Disease-induced microbial shifts in citrus indicate microbiome-derived responses to Huanglongbing across the disease severity spectrum

Authors: GINNAN, NICOLE - University Of California; DANG, TYLER - University Of California; BODAGHI, SOHRAB - University Of California; RUEGGER, PAUL - University Of California; McCollum, Thomas; ENGLAND, GARY - University Of Florida; VIDILAKIS, GEORGIOS - University Of California; BORNEMAN, JAMES - University Of California; ROLSHAUSEN, PHILLPPE - University Of California; ROPER, CAROLINE - University Of California

Submitted to: The ISME Journal: Multidisciplinary Journal of Microbial Ecology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 4/10/2020
Publication Date: 7/14/2020
Citation: Ginnan, N.A., Dang, T., Bodaghi, S., Ruegger, P.M., Mccollum, T.G., England, G., Vidilakis, G., Borneman, J., Rolshausen, P.E., Roper, C.M. 2020. Disease-induced microbial shifts in citrus indicate microbiome-derived responses to Huanglongbing across the disease severity spectrum. The ISME Journal: Multidisciplinary Journal of Microbial Ecology. online. https://doi.org/10.1094/PBIOMES-04-20-0027-R.
DOI: https://doi.org/10.1094/PBIOMES-04-20-0027-R

Interpretive Summary: Huanglongbing disease has devastated the Florida citrus industry during the last 15 years and actually threatens survival of citrus worldwide. There is a desperate need to develop strategies to mitigate the impact of Huanglongbing. The microbiome is the genetic material of all the microbes - bacteria, fungi, protozoa and viruses - that live on and inside another organism. Plant microbiomes have proven to be important to plant health and can influence disease outcomes. In this project we determined how the citrus microbiome relate to the development of Huanglongbing disease. We found shifts within the citrus microbiome at different levels of Huanglongbing (HLB) disease severity. Based on our findings we propose a disease ecology model that illustrates the relationship between the pathogen that causes Huanglongbing and identified microorganisms that may be disease facilitators or antagonists. Our findings lay the foundation for consideration of practices that enrich for or enhance microbial keystone and beneficial taxa as part of routine agriculture cultural practices and disease management schemes.

Technical Abstract: Plant microbiomes are critical components to plant health and can influence disease outcomes. We provide empirical data describing disease-induced shifts within the citrus microbiome at different levels of Huanglongbing (HLB) disease severity. HLB is associated with a phloem-limited bacterium, Candidatus Liberibacter asiaticus, that is introduced into the aerial portions of the tree by an insect vector. Disease manifests as above ground foliar and fruit symptoms and significant root decline below ground. During the early phase of disease, there were depletions of putative keystone species in leaves and roots, followed by enrichment of putative beneficial species suggesting a microbial response involved in plant protection. In the late phase of disease when trees are classified as severely diseased, we observed enrichments of parasitic and saprophytic microorganisms particularly in the roots. Furthermore, we define key taxa enriched in trees with a slower rate of disease development, referred to as survivor trees, that are hallmarks of those in trees in the early phase of disease that may be drivers of the survivor tree phenotype. We propose a disease ecology model that illustrates the relationship between the pathogen, the microbiome and the plant that highlights microorganisms that may be disease facilitators or antagonists.