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Antimicrobial Peptides Expressed in Medicinal Maggots of the Blow Fly Lucilia Sericata Show Combinatorial Activity Against Bacteria

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Antimicrobial Peptides Expressed in Medicinal Maggots of the Blow Fly Lucilia Sericata Show Combinatorial Activity Against Bacteria Antimicrobial Peptides Expressed in Medicinal Maggots of the Blow Fly Lucilia sericata Show Combinatorial Activity against Bacteria Anne-Kathrin Pöppel,a Heiko Vogel,b Jochen Wiesner,a Andreas Vilcinskasa,c Fraunhofer Institute for Molecular Biology and Applied Ecology, Department of Bioresources, Giessen, Germanya; Max Planck Institute for Chemical Ecology, Department of Entomology, Jena, Germanyb; Institute of Phytopathology and Applied Zoology, Justus-Liebig-University of Giessen, Giessen, Germanyc The larvae of the common green bottle fly (Lucilia sericata) produce antibacterial secretions that have a therapeutic effect on chronic and nonhealing wounds. Recent developments in insect biotechnology have made it possible to use these larvae as a source of novel anti-infectives. Here, we report the application of next-generation RNA sequencing (RNA-Seq) to characterize the transcriptomes of the larval glands, crop, and gut, which contribute to the synthesis of antimicrobial peptides (AMPs) and proteins secreted into wounds. Our data confirm that L. sericata larvae have adapted in order to colonize microbially contami- nated habitats, such as carrion and necrotic wounds, and are protected against infection by a diverse spectrum of AMPs. L. seri- cata AMPs include not only lucifensin and lucimycin but also novel attacins, cecropins, diptericins, proline-rich peptides, and sarcotoxins. We identified 47 genes encoding putative AMPs and produced 23 as synthetic analogs, among which some displayed activities against a broad spectrum of microbial pathogens, including Pseudomonas aeruginosa, Proteus vulgaris, and Enterococ- cus faecalis. Against Escherichia coli (Gram negative) and Micrococcus luteus (Gram positive), we found mostly additive effects but also synergistic activity when selected AMPs were tested in combination. The AMPs that are easy to synthesize are currently being produced in bulk to allow their evaluation as novel anti-infectives that can be formulated in hydrogels to produce thera- peutic wound dressings and adhesive bandages. he larvae of the common green bottle fly Lucilia sericata,a tion by its AMP repertoire, we injected larvae with bacteria and Tmember of the blow fly family (Calliphoridae), are known as cataloged the transcriptomes by high-throughput RNA sequenc- medical maggots or wound maggots, because they have been used ing (RNA-Seq) to identify the inducible immunity-related genes. to treat wounds as part of traditional medicine (1). This approach, In order to separate AMPs that are secreted into wounds from commonly termed maggot therapy, is an approved and prosper- those with other functions, we compared the transcriptomes of ing alternative for the treatment of chronic and nonhealing whole larvae, dissected salivary glands, crops, and gut samples, wounds, e.g., those associated with diabetic ulcers (2–4). The ther- because antimicrobial activity has been detected in oral secretions apeutic effects include the removal of necrotic tissue (debride- and is also regurgitated from the gut (15, 16). We identified an ment), the acceleration of wound healing, and wound disinfection impressive spectrum of genes encoding 47 putative AMPs, many (5, 6). The wound disinfection property has been attributed to of which were found to be differentially expressed in the relevant antimicrobial components in the larval secretions, including small tissues. We produced 23 of the novel L. sericata AMPs as synthetic molecules with antibacterial activity (7, 8) and antimicrobial pep- peptides to test their activities, alone or in combination, against tides (AMPs), such as the defensin-like lucifensin (9) and a re- bacteria. cently reported AMP with potent antifungal activity, which ac- cordingly was named lucimycin (10). MATERIALS AND METHODS The ability of L. sericata larvae to prosper on carrion and ne- Biological samples. L. sericata maggots were obtained from BioMonde crotic wounds suggests that they are adapted to colonize contam- GmbH (Barsbüttel, Germany) and maintained under sterile conditions inated environments, e.g., by expressing a diverse spectrum of on blood agar plates (Columbia Agar with Sheep Blood Plus; Oxoid, AMPs to protect them against the microbes they encounter (11). This theory is supported by the unique ability of rat-tailed mag- gots (larvae of the drone fly Eristalis tenax) to survive in highly Received 31 December 2014 Returned for modification 25 January 2015 contaminated aquatic habitats, such as liquid manure storage pits Accepted 4 February 2015 and cesspools, which also reflects their production of multiple Accepted manuscript