Antibiotic-producing symbionts dynamically transition between plant pathogenicity and insect-defensive mutualism

Laura V Flórez,Laura V Flórez,Andre Rodrigues,Martin Kaltenpoth,Christian Hertweck,Christian Hertweck,Martin Kaltenpoth,Paul Gaube,Elisabeth Sitte,Claudia Ross,Kirstin Scherlach,Cornelia Hermes

doi:10.1038/ncomms15172

Abstract

Pathogenic and mutualistic bacteria associated with eukaryotic hosts often lack distinctive genomic features, suggesting regular transitions between these lifestyles. Here we present evidence supporting a dynamic transition from plant pathogenicity to insect-defensive mutualism in symbiotic Burkholderia gladioli bacteria. In a group of herbivorous beetles, these symbionts protect the vulnerable egg stage against detrimental microbes. The production of a blend of antibiotics by B. gladioli, including toxoflavin, caryoynencin and two new antimicrobial compounds, the macrolide lagriene and the isothiocyanate sinapigladioside, likely mediate this defensive role. In addition to vertical transmission, these insect symbionts can be exchanged via the host plant and retain the ability to initiate systemic plant infection at the expense of the plant’s fitness. Our findings provide a paradigm for the transition between pathogenic and mutualistic lifestyles and shed light on the evolution and chemical ecology of this defensive mutualism.

Highlights

Pathogenic and mutualistic bacteria associated with eukaryotic hosts often lack distinctive genomic features, suggesting regular transitions between these lifestyles
We report on a transition between pathogenicity and mutualism in Burkholderia bacteria associated with a widespread group of herbivorous beetles, the Lagriinae (Coleoptera: Tenebrionidae)
To identify the bacterial symbionts associated with the invasive South American soybean pest Lagria villosa[8] and to confirm their vertical transmission route, we characterized the bacterial community in the symbiont-bearing structures of field-collected adult females and eggs laid by these females, as well as in larvae of laboratory cultures using 454 sequencing of bacterial 16S ribosomal RNA amplicons and quantitative PCR

Summary

Introduction

Pathogenic and mutualistic bacteria associated with eukaryotic hosts often lack distinctive genomic features, suggesting regular transitions between these lifestyles. Microbial symbionts influence virtually all aspects of eukaryote biology[2], and their impact on host fitness ranges from detrimental to beneficial, occasionally shifting along this continuum[3] Such shifts have important implications for the ecological and evolutionary dynamics of symbiosis, observations of recent or dynamic transitions between parasitic and mutualistic lifestyles are scarce, and reports on their occurrence rely largely on phylogenetic evidence[4]. We report on a transition between pathogenicity and mutualism in Burkholderia bacteria associated with a widespread group of herbivorous beetles, the Lagriinae (Coleoptera: Tenebrionidae) We show that these insect-defensive mutualists likely evolved from plant pathogenic bacteria, and that they can still infect a plant host, proposing an ecological context in which the lifestyle transition may have occurred. We elucidate symbiont-produced compounds that inhibit the growth of relevant microbial antagonists of the insect

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