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ARS Home » Midwest Area » Wooster, Ohio » Corn, Soybean and Wheat Quality Research » Research » Publications at this Location » Publication #241917

Title: A bacterial pathogen uses distinct type III secretion systems to alternate between host kingdoms

item CORREA, VALDIR - The Ohio State University
item MAJERCZAK, DORIS - The Ohio State University
item AMMAR, EL-DESOUKY - The Ohio State University
item MERIGHI, MASSIMO - The Ohio State University
item PRATT, RICHARD - The Ohio State University
item HOGENHOUT, SASKIA - John Innes Center
item COPLIN, DAVID - The Ohio State University
item Redinbaugh, Margaret

Submitted to: Applied and Environmental Microbiology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 7/9/2012
Publication Date: 8/9/2012
Citation: Correa, V.R., Majerczak, D.R., Ammar, E., Merighi, M., Pratt, R.C., Hogenhout, S.A., Coplin, D.L., Redinbaugh, M.G. 2012. A bacterial pathogen uses distinct type III secretion systems to alternate between host kingdoms. Applied and Environmental Microbiology. 78:6327-6336.

Interpretive Summary: In order to invade their plant or animal hosts, some bacterial pathogens secret proteins directly into host cells using needle-like protein structures. These protein structures, known as type III secretion systems or T3SS, are specialized for injecting proteins into either plant or animal cells. Most pathogenic bacteria have either the animal type or plant type T3SS depending on their host, but a few have both animal- and plant-type T3SS. Pantoea stewartii, which causes Stewart’s wilt in corn, has both the animal- and plant-type T3SS. Previous research demonstrated that the plant-type T3SS was necessary for the Stewart’s wilt bacteria to invade corn, but nothing was known about the function of the animal-type T3SS. Since this bacteria is transmitted in nature by flea beetles, we hypothesized that the animal-type T3SS is required for colonization of the flea beetle vector, Chaetocnema pulicaria. We could detect the Stewart’s wilt bacteria in the guts of flea beetles collected from corn fields, indicating that the bacteria resides in the insects. When we mutated a gene that is required for making the animal-type T3SS in Stewart’s wilt bacteria, the ability of the bacteria to persist in the insect gut was reduced and so was the ability of the insect to transmit the pathogen to corn. We could restore the ability of the bacteria to persist in and be transmitted by beetles by complementing the mutation. However, the mutant bacteria could infect corn similarly to non-mutant bacteria if we mechanically inoculated them into corn, indicating the animal-type T3SS wasn’t needed to invade the plant. These results demonstrate that the animal- and plant-type T3SS in Stewart’s wilt bacteria have different and essential roles in adapting the bacteria to its insect and corn hosts, and suggests similar mechanisms may be important in other bacteria that carry the two types of T3SS.

Technical Abstract: Plant and animal-pathogenic bacteria utilize phylogenetically distinct type III secretion systems (T3SS) that produce needle-like injectisomes or pili for the delivery of effector proteins into host cells. Pantoea stewartii subsp. stewartii (Pnss), the causative agent of Stewart’s bacterial wilt and leaf blight of maize, carries phylogenetically distinct T3SSs. In addition to an Hrc-Hrp T3SS, known to be essential for maize pathogenesis, Pnss has a second T3SS (PSI-2) that is required for persistence in its flea beetle vector, Chaetocnema pulicaria (Melsh). PSI-2 belongs to the Inv-Mxi-Spa T3SS family typically found in animal pathogens. Mutagenesis of the PSI-2 psaN gene, which encodes an ATPase essential for secretion of T3SS effectors by the injectisome, greatly reduces both the persistence of Pnss in flea beetle guts and the beetle’s ability to transmit Pnss to maize. Ectopic expression of the psaN gene complements these phenotypes. In addition, the PSI-2 psaN gene is not required for Pnss pathogenesis of maize and is transcriptionally up-regulated in insects compared to maize tissues. Thus, the Hrp and PSI-2 T3SSs play different roles in the life cycle of Pnss as it alternates between its insect vector and plant host.