Abstract
Multicellular organisms can be regarded as metaorganisms, comprising of a macroscopic host interacting with associated microorganisms. Within this alliance, the host has to ensure attracting beneficial bacteria and defending against pathogens to establish and maintain a healthy homeostasis. Here, we obtained several lines of evidence arguing that Aurelia aurita uses interference with bacterial quorum sensing (QS) - quorum quenching (QQ) - as one host defense mechanism. Three A. aurita-derived proteins interfering with bacterial QS were identified by functionally screening a metagenomic library constructed from medusa-derived mucus. Native expression patterns of these host open reading frames (ORFs) differed in the diverse life stages (associated with different microbiota) pointing to a specific role in establishing the developmental stage-specific microbiota. Highly increased expression of all QQ-ORFs in germ-free animals further indicates their impact on the microbiota. Moreover, incubation of native animals with pathogenic bacteria induced expression of the identified QQ-ORFs arguing for a host defense strategy against confronting bacteria by interference with bacterial QS. In agreement, immobilized recombinant QQ proteins induced restructuring of polyp-associated microbiota through changing abundance and operational taxonomic unit composition. Thus, we hypothesize that additional to the immune system host-derived QQ-activities potentially control bacterial colonization.
Highlights
In natural habitats, members of different kingdoms of life do not exist isolated from one another but form complex associations and are connected to each other by diverse interactions[1]
The functional screen resulted in the identification of 17 single fosmid clones interfering with Gram-negative acyl-homoserine lactones (AHLs), three interfering with universal autoinducer-2 (AI-2), and two fosmid clones simultaneously interfering with both quorum sensing (QS) signaling molecules
quorum quenching (QQ) activities against both signaling molecules were evaluated using reporter strains AI1-QQ.[1] and AI2-QQ.[121] and respective control experiments, both clearly demonstrated that all three proteins effectively interfered with AHL and AI-2 QS signals (Fig. 2B)
Summary
Members of different kingdoms of life do not exist isolated from one another but form complex associations and are connected to each other by diverse interactions[1]. One of the best-studied marine examples with regard to chemically mediated interactions between a host and its epiphytic bacteria is the red alga Delisea pulchra[9]. D. pulchra produces a halogenated furanone that antagonizes acylated homoserine lactones (AHL), the key signaling molecules of Gram-negative bacteria for QS The presence of this antagonist inhibits biofilm formation, protecting the alga against fouling[10]. The moon jellyfish Aurelia aurita, a member of the marine evolutionarily ancient phylum Cnidaria, has been put into focus. This invertebrate represents one of the most widely distributed Scyphozoa[12] and shows a complex life cycle[13]. We intended to gain insights into fundamental host-microbe interactions already present in a basal metazoan
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