Linking metabolic phenotypes to pathogenic traits among ‘Candidatus Liberibacter asiaticus’ and its hosts

Authors: ZUNIGA, CRISTAL - University Of California; PEACOCK, BETH - University Of California; LIANG, BO - University Of California; McCollum, Thomas; IRIGOYEN, SONIA - Texas A&M University; DIEGO, TEC - University Of California; MAROTZ, CLARISSE - University Of California; WENG, NIEN-CHEN - University Of California; ZEPEDA, ALEJANDRO - Autonomous University Of Yucatan; VIDALAKIS, GEORGIOS - University Of California; MANDADI, KRANTHI - Texas A&M University; BORNEMAN, JAMES - University Of California; ZENGLER, KARSTEN - University Of California

Submitted to: NPJ Systems Biology and Applications
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 6/18/2020
Publication Date: 8/4/2020
Citation: Zuniga, C., Peacock, B., Liang, B., Mccollum, T.G., Irigoyen, S.C., Diego, T., Marotz, C., Weng, N., Zepeda, A., Vidalakis, G., Mandadi, K.K., Borneman, J., Zengler, K. 2020. Linking metabolic phenotypes to pathogenic traits among ‘Candidatus Liberibacter asiaticus’ and its hosts. NPJ Systems Biology and Applications. 6:24. https://doi.org/10.1038/s41540-020-00142-w.
DOI: https://doi.org/10.1038/s41540-020-00142-w

Interpretive Summary: Huanglongbing, regarded as the most devastating of all citrus diseases, threatens the sustainability of citrus production worldwide. In Florida Huanglongbing has resulted in a seventy percent reduction citrus production during the fifteen years since being confirmed present in the state. To prevent destruction of citrus industries it is essential that understanding Candidatus Liberibacter asiaticus, the microbe that is associated with Huanglongbing, be better understood. However, Candidatus Liberibacter asiaticus has yet to be grown in culture making study of the organism challenging. In this project, we conducted genome sequencing of citrus and Asian citrus psyllids, the insect that transmits Candidatus Liberibacter to citrus. In this project the genomes of six strains of Candidatus Liberibacter asiaticus were analyzed to identify metabolic pathways that may distinguish the strains. Results identified conserved and unique metabolic traits among the bacterial strains and revealed strain-specific interactions between CLas and its hosts, laying the foundation for the development of model-driven HLB-treatment strategies.

Technical Abstract: Candidatus Liberibacter asiaticus (CLas) has been suggested as the bacterial pathogen associated with Huanglongbing (HLB), also known as citrus greening, a lethal disease affecting citrus crops worldwide that reduces crop productivity by up to 80%. Although this putative pathogen has eluded cultivation, omic tools enabled genome sequencing of multiple CLas strains collected from the environment. Comparative genome analyses have provided preliminary insights into the metabolic capabilities of CLas. However, a comprehensive functional characterization of CLas’ metabolism is currently lacking, delaying the development of treatment strategies against this pathogen. Here we reconstructed and manually curated genome-scale metabolic models for the six CLas strains A4, FL17, gxpsy, Ishi-1, psy62, and YCPsy, in addition to a model of the most closely related microorganism, the culturable bacterium L. crescens BT-1. We predicted distinct nutritional requirements for each bacterium and performed experimental assays of growth phenotypes for CLas strains in hairy root-based systems and for L. crescens BT-1 in cultivation, thus determining and providing knowledge about their specific niches. Additionally, CLas models were constrained using expression data obtained from CLas-infected citrus trees, as well as from CLas residing in the psyllid host Diaphorina citri, revealing host-dependent metabolic phenotypes. Lastly, we determined the unique metabolic capabilities for all strain-specific variants of the seven Liberibacter spp. Results identified conserved and unique metabolic traits among the bacterial strains and revealed strain-specific interactions between CLas and its hosts, laying the foundation for the development of model-driven HLB-treatment strategies.