Reciprocal immune benefit based on complementary production of antibiotics by the leech Hirudo verbana and its gut symbiont Aeromonas veronii

Abstract

The medicinal leech has established a long-term mutualistic association with Aeromonas veronii, a versatile bacterium which can also display free-living waterborne and fish- or human-pathogenic lifestyles. Here, we investigated the role of antibiotics in the dynamics of interaction between the leech and its gut symbiont Aeromonas. By combining biochemical and molecular approaches, we isolated and identified for the first time the antimicrobial peptides (AMPs) produced by the leech digestive tract and by its symbiont Aeromonas. Immunohistochemistry data and PCR analyses evidenced that leech AMP genes are induced in the gut epithelial cells when Aeromonas load is low (starved animals), while repressed when Aeromonas abundance is the highest (post blood feeding). The asynchronous production of AMPs by both partners suggests that these antibiotic substances (i) provide them with reciprocal protection against invasive bacteria and (ii) contribute to the unusual simplicity of the gut microflora of the leech. This immune benefit substantially reinforces the evidence of an evolutionarily stable association between H. verbana and A. veronii. Altogether these data may provide insights into the processes making the association with an Aeromonas species in the digestive tract either deleterious or beneficial.

Characteristics of meiofauna in extreme marine ecosystems: a review

“…In the last decade, AMPs have also been shown to control and confine the symbiotic microflora in specific anatomical compartments (e.g. gut, bacteriomes, skin), thus contributing to the symbiostasis of both invertebrates and vertebrates (Salzman et al 2009;Gallo and Nakatsuji 2011;Login et al 2011;Franzenburg et al 2013;Tasiemski et al 2015). A substantial body of data demonstrates that AMPs not only act internally but can also be secreted into the environment surrounding an organism where they participate in external immunity, referred to as Bany heritable trait acting outside of an organism improving protection from pathogens or manipulating the composition of the microbial community in favor of an organism^ (Otti et al 2014).…”

Life history and eco‐evolutionary dynamics in light of the gut microbiota

“…In mice, individuals treated with antibiotics or raised under germ‐free conditions have significantly impaired immune responses, and are thus more susceptible to pathogens (Belkaid and Hand ). As discussed previously, commensal bacteria produce signals that can enhance expression of host defense genes, such as AMPs, which have the dual effect of promoting their own containment and to limit pathogen invasion (Belkaid and Hand , Tasiemski et al ). In mice, the loss of microbiota‐induced antimicrobial lectin leads to increased bacterial dissemination and susceptibility to bacterial pathogens (Kamada et al , Belkaid and Hand ).…”

“…The intestinal epithelium, as the outermost cell layer, constitutes the first line of defense, ensuring the elimination of pathogens while maintaining a coexistence with mutualistic partners (Belkaid and Hand , Gilbert et al ). AMPs (Box 1), natural antibiotics produced in the gut of most animals, are of particular importance in shaping the gut microbiota, in both vertebrate and invertebrate species (Franzenburg et al , Ostaff et al , Tasiemski et al ). When their expression is reduced, either experimentally or in the context of immune deficiencies, it results in a dramatic alteration of gut microbial communities (Ostaff et al ).…”

“…The molecular dialog between hosts and gut symbionts starts to be deciphered, highlighting a crucial role of host immune pathways in the acquisition and control of gut microbiota (Vavre and Kremer , Tasiemski et al ). Although the study of these mechanisms is still in its infancy, it may provide an opportunity to better understand host–microbiota interactions, as well as their ecological and evolutionary impacts.…”

Invasions of Host-Associated Microbiome Networks

“…Indeed, in WH systems, competitive interactions of resident species can help prevent invasions. For instance, gut microbiota species in leeches have been shown to prevent invasions by production of antibiotics (Graf et al 2006;Tasiemski et al 2015). Also, experimental evolution studies in a nematode model showed how a resident bacteria rapidly evolved increased antimicrobial superoxide production as a defense against Staphylococcus aureus infections .…”