Abstract

As a worldwide sanitary insect pest, the housefly Musca domestica can carry and transmit more than 100 human pathogens without suffering any illness itself, indicative of the high efficiency of its innate immune system. Antimicrobial peptides (AMPs) are the effectors of the innate immune system of multicellular organisms and establish the first line of defense to protect hosts from microbial infection. To explore the molecular diversity of the M. domestica AMPs and related evolutionary basis, we conducted a systematic survey of its full AMP components based on a combination of computational approaches. These components include the cysteine-containing peptides (MdDefensins, MdEppins, MdMuslins, MdSVWCs and MdCrustins), the linear α-helical peptides (MdCecropins) and the specific amino acid-rich peptides (MdDomesticins, MdDiptericins, MdEdins and MdAttacins). On this basis, we identified multiple genetic mechanisms that could have shaped the molecular and structural diversity of the M. domestica AMPs, including: (1) Gene duplication; (2) Exon duplication via shuffling; (3) Protein terminal variations; (4) Evolution of disulfide bridges via compensation. Our results not only enlarge the insect AMP family members, but also offer a basic platform for further studying the roles of such molecular diversity in contributing to the high efficiency of the housefly antimicrobial immune system.

Highlights

  • Insects account for 90% of all extant animal organisms in the world [1,2] and coexist with a variety of microorganisms in different environments [3]

  • We report the molecular diversity of the M. dometica Antimicrobial peptides (AMPs) based on a systematic database search, which could provide us with a special perspective to understand how the evolution of the antimicrobial immune system occurs in a species with the tenacious vitality

  • We found that different from Drosophila that has a limited number of AMPs [6], M. domestica has largely expanded its AMP number via multiple genetic mechanisms to create structural diversity of their AMPs, which would have commonly shaped its high-efficient antimicrobial immune system

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Summary

Introduction

Insects account for 90% of all extant animal organisms in the world [1,2] and coexist with a variety of microorganisms in different environments [3]. Many AMPs are induced from the insect immune organs (e.g., fat body) in response to microbial infections They secret into hemolymph to reach a concentration between 0.1 and 100 μM to inhibit the growth of exotic microorganisms [6]. Like the counterparts in non-insect organisms, insect AMPs are classified into three distinct structural classes They are the cysteine-rich peptides (e.g., drosomycins and insect defensins, two subfamilies of defensins in Drosophila) [7,8,9]; the peptides adopting an α-helical conformation (e.g., cecropins and moricins) [10]; and the peptides with an unusual bias in certain amino acids, such as proline-rich peptides (e.g., metchnikowins, apidaecins, drosocins, and lebocins) [11,12,13] and glycine-rich peptides/proteins (e.g., diptericins, attacins and gloverins) [6]. In Drosophila, their AMPs are initially divided into three functional classes based on their target specificity, which comprises antifungal

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