Host–microbiota–insect interactions drive emergent virulence in a complex tree disease

Abstract

Forest declines caused by climate disturbance, insect pests and microbial pathogens threaten the global landscape, and tree diseases are increasingly attributed to the emergent properties of complex ecological interactions between the host, microbiota and insects. To address this hypothesis, we combined reductionist approaches (single and polyspecies bacterial cultures) with emergentist approaches (bacterial inoculations in an oak infection model with the addition of insect larvae) to unravel the gene expression landscape and symptom severity of host–microbiota–insect interactions in the acute oak decline (AOD) pathosystem. AOD is a complex decline disease characterized by predisposing abiotic factors, inner bark lesions driven by a bacterial pathobiome, and larval galleries of the bark-boring beetle Agrilus biguttatus . We identified expression of key pathogenicity genes in Brenneria goodwinii , the dominant member of the AOD pathobiome, tissue-specific gene expression profiles, cooperation with other bacterial pathobiome members in sugar catabolism, and demonstrated amplification of pathogenic gene expression in the presence of Agrilus larvae. This study highlights the emergent properties of complex host–pathobiota–insect interactions that underlie the pathology of diseases that threaten global forest biomes.

Application of ecological and evolutionary theory to microbiome community dynamics across systems

“…Such advances require the development of theoretical and conceptual frameworks such as those discussed in §3 to drive hypothesis generation and predictions that can be tested through the careful design of empirical studies. The field of microbiome research therefore transcends disciplines, as exemplified by the diversity of methodological and analytical approaches described in the contributions to the special feature, including mathematical modelling [9,[16][17][18], DNA and RNA sequencing [7,10,14,18], flow cytometry [14], infection tests in model and non-model pathosystems [7,18], physico-chemical and volatile analysis [7], and measures of hormone activity to assess host physiological responses to its environment [10]. A major theme pervading this special feature is the link between mathematical model simulations and empirical studies [9,11,16,17].…”

“…Their analysis suggests that the 'EcoReality' of microbiota transplant studies has increased over time, and they present a roadmap for enhancing EcoReality in future transplantation experiments. Following this theme, Doonan et al [18] describe the emergent properties of host-microbiota-insect interactions that drive AOD, a complex decline disease of oak trees. They combined in vitro transcriptome experiments comprising single and poly-species bacterial cultures growing on oak tissue, with more complex infection tests combining bacterial inoculations with the addition of beetle larvae in a novel oak log infection model, to demonstrate the cumulative impact of these interactions on the pathology of AOD.…”

“…Emergent properties cannot be explained by their individual components, and the outcome of these interactions is greater than the sum of its individual parts and not irreducible to their individual components [19]. Using emergent virulence as a conceptual framework to assess the interactions between the host, microbiota and insects in AOD, Doonan et al [18] combined reductionist (RNAseq analysis of single and dual cultures of bacterial species) and emergentist approaches (log infection tests inoculated with insect larvae and bacterial cultures) to demonstrate the emergent properties of microbe-microbe and host-microbiota-insect interactions. These experiments revealed cooperation between key bacteria associated with tissue necrosis in affected trees, and in the presence of beetle larvae, gene expression of bacterial virulence genes and symptom severity (tissue necrosis) were amplified, demonstrating the emergent properties of microbiota-host-insect interactions in AOD symptomology.…”

“…Combinations of reductionist approaches and more complex experiments in vivo for model systems where they are more amenable, for example, where ethical considerations are less restrictive compared to human microbiome studies (e.g. infection tests and microbiota transplants in plants), provide excellent opportunities to explore such hypotheses [18]. Angell & Rudi [16] investigated factors that shape the assembly, dynamics and diversity of the infant gut microbiota within the first 12 months of age.…”

“…Niche availability and niche discordance are key factors that govern the capacity for a lineage with a certain phenotype to persist in an environment. Two relevant empirical studies in this special feature also address the functional interactions between plant hosts, microbiota and the environment in the context of plant disease [7,18].…”