Interactions in the bacterial pathobiome associated with crown gall disease: coexistence or competition?
Final Report Abstract
Crown gall is an important plant disease causing economic losses on numerous agricultural crops worldwide. The causal agents of this disease are tumorigenic bacteria belonging to the family Rhizobiaceae, collectively named tumorigenic agrobacteria. These phytopathogenic bacteria harbor a tumor-inducing (Ti) plasmid that is indispensable for pathogenicity. Pathogenesis of tumorigenic agrobacteria involves genetic transformation of host plant and thus formation of an ecological niche (tumors or galls), in which specific metabolites (i.e., opines) are produced. Opines provide the pathogen with multiple competitive advantages, but they can also be utilized by other bacteria colonizing galls. This project focused on crown gall of rhododendron, a disease that recurrently occurred in Northern Germany during the last decades. In a study preceding this project, which was also conducted by our group, the etiology of this disease was resolved, and novel strains of tumorigenic Rhizobium sp. were discovered. In this project, these atypical Rhizobium strains were further analyzed and the obtained results showed that they represent a novel species of the genus Rhizobium for which the name Rhizobium rhododendri was proposed. Furthermore, important insights on the genome architecture and evolution of chromids and plasmids of R. rhododendri were provided. In particular, the obtained findings contribute to a better understanding of the evolution and diversification of Ti plasmids. Furthermore, in this project, the bacterial pathobiome associated with crown gall tumors (gallobiome) on rhododendron was comprehensively investigated. The obtained results clearly indicated that R. rhododendri and the group of Agrobacterium spp., primarily belonging to the so-called “rubi” clade were the dominant members of bacterial microbiota in rhododendron galls. While the Ti plasmid-harboring R. rhododendri strains are causative agents of crown gall disease, Agrobacterium spp. strains were nonpathogenic and carried genes for the catabolism of opines, enabling these bacteria to efficiently colonize tumor tissue. Overall, tumorigenic R. rhododendri and nonpathogenic opine-catabolizing Agrobacterium spp. were considered the key players within the bacterial microbiota associated with aerial crown gall tumors on rhododendron. The results of greenhouse plant inoculation trials indicated that these two bacteria stably coexist within the pathobiome of crown gall tumors. In other words, the population of the pathogen is maintained in the multispecies community and not outcompeted by nonpathogenic opine-catabolizing bacteria, which unlike pathogen, do not have great fitness costs associated with pathogenesis. However, disease severity (size of galls) was reduced when plants were inoculated with both of these bacteria, compared to treatments involving inoculation with the pathogen alone. Although the underlying mechanism associated with reduced tumor size remains to be investigated, nontumorigenic Agrobacterium sp. might be a promising agent in the biocontrol of crown gall disease. Taken together, the results obtained provide a solid ground to further study the epidemiology and ecology of crown gall, as well as to develop new and more sustainable strategies for disease management.
Publications
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A novel plant tumorigenic Rhizobium sp. associated with crown gall disease of rhododendron, as revealed through genomics. 6th Joint Conference of the DGHM & VAAM – 72nd Annual Meeting of the DGHM & Annual Meeting of the VAAM, Leipzig, Deutschland, Abstract Book.
Kuzmanović, N., Idczak, E., Wagner, S., Götz, M., Spröer, C., Bunk, B., Overmann, J. & Smalla, K.
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Bacterial community composition of crown gall tumors on rhododendron. FEMS Conference on Microbiology in association with Serbian Society of Microbiology : 30 June - 2 July 2022, Serbia ; Electronic Abstract Book.
Kuzmanović, N., Nesme, J., Spröer, C., Bunk, B., Overmann, J., Sørensen, S. & Smalla, K.
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Wurzelhalsgallenkrebs - Epidemiologie, Pathogendiagnostik, der Erreger und ihrer Plasmide. JKI Datenblätter - Pflanzenkrankheiten und Diagnose 2022 (1): 1-13
Kuzmanović, N. & Smalla, K.
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Diversity and Evolutionary History of Ti Plasmids of “tumorigenes” Clade of Rhizobium spp. and Their Differentiation from Other Ti and Ri Plasmids. Genome Biology and Evolution, 15(8).
Kuzmanović, Nemanja; Wolf, Jacqueline; Will, Sabine Eva; Smalla, Kornelia; diCenzo, George C. & Neumann-Schaal, Meina
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Genomics and taxonomy of the “tumorigenes” clade of the family Rhizobiaceae. 10th Congress of European Microbiologists (FEMS 2023), Hamburg, Germany, July 09-13.
Kuzmanović, N., diCenzo, G. C., Bunk, B., Spröer, C., Frühling, A., Neumann‐Schaal, M., Overmann, J. & Smalla, K.
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Genomics of the “tumorigenes” clade of the family Rhizobiaceae and description of Rhizobium rhododendri sp. nov.. MicrobiologyOpen, 12(2).
Kuzmanović, Nemanja; diCenzo, George C.; Bunk, Boyke; Spröer, Cathrin; Frühling, Anja; Neumann‐Schaal, Meina; Overmann, Jörg & Smalla, Kornelia
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Neue Einblicke in die Vielfalt der tumorauslösenden Agrobakterien. 63. Deutsche Pflanzenschutztagung: Pflanzenschutz morgen - Transformation durch Wissenschaft; 26. bis 29. September 2023
Kuzmanović, N., Idczak, E., Götz, M. & Smalla, K.
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Deciphering the Key Players of the Bacterial Microbiota Associated with Aerial Crown Gall Tumors on Rhododendron: Insights into the Gallobiome. Phytobiomes Journal, 8(3), 401-415.
Kuzmanović, Nemanja; Nesme, Joseph; Wolf, Jacqueline; Neumann-Schaal, Meina; Petersen, Jörn; Fernandez-Gnecco, Gabriela; Spröer, Cathrin; Bunk, Boyke; Overmann, Jörg; Sørensen, Søren Johannes; Idczak, Elke & Smalla, Kornelia
