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

Cristal Zuñiga; Beth Peacock; Bo Liang; Greg McCollum; Sonia C Irigoyen; Diego Tec-Campos; Clarisse Marotz; Nien-Chen Weng; Alejandro Zepeda; Georgios Vidalakis; Kranthi K Mandadi; James Borneman; Karsten Zengler

doi:10.1038/s41540-020-00142-w

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

NPJ Syst Biol Appl. 2020 Aug 4;6(1):24. doi: 10.1038/s41540-020-00142-w.

Authors

Cristal Zuñiga¹, Beth Peacock^#², Bo Liang^#^{1

3}, Greg McCollum⁴, Sonia C Irigoyen⁵, Diego Tec-Campos^{1

6}, Clarisse Marotz¹, Nien-Chen Weng¹, Alejandro Zepeda⁶, Georgios Vidalakis², Kranthi K Mandadi^{5

7}, James Borneman⁸, Karsten Zengler^{9

10

11}

Affiliations

¹ Department of Pediatrics, University of California, San Diego, 9500 Gilman Drive, La Jolla, CA, 92093-0760, USA.
² Department of Microbiology and Plant Pathology, University of California, Riverside, 900 University Avenue, Riverside, CA, 92521, USA.
³ State Key Laboratory of Bioreactor Engineering and Institute of Applied Chemistry, East China University of Science and Technology, Shanghai, People's Republic of China.
⁴ USDA, ARS, US Horticultural Research Laboratory, 2001 S. Rock Road, Fort Pierce, FL, 34945, USA.
⁵ Texas A&M AgriLife Research and Extension Center, Texas A&M University System, Weslaco, TX, USA.
⁶ Facultad de Ingeniería Química, Universidad Autónoma de Yucatán, Campus de Ciencias Exactas e Ingenierías, Mérida, 97203, Yucatán, México.
⁷ Department of Plant Pathology and Microbiology, Texas A&M University, College Station, TX, USA.
⁸ Department of Microbiology and Plant Pathology, University of California, Riverside, 900 University Avenue, Riverside, CA, 92521, USA. borneman@ucr.edu.
⁹ Department of Pediatrics, University of California, San Diego, 9500 Gilman Drive, La Jolla, CA, 92093-0760, USA. kzengler@ucsd.edu.
¹⁰ Department of Bioengineering, University of California, San Diego, La Jolla, CA, 92093-0412, USA. kzengler@ucsd.edu.
¹¹ Center for Microbiome Innovation, University of California, San Diego, 9500 Gilman Drive, La Jolla, CA, 92093-0403, USA. kzengler@ucsd.edu.

^# Contributed equally.

Abstract

Candidatus Liberibacter asiaticus (CLas) has been associated with Huanglongbing, a lethal vector-borne disease affecting citrus crops worldwide. While comparative genomics has provided preliminary insights into the metabolic capabilities of this uncultured microorganism, a comprehensive functional characterization is currently lacking. 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 closest related culturable microorganism, L. crescens BT-1. Predictions about nutrient requirements and changes in growth phenotypes of CLas were confirmed using in vitro hairy root-based assays, while the L. crescens BT-1 model was validated using cultivation assays. Host-dependent metabolic phenotypes were revealed using expression data obtained from CLas-infected citrus trees and from the CLas-harboring psyllid Diaphorina citri Kuwayama. These results identified conserved and unique metabolic traits, as well as strain-specific interactions between CLas and its hosts, laying the foundation for the development of model-driven Huanglongbing management strategies.

Publication types

Research Support, Non-U.S. Gov't
Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

Citrus / microbiology
Host-Pathogen Interactions*
Liberibacter / metabolism*
Liberibacter / physiology
Phenotype*
Plant Diseases / microbiology