Friend, foe or food? Recognition and the role of antimicrobial peptides in gut immunity and Drosophila –microbe interactions

Abstract

One contribution of 13 to a theme issue 'Evolutionary ecology of arthropod antimicrobial peptides'. Drosophila melanogaster lives, breeds and feeds on fermenting fruit, an environment that supports a high density, and often a diversity, of microorganisms. This association with such dense microbe-rich environments has been proposed as a reason that D. melanogaster evolved a diverse and potent antimicrobial peptide (AMP) response to microorganisms, especially to combat potential pathogens that might occupy this niche. Yet, like most animals, D. melanogaster also lives in close association with the beneficial microbes that comprise its microbiota, or microbiome, and recent studies have shown that antimicrobial peptides (AMPs) of the epithelial immune response play an important role in dictating these interactions and controlling the host response to gut microbiota. Moreover, D. melanogaster also eats microbes for food, consuming fermentative microbes of decaying plant material and their by-products as both larvae and adults. The processes of nutrient acquisition and host defence are remarkably similar and use shared functions for microbe detection and response, an observation that has led to the proposal that the digestive and immune systems have a common evolutionary origin. In this manner, D. melanogaster provides a powerful model to understand how, and whether, hosts differentiate between the microbes they encounter across this spectrum of associations.This article is part of the themed issue 'Evolutionary ecology of arthropod antimicrobial peptides'.

Perspectives on the evolutionary ecology of arthropod antimicrobial peptides

“…The microbiota has emerged as an important third party in host -parasite interactions in almost all organisms studied to date [138,139]. Even small changes in how AMPs are expressed could affect the composition or effectiveness of the microbiota as a defence system against infections as also discussed here [91]. Again, while this scenario is very plausible and accumulating evidence strongly supports the idea that AMPs mediate interactions with the microbiota, we still largely lack an understanding of how this interaction can also keep rapidly co-evolving parasites at bay and keep the AMPs effective as primary tools of the host.…”

“…Gut immunity in insects has been studied in Drosophila [91], an organism that mostly feeds on substrates very rich in microbes, resulting in a close resemblance of the gut microbiota with the microbial food community [93]. At the same time, the gut is constantly changing, both because of the influx of microbes and because of the replacement of host cells by intestinal stem cells.…”

Stable Host Gene Expression in the Gut of Adult Drosophila melanogaster with Different Bacterial Mono-Associations

“…However, immunomodulatory mechanisms to tolerate commensals have also been described [32], which would dampen any effects we see. To detect these differences, we specifically looked at AMP production because different AMPs are produced downstream of Toll versus IMD activation [33]. While immune related genes as a group showed significant differences between conventionally reared whole adult flies and other treatments, when we examined individual genes across our dataset by ANOVA, only AttacinD stood out as a significantly overexpressed AMP in whole, conventionally reared flies (S8 Fig).…”

Antimicrobial effectors in the nematode Caenorhabditis elegans : an outgroup to the Arthropoda

“…As suggested for spp-5 [49], constitutively expressed effector genes might function in both defence and digestion, because they could enable the worm to access bacteria-derived nutrients and at the same time eliminate potential pathogens. Such a dual function of effectors is similarly discussed for Drosophila fruitflies, which also inhabit microbe-rich environments (see review by Broderick [84]). …”

“…Last but not least, it is conceivable that antimicrobial effectors in C. elegans are also used to control the worm's microbiome, in analogy to what is known for example for weevils (see review by Masson et al [97]) and proposed for fruitflies (see review by Broderick [84]). At the same time, it is possible that members of the worm's microbial associates themselves produce protective antimicrobial factors, thus increasing the nematode's arsenal of effector molecules.…”