title: AvrRxo1 Is a Bifunctional Type III Secreted Effector and Toxin-Antitoxin System Component with Homologs in Diverse Environmental Contexts.
abstract: Toxin-antitoxin (TA) systems are ubiquitous bacterial systems that may function in genome maintenance and metabolic stress management, but are also thought to play a role in virulence by helping pathogens survive stress. We previously demonstrated that the Xanthomonas oryzae pv. oryzicola protein AvrRxo1 is a type III-secreted virulence factor that has structural similarities to the zeta family of TA toxins, and is toxic to plants and bacteria in the absence of its predicted chaperone Arc1. In this work, we confirm that AvrRxo1 and its binding partner Arc1 function as a TA system when expressed in Escherichia coli. Sequences of avrRxo1 homologs were culled from published and newly generated phytopathogen genomes, revealing that avrRxo1:arc1 modules are rare or frequently inactivated in some species and highly conserved in others. Cloning and functional analysis of avrRxo1 from Acidovorax avenae, A. citrulli, Burkholderia andropogonis, Xanthomonas translucens, and Xanthomonas euvesicatoria showed that some AvrRxo1 homologs share the bacteriostatic and Rxo1-mediated cell death triggering activities of AvrRxo1 from X. oryzae. Additional distant putative homologs of avrRxo1 and arc1 were identified in genomic or metagenomic sequence of environmental bacteria with no known pathogenic role. One of these distant homologs was cloned from the filamentous soil bacterium Cystobacter fuscus. avrRxo1 from C. fuscus caused watersoaking and triggered Rxo1-dependent cell collapse in Nicotiana benthamiana, but no growth suppression in E. coli was observed. This work confirms that a type III effector can function as a TA system toxin, and illustrates the potential of microbiome data to reveal new environmental origins or reservoirs of pathogen virulence factors.
authors.affiliation: Department of Plant Pathology and Ecology, The Connecticut Agricultural Experiment Station, New Haven, CT, United States of America.
authors.forename: Lindsay R
authors.initials: LR
authors.lastname: Triplett
authors.affiliation: Department of Plant Pathology and Ecology, The Connecticut Agricultural Experiment Station, New Haven, CT, United States of America.
authors.forename: Teja
authors.initials: T
authors.lastname: Shidore
authors.affiliation: Department of Bioagricultural Sciences and Pest Management and Program in Plant Molecular Biology, Colorado State University, Fort Collins, CO, United States of America.
authors.forename: John
authors.initials: J
authors.lastname: Long
authors.affiliation: Department of Horticulture, Virginia Polytechnic Institute and State University, Blacksburg, VA, United States of America.
authors.forename: Jiamin
authors.initials: J
authors.lastname: Miao
authors.affiliation: Department of Horticulture, Virginia Polytechnic Institute and State University, Blacksburg, VA, United States of America.
authors.forename: Shuchi
authors.initials: S
authors.lastname: Wu
authors.affiliation: Department of Biochemistry, Virginia Polytechnic Institute and State University, Blacksburg, VA, United States of America.|Laboratory of Tropical Veterinary Medicine and Vector Biology, College of Agriculture, Hainan University, Haikou, 570228, Hainan, China.
authors.forename: Qian
authors.initials: Q
authors.lastname: Han
authors.affiliation: Department of Horticulture, Virginia Polytechnic Institute and State University, Blacksburg, VA, United States of America.
authors.forename: Changhe
authors.initials: C
authors.lastname: Zhou
authors.affiliation: Department of Bioagricultural Sciences and Pest Management and Program in Plant Molecular Biology, Colorado State University, Fort Collins, CO, United States of America.
authors.forename: Hiromichi
authors.initials: H
authors.lastname: Ishihara
authors.affiliation: Department of Biochemistry, Virginia Polytechnic Institute and State University, Blacksburg, VA, United States of America.
authors.forename: Jianyong
authors.initials: J
authors.lastname: Li
authors.affiliation: Department of Horticulture, Virginia Polytechnic Institute and State University, Blacksburg, VA, United States of America.
authors.forename: Bingyu
authors.initials: B
authors.lastname: Zhao
authors.affiliation: Department of Bioagricultural Sciences and Pest Management and Program in Plant Molecular Biology, Colorado State University, Fort Collins, CO, United States of America.
authors.forename: Jan E
authors.initials: JE
authors.lastname: Leach
mesh_terms: D001426:Bacterial Proteins / Q000235:genetics / Q000378:metabolism*; D058947:Bacterial Secretion Systems / Q000235:genetics / Q000378:metabolism*; D004926:Escherichia coli / Q000235:genetics / Q000378:metabolism; D010935:Plant Diseases / Q000382:microbiology; D014026:Nicotiana / Q000382:microbiology; D014974:Xanthomonas / Q000235:genetics / Q000378:metabolism*
chemical_list: D001426:Bacterial Proteins; D058947:Bacterial Secretion Systems