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

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.

The specificity of Burkholderia symbionts in the social amoeba farming symbiosis: Prevalence, species, genetic and phenotypic diversity

“…Environmentally acquired Burkholderia infections are prevalent in many groups of insects, and these Burkholderia play diverse roles in the lives of their hosts, including enhancing immunity (Kim et al, ), providing insecticide resistance (Kikuchi et al, ), and protecting against fungal pathogens (Flórez et al, ). The specificity and dynamics of these interactions are variable, as some insect groups associate with a wide range of Burkholderia in the plant beneficial and environmental group (Flórez et al, ; Garcia et al, ; Kikuchi, Hosokawa, & Fukatsu, ). Burkholderia symbioses are more promiscuous in the Riptortus bean bug system, where these insects are colonized each generation by genetically diverse Burkholderia strains (Takeshita & Kikuchi, ).…”

“…Lagria beetles have more specific interactions with their environmentally acquired Burkholderia symbionts from the B. gladioli clade (Flórez et al, ). Two closely related clades of B. gladioli bacteria infect these beetles in a similar pattern to the one we find in the B. agricolaris symbionts of amoebae.…”

Angiosperm to Gymnosperm host‐plant switch entails shifts in microbiota of theWelwitschiabug,Probergrothius angolensis(Distant, 1902)

“…As pyrrhocorids are known to transmit gut bacteria on the egg surface (Kaltenpoth, Winter, & Kleinhammer, 2009;Salem, Florez, Gerardo, & Kaltenpoth, 2015), the symbionts may protect the eggs that are laid in leaf litter or soil substrate against opportunistic fungi (Schaefer & Ahmad, 2000), as has recently been shown in Lagria beetles (Flórez et al, 2017(Flórez et al, , 2018. In other insects, Klebsiella are commonly found in the gut (Engel & Moran, 2013) and are known to have wide-ranging metabolic capabilities, including nitrogen fixation, and can utilize diverse food sources (Temme, Zhao, & Voigt, 2012).…”

Horizontal gene transfer to a defensive symbiont with a reduced genome amongst a multipartite beetle microbiome

“…Mutualistic symbioses between animals and bacteria, widespread in nature, serve a variety of functions such as biosynthesis of nutrients not found in the host’s diet (Akman et al, 2002; Shigenobu et al, 2000), and protection from predation (Lopera et al, 2017; Miller et al, 2016a; Piel, 2002) or infection (Currie et al, 1999; Flórez et al, 2018; Kroiss et al, 2010). Such relationships exist on a continuous spectrum of dependency and exclusivity from the perspective of both the host and symbiont.…”

“…However, in field collections of L. villosa , Lv-StA is only found sporadically, and is never highly abundant (Flórez and Kaltenpoth, 2017). Instead, the most abundant strain is often the uncultured Lv-StB (Flórez and Kaltenpoth, 2017), which has been implicated in the production of the antifungal lagriamide, a defensive compound found in field egg collections (Flórez et al, 2018). We previously found through metagenomic sequencing that the genome of Lv-StB was much smaller than that of Lv-StA, suggesting it has undergone genome reduction (Flórez et al, 2018).…”