Integrated multi-omic analysis of host-microbiota interactions in acute oak decline

Abstract

BackgroundBritain’s native oak species are currently under threat from acute oak decline (AOD), a decline-disease where stem bleeds overlying necrotic lesions in the inner bark and larval galleries of the bark-boring beetle, Agrilus biguttatus, represent the primary symptoms. It is known that complex interactions between the plant host and its microbiome, i.e. the holobiont, significantly influence the health status of the plant. In AOD, necrotic lesions are caused by a microbiome shift to a pathobiome consisting predominantly of Brenneria goodwinii, Gibbsiella quercinecans, Rahnella victoriana and potentially other bacteria. However, the specific mechanistic processes of the microbiota causing tissue necrosis, and the host response, have not been established and represent a barrier to understanding and managing this decline.ResultsWe profiled the metagenome, metatranscriptome and metaproteome of inner bark tissue from AOD symptomatic and non-symptomatic trees to characterise microbiota-host interactions. Active bacterial virulence factors such as plant cell wall-degrading enzymes, reactive oxygen species defence and flagella in AOD lesions, along with host defence responses including reactive oxygen species, cell wall modification and defence regulators were identified. B. goodwinii dominated the lesion microbiome, with significant expression of virulence factors such as the phytopathogen effector avrE. A smaller proportion of microbiome activity was attributed to G. quercinecans and R. victoriana. In addition, we describe for the first time the potential role of two previously uncharacterised Gram-positive bacteria predicted from metagenomic binning and identified as active in the AOD lesion metatranscriptome and metaproteome, implicating them in lesion formation.ConclusionsThis multi-omic study provides novel functional insights into microbiota-host interactions in AOD, a complex arboreal decline disease where polymicrobial-host interactions result in lesion formation on tree stems. We present the first descriptions of holobiont function in oak health and disease, specifically, the relative lesion activity of B. goodwinii, G. quercinecans, Rahnella victoriana and other bacteria. Thus, the research presented here provides evidence of some of the mechanisms used by members of the lesion microbiome and a template for future multi-omic research into holobiont characterisation, plant polymicrobial diseases and pathogen defence in trees.Electronic supplementary materialThe online version of this article (10.1186/s40168-018-0408-5) contains supplementary material, which is available to authorized users.

Identification and characterization of bacterial strains associated with diseased oak trees in Northern Iran

“…Acute Oak Decline symptoms are well characterized, when compared with problems caused by pathogenic fungi, insects and abiotic factors (Broberg et al, ; Brown, Inward, Jeger, & Denman, ; Denman et al, , ). In agreement with AOD reports from Britain, the height of the cankers on the tree trunk, the colour of the exudates and the sapwood damage were distinctive in Hyrcanian oaks (Table S1).…”

“…With advances in high‐throughput sequencing technologies and improved “omics” analyses (e.g., metagenomics), studies of tree and forest ecosystem microbiomes have increased (Feau & Hamelin, ). Broberg et al () developed a system‐level approach in AOD syndrome research that identified the more reliable roles of bacterial communities and functions in disease occurrence and progression. Brennaria goodwinii , R. victoriana and G. quercinecans were shown to act as polyspecies causative agents in AOD (Broberg et al, ).…”

“…Two types of oak decline have been characterized—Chronic Oak Decline (COD) and Acute Oak Decline (AOD)—with slow or rapid effects on oak trees, respectively. AOD affecting Quercus petrea and Quercus robur has recently been noted as a major problem in the United Kingdom (Broberg, Doonan, Mundt, Denman, & McDonald, ; Brown et al, ; Denman et al, , , ; Denman & Webber, ). Compared with COD, the symptoms of AOD are observed on stems (inner bark tissues) and include larval galleries of Agrilus biguttatus associated with symptomatic trees.…”

“…A systematic study was performed to determine microbial composition on healthy and AOD symptomatic oaks (Denman et al, ). Recent work has indicated that AOD involves a complex syndrome in which B. goodwinii , G. quercinecans and Rahnella victoriana act as polymicrobial causal agents (Broberg et al, ; Denman et al, ).…”

Bacillus pumilus and Stenotrophomonas maltophilia as two potentially causative agents involved in Persian oak decline in Zagros forests (Iran)

“…This implies that lesions that characterize oak decline are not caused by a single organism but are likely to have a polymicrobial cause (Brady et al, 2017;Broberg et al, 2018;Denman et al, 2018Denman et al, , 2016. Identification and characterization of all bacteria associated with bacterial etiolating and decline will ultimately improve our understanding of the aetiology of this phenomenon and may result in improved management techniques for control.…”