An antifungal polyketide associated with horizontally acquired genes supports symbiont-mediated defense in Lagria villosa beetles

Laura V Flórez,Andre Rodrigues,Martin Kaltenpoth,Ian J Miller,Jason C Kwan,Christian Hertweck,Kirstin Scherlach

doi:10.1038/s41467-018-04955-6

Abstract

Microbial symbionts are often a source of chemical novelty and can contribute to host defense against antagonists. However, the ecological relevance of chemical mediators remains unclear for most systems. Lagria beetles live in symbiosis with multiple strains of Burkholderia bacteria that protect their offspring against pathogens. Here, we describe the antifungal polyketide lagriamide, and provide evidence supporting that it is produced by an uncultured symbiont, Burkholderia gladioli Lv-StB, which is dominant in field-collected Lagria villosa. Interestingly, lagriamide is structurally similar to bistramides, defensive compounds found in marine tunicates. We identify a gene cluster that is probably involved in lagriamide biosynthesis, provide evidence for horizontal acquisition of these genes, and show that the naturally occurring symbiont strains on the egg are protective in the soil environment. Our findings highlight the potential of microbial symbionts and horizontal gene transfer as influential sources of ecological innovation.

Highlights

Microbial symbionts are often a source of chemical novelty and can contribute to host defense against antagonists
Given that the symbiont strain composition in female L. villosa beetles was recently shown to differ between laboratory-reared and field-collected individuals[17], we determined the relative abundance of Burkholderia strains on beetle eggs laid by fieldcollected females (Fig. 1), and set out to characterize the bioactive molecules produced by the dominant symbiont strain (B. gladioli Lv-StB)
Beetles of the genus Lagria engage in a dynamic defensive symbiosis with multiple coinfecting B. gladioli strains

Summary

Introduction

Microbial symbionts are often a source of chemical novelty and can contribute to host defense against antagonists. For animals living in environments like humid soil and leaf litter, substantial exposure to complex and variable pathogen communities can represent a major threat demanding swift and flexible solutions that ensure survival In such scenarios, defense provided by symbiotic microorganisms might be advantageous due to the potential for higher versatility compared to host-encoded traits. There is a growing number of reports on bacteria with bioactive potential found in eukaryotic hosts[6,11,12]; knowledge on the chemical basis of symbiont-mediated defense in the field is scarce[3,5] This in-depth knowledge is fundamental for understanding the ecological context and evolutionary dynamics of protective symbioses[13,14,15,16]. We demonstrate its occurrence in field-collected beetles’ eggs, show its ability to inhibit fungal antagonists in vitro and in vivo, describe the chemical structure of the compound, and identify a gene cluster that may be responsible for its biosynthesis, providing evidence for the horizontal acquisition of the cluster

Methods

Results

Conclusion