FUTURE OAK: Characterising and engineering the oak microbiome to future-proof an arboreal icon

Tree declines caused by climate perturbation, anthropogenic stressors and disease outbreaks have resulted in recent forest mega-disturbances and are a major global concern. Until recently, progress has been hampered by a lack of high-throughput analytical approaches for systems-based analysis of the multidimensional factors that drive declines. Our previous research on Acute Oak Decline, a complex decline disease of native British oak, has highlighted how microbiome shifts to a 'pathobiome', are associated with tree disease. This work challenges the one pathogen = disease paradigm, leading to new hypotheses on the role of microbiomes in health and disease, and highlighting the need to revise classical disease paradigms to include the microbiome. The microbiome is a major determinant of plant health, and we hypothesise that the oak microbiome can be manipulated to improve host fitness and disease suppression. Here, we propose a landscape-scale analysis of the oak microbiome and metabolome in health and disease, to inform the design and validation of engineered microbiomes for disease suppression. Microbiome engineering is an emerging research frontier with many novel applications. The project will address new hypotheses regarding how complex multidimensional interactions between the tree host and its microbiota, encountered pathogens, and the environment, influence host fitness and disease susceptibility. The research will initiate a new frontier in forest microbiome engineering and precision medicine to future-proof iconic tree species and the ecosystem services they provide.

Forest disturbances mediated by climate perturbation and tree disease outbreaks represent a significant global challenge. Tree declines are complex and involve both biotic and abiotic stressors, and consequently, limited progress has been achieved in understanding the multi-dimensional interactions between the host and its associated microbiota, pathogenic microorganisms, and the environment, that underpin tree health and disease. However, recent developments in high-throughput analytical approaches for nucleic acid sequencing, metabolite profiling and microbial isolation, coupled with advances in machine learning computational approaches, now enable systems-based analyses of the multi-scale interactions that confer unprecedented insights into complex tree diseases. This proposal addresses new hypotheses on the role of the microbiome in health and disease, using Acute Oak Decline (AOD), a complex decline disease mediated by abiotic predisposing factors and biotic (insect and bacterial) contributing factors, as a model system. The project will deliver a systems-based analysis of AOD at the landscape-scale, representing the most comprehensive analysis of a tree disease to date, and the first to integrate host, microbiota and ecological factors at this level (Obj. 1). Consequently, these data will be used to identify and isolate oak microbiota associated with host fitness and disease suppression, validated by experimental ecology approaches (Obj. 2). Engineered microbiomes will be designed and tested to engineer the oak microbiome for increased resilience and host fitness (Obj. 3). Finally, we will assess the feasibility and management implications of deploying engineered microbiomes to address tree health challenges (Obj. 4).The project will provide a paradigm-shift in our understanding of the factors that drive complex tree declines, initiating a new era of microbiome engineering to future proof global forests and the ecosystem services they provide.

Complex interactions between plant hosts and their associated microbiota significantly influence the health status of an individual. The plant microbiome (the collection of plant-associated microorganisms and their encoded genes) is therefore a major determinant of health and productivity, promoting nutrient availability, resistance to environmental stresses, and defence from pathogens. Climate change and increasing outbreaks of disease represent a major threat to global forests that support the most diverse ecosystems in the biosphere, provide key ecosystem services, and valuable forest products. However, advances in high-throughput DNA sequencing technologies are transforming our understanding of plant-microbiota interactions and will play a central role in the future preservation of global plant health. In addition, engineering plant and animal microbiomes using cultivated disease suppressive microbiota is an emerging research frontier with many novel applications. Here, we will undertake a UK landscape-scale analysis of the oak microbiome and metabolome in health and disease, to inform the design and validation of engineered microbiomes for disease suppression. Microbiome engineering is an emerging research frontier with many novel applications. The project will address new hypotheses regarding how complex multidimensional interactions between the tree host and its microbiota, encountered pathogens, and the environment, influence host fitness and disease susceptibility. The research will inform future efforts to select optimal environmental conditions, microbiome composition and host genetics for tree health and resilience, initiating a new frontier in forest microbiome engineering to future-proof iconic tree species and the ecosystem services they provide. This project will be the first to focus on the core microbiome of oak trees and will address a key knowledge gap in oak microbiome research. Although AOD is the disease focus in this project, similar decline diseases are being described globally, with reports of similar oak diseases and detection of bacterial agents related to the cause of AOD described globally. The reports highlight that AOD is likely an underreported and emerging global issue and represents only one of the many current threats to oak, notwithstanding Xyllela fastidiosa, that has not currently been detected in the UK, but remains an imminent threat. Consequently, data on the healthy core microbiome and disease suppressive microbiota obtained in this project could translate to suppression of other pests and pathogens of oak at the EU and global scale, such as Chronic Oak Decline, Phytophthora spp., Oak Processionary Moth, and bark boring beetle attack, for example, and the tools and approach can ultimately be translated for application in other at-risk tree species. Microbiome engineering for disease suppression is a new frontier in plant and animal health and represents a promising approach to safeguard the health of forest biomes. The research proposed here therefore has global relevance and will feed into international efforts to protect native oak species globally. The project outputs would also directly align with DEFRA's 'Tree Health Resilience Strategy', part of the UK government's 25-year plan to improve the environment through protecting broadleaf woodlands from pests and disease.