Antimicrobial peptides and cell processes tracking endosymbiont dynamics

Abstract

One contribution of 13 to a theme issue 'Evolutionary ecology of arthropod antimicrobial peptides'. Many insects sustain long-term relationships with intracellular symbiotic bacteria that provide them with essential nutrients. Such endosymbiotic relationships likely emerged from ancestral infections of the host by free-living bacteria, the genomes of which experience drastic gene losses and rearrangements during the host-symbiont coevolution. While it is well documented that endosymbiont genome shrinkage results in the loss of bacterial virulence genes, whether and how the host immune system evolves towards the tolerance and control of bacterial partners remains elusive. Remarkably, many insects rely on a 'compartmentalization strategy' that consists in secluding endosymbionts within specialized host cells, the bacteriocytes, thus preventing direct symbiont contact with the host systemic immune system. In this review, we compile recent advances in the understanding of the bacteriocyte immune and cellular regulators involved in endosymbiont maintenance and control. We focus on the cereal weevils Sitophilus spp., in which bacteriocytes form bacteriome organs that strikingly evolve in structure and number according to insect development and physiological needs. We discuss how weevils track endosymbiont dynamics through at least two mechanisms: (i) a bacteriome local antimicrobial peptide synthesis that regulates endosymbiont cell cytokinesis and helps to maintain a homeostatic state within bacteriocytes and (ii) some cellular processes such as apoptosis and autophagy which adjust endosymbiont load to the host developmental requirements, hence ensuring a fine-tuned integration of symbiosis costs and benefits.This article is part of the themed issue 'Evolutionary ecology of arthropod antimicrobial peptides'.

Antimicrobial defence and persistent infection in insects revisited

“…Persistent associations between hosts and microbes are often not pathogenic; mutualists in insects, for example, establish persistent colonization of host organs and provide benefits to the hosts [6]. Such persistent associations by mutualists are maintained by AMPs [7].…”

Perspectives on the evolutionary ecology of arthropod antimicrobial peptides

“…Microbes entering the gut can potentially become pathogenic, but perhaps could also be considered as competitors for food (in the sense of Janzen's inter-kingdom competition between microbes and, in the original version, scavengers [90]). In many invertebrates, AMPs play an important role interacting with the gut microbiota [91] or co-evolved symbionts [10,92]. Studies in C. elegans have demonstrated that the combination of AMPs expressed in the gut differs from the composition of AMPs expressed on the exterior cuticle [56], which would add to the interaction scenario.…”

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

“…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.…”