posted online 9 February 2015 diverse AMPs (12). Similarly, we found that the burying beetle Citation Pöppel A-K, Vogel H, Wiesner J, Vilcinskas A. 2015. Antimicrobial peptides Nicrophorus vespilloides, which lives and reproduces on cadavers, expressed in medicinal maggots of the blow fly Lucilia sericata show combinatorial activity against bacteria. Antimicrob Agents Chemother also produces a wide spectrum of AMPs (13). The synthesis of 59:2508–2514. doi:10.1128/AAC.05180-14. diverse AMPs also provides the potential for beneficial combina- Address correspondence to Andreas Vilcinskas, torial interactions, such as additive antimicrobial effects, synergy [email protected]. (greater-than-additive effects), or potentiation (one AMP en- Supplemental material for this article may be found at http://dx.doi.org/10.1128 abling or enhancing the activity of others). The diversification of /AAC.05180-14. genes encoding AMPs by duplication and sequence divergence is Copyright © 2015, American Society for Microbiology. All Rights Reserved. often replicated at the functional level, thus providing protection doi:10.1128/AAC.05180-14 against a broader spectrum of microbes (11, 14). The authors have paid a fee to allow immediate free access to this article. To test the hypothesis that L. sericata is protected from infec- 2508 aac.asm.org Antimicrobial Agents and Chemotherapy May 2015 Volume 59 Number 5 Antimicrobial Peptides Expressed in Medicinal Maggots United Kingdom) at 28°C in the dark. A prescreening experiment was version 6.5. The de novo transcriptome assembly was carried out using the used to identify the optimal bacterial species and the inoculation time for same software by comparing an assembly with standard settings and two maximum immune induction. For each experimental group, 10 larvae additional CLC-based assemblies with different parameters and then se- (ϳ5 mm in length) reared on blood agar plates for 48 h were placed in lecting the presumed optimal consensus transcriptome, as described pre- petri dishes on ice to reduce their mobility and facilitate injection. The viously (20). Any conflicts among the individual bases were resolved by bacteria were introduced ventrolaterally by pricking the abdomen using a voting for the base with highest frequency. Contigs Ͻ200 bp were re- dissecting needle dipped in an aqueous solution of individual or mixed moved from the final analysis. The resulting final de novo reference tran- bacterial cultures (Escherichia coli, Pseudomonas aeruginosa, Staphylococ- scriptome assembly (backbone) contained 67,193 contigs Ͼ200 bp, with cus aureus, Staphylococcus epidermidis, and Micrococcus luteus), or in an N50 contig size of 1,097 bp and a maximum contig length of 27,637 bp. phosphate-buffered saline (PBS). Hemolymph samples were taken from The transcriptome was annotated using BLAST, Gene Ontology, and five larvae in each treatment group 8 and 24 h after injection and tested for InterProScan searches with Blast2GO Pro version 2.6.1 (21). For BLASTx antimicrobial activity in bacterial plate growth inhibition assays. Based on searches against the nonredundant NCBI protein database (NR database), these initial assays, we used a mixture of P. aeruginosa (strain DSM 50071) up to 20 best NR hits per transcript were retained, with an E value cutoff of and S. aureus (strain DSM 20044) for the subsequent immune induction Յ10Ϫ1 and a minimum match length of 15 amino acids to obtain the best experiments. In this new series of experiments, the eight infected larvae homolog for the predicted short polypeptides. Annex (22) was used to and 15 controls were shock frozen in liquid nitrogen 8 h after injection optimize the Gene Ontology (GO) term identification further by crossing and stored at Ϫ80°C. Pools of infected or control larvae (first and third the three GO categories (biological process, molecular function, and cel- instar) were used to prepare RNA samples for the 454-FLX-based se- lular component) to search for name similarities, GO term relationships, quencing of normalized RNA and the Illumina-based sequencing of non- and enzyme relationships within metabolic pathways (Kyoto Encyclope- normalized RNA. The infected and control third instar larvae were also dia of Genes and Genomes) (23). To identify candidate genes in the L. dissected to separate the salivary glands, crops, and guts from the rest of sericata transcriptome assembly, we established a reference set of known the body to prepare the RNA samples for Illumina RNA-Seq analysis. or predicted insect-derived AMPs using published sequences and by RNA isolation. Total RNA was extracted from each of the pooled searching our in-house database and public databases (NCBI). larval samples and tissues described above using the innuPREP RNA mini Digital gene expression analysis. Digital gene expression analysis was isolation kit (Analytik Jena, Jena, Germany), followed by additional RNA carried
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