacterial infection.

ABSTRACT: The house fly Musca domestica, a cosmopolitan dipteran insect, is a significant vector for human and animal bacterial pathogens, but little is known about its immune response to these pathogens. To address this issue, we inoculated the larvae with a mixture of Escherichia coli and Staphylococcus aureus and profiled the transcriptome 6, 24, and 48 h thereafter. Many genes known to controlling innate immunity in insects were induced following infection, including genes encoding pattern recognition proteins (PGRPs), various components of the Toll and IMD signaling pathways and of the proPO-activating and redox systems, and multiple antimicrobial peptides. Interestingly, we also uncovered a large set of novel immune response genes including two broad-spectrum antimicrobial peptides (muscin and domesticin), which might have evolved to adapt to house-fly's unique ecological environments. Finally, genes mediating oxidative phosphorylation were repressed at 48 h post-infection, suggesting disruption of energy homeostasis and mitochondrial function at the late stages of infection. Collectively, our data reveal dynamic changes in gene expression following bacterial infection in the house fly, paving the way for future in-depth analysis of M. domestica's immune system.

SUBMITTER: Tang T

PROVIDER: S-EPMC4138075 | biostudies-literature | 2014

REPOSITORIES: biostudies-literature

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Transcriptional response of Musca domestica larvae to bacterial infection.

Tang Ting T Li Xiang X Yang Xue X Yu Xue X Wang Jianhui J Liu Fengsong F Huang Dawei D

PloS one 20140819 8

The house fly Musca domestica, a cosmopolitan dipteran insect, is a significant vector for human and animal bacterial pathogens, but little is known about its immune response to these pathogens. To address this issue, we inoculated the larvae with a mixture of Escherichia coli and Staphylococcus aureus and profiled the transcriptome 6, 24, and 48 h thereafter. Many genes known to controlling innate immunity in insects were induced following infection, including genes encoding pattern recognition ...[more]

PMID: 25137050

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Project description:Beneficial symbiotic bacteria have positive effects on some insects' (such as mosquitoes, cockroaches, and flies) biological activities. However, the effects of a lack of one specific symbiotic bacterium on the life activities of some insects and their natural gut microbiota composition remain unclear. Bacteriophages are viruses that specifically target and kill bacteria and have the potential to shape gut bacterial communities. In previous work, Pseudomonas aeruginosa that naturally colonized the intestines of housefly larvae was shown to be essential to protect housefly larvae from entomopathogenic fungal infections, leading us to test whether a deficiency in Pseudomonas aeruginosa strains in housefly larvae that was specifically caused using bacteriophages could remold the composition of the intestinal bacteria and affect the development of housefly larvae. Our research revealed that the phage, with a titer of 108 PFU/ml, can remove 90% of Pseudomonas aeruginosa in the gut. A single feeding of low-dose phage had no effect on the health of housefly larvae. However, the health of housefly larvae was affected by treatment with phage every 24 h. Additionally, treating housefly larvae with bacteriophages every 24 h led to bacterial composition changes in the gut. Collectively, the results revealed that deficiency in one symbiotic gut bacteria mediated by precise targeting using bacteriophages indirectly influences the intestinal microbial composition of housefly larvae and has negative effects on the development of the host insect. Our results indicated the important role of symbiotic gut bacteria in shaping the normal gut microbiota composition in insects. IMPORTANCE The well-balanced gut microbiota ensures appropriate development of the host insect, such as mosquitoes, cockroaches, and flies. Various intestinal symbiotic bacteria have different influences on the host gut community structure and thus exert different effects on host health. Therefore, it is of great importance to understand the contributions of one specific bacterial symbiont to the gut microbiota community structure and insect health. Bacteriophages that target certain bacteria are effective tools that can be used to analyze gut bacterial symbionts. However, experimental evidence for phage efficacy in regulating insect intestinal bacteria has been little reported. In this study, we used phages as precision tools to regulate a bacterial community and analyzed the influence on host health after certain bacteria were inhibited by bacteriophage. The ability of phages to target intestinal-specific bacteria in housefly larvae and reduce the levels of target bacteria makes them an effective tool for studying the function of gut bacteria.

Project description:American foulbrood disease of honey bees is caused by the bacterium Paenibacillus larvae. Infection occurs per os in larvae and systemic infection requires a breaching of the host peritrophic matrix and midgut epithelium. Genetic variation exists for both bacterial virulence and host resistance, and a general immunity is achieved by larvae as they age, the basis of which has not been identified. To quickly identify a pool of candidate genes responsive to P. larvae infection, we sequenced transcripts from larvae inoculated with P. larvae at 12 hours post-emergence and incubated for 72 hours, and compared expression levels to a control cohort. We identified 75 genes with significantly higher expression and six genes with significantly lower expression. In addition to several antimicrobial peptides, two genes encoding peritrophic-matrix domains were also up-regulated. Extracellular matrix proteins, proteases/protease inhibitors, and members of the Osiris gene family were prevalent among differentially regulated genes. However, analysis of Drosophila homologs of differentially expressed genes revealed spatial and temporal patterns consistent with developmental asynchrony as a likely confounder of our results. We therefore used qPCR to measure the consistency of gene expression changes for a subset of differentially expressed genes. A replicate experiment sampled at both 48 and 72 hours post infection allowed further discrimination of genes likely to be involved in host response. The consistently responsive genes in our test set included a hymenopteran-specific protein tyrosine kinase, a hymenopteran specific serine endopeptidase, a cytochrome P450 (CYP9Q1), and a homolog of trynity, a zona pellucida domain protein. Of the known honey bee antimicrobial peptides, apidaecin was responsive at both time-points studied whereas hymenoptaecin was more consistent in its level of change between biological replicates and had the greatest increase in expression by RNA-seq analysis.

Dataset Information

Transcriptional response of Musca domestica larvae to bacterial infection.

Publications

Transcriptional response of Musca domestica larvae to bacterial infection.

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