Rapid dissemination of host metabolism–manipulating genes via integrative and conjugative elements
Elena Colombi 1,2, Frederic Bertels 3, Guilhem Doulcier 4, Ellen McConnell 3, Tatyana Pichugina 3, Kee Hoon Sohn 5,6,7,8, Christina Straub 9,10, Honour C. McCann* 11, and Paul B. Rainey* 3,4
1 School of Natural Sciences, Macquarie University, New South Wales, Sydney Australia
2 ARC Centre of Excellence for Synthetic Biology, Macquarie University, New South Wales, Sydney, Australia
3 Department of Microbial Population Biology, Max Planck Institute for Evolutionary Biology, Plön24306, Germany
4 Laboratoire Biophysique et Évolution, Institut Chemie Biologie Innovation, École Supérieure de Physique et de Chemie Industrielles de la Ville de Paris, Université Paris Science et Lettres, Centre National de al Reserche Scientifique, Paris 75005, France
5 Plant Immunity Research Center, Seoul National University, Seoul 08826, Republic of Korea
6 Department of Agricultural Biotechnology, Seoul National University, Seoul 08826, Republic of Korea
7 Research Institute of Agriculture and Life Sciences, Seoul National University, Seoul 08826, Republic of Korea
8 Plant Genomics and Breeding Institute, Seoul National University, Seoul 08826, Republic of Korea
9 Health and Environment, Institute of Environmental Science and Research, Auckland 1025, New Zealand
10 Division of Microbial Ecology, Center for Microbiology and Environmental Systems Science, University of Vienna, Vienna 1030, Austria
11 Plant Pathogen Evolution Research Group, Max Planck Institute for Biology, Tübingen 72076, Germany
Integrative and conjugative elements (ICEs) are self-transmissible mobile elements that transfer functional genetic units across broad phylogenetic distances. Accessory genes shuttled by ICEs can make significant contributions to bacterial fitness. Most ICEs characterized to date encode readily observable phenotypes contributing to symbiosis, pathogenicity, and antimicrobial resistance, yet the majority of ICEs carry genes of unknown function. Recent observations of rapid acquisition of ICEs in a pandemic lineage of Pseudomonas syringae pv. actinidae led to investigation of the structural and functional diversity of these elements. Fifty-three unique ICE types were identified across the P. syringae species complex. Together they form a distinct family of ICEs (PsICEs) that share a distant relationship to ICEs found in Pseudomonas aeruginosa. PsICEs are defined by conserved backbone genes punctuated by an array of accessory cargo genes, are highly recombinogenic, and display distinct evolutionary histories compared to their bacterial hosts. The most common cargo is a recently disseminated 16-kb mobile genetic element designated Tn6212. Deletion of Tn6212 did not alter pathogen growth in planta, but mutants displayed fitness defects when grown on tricarboxylic acid (TCA) cycle intermediates. RNA-seq analysis of a set of nested deletion mutants showed that a Tn6212-encoded LysR regulator has global effects on chromosomal gene expression. We show that Tn6212 responds to preferred carbon sources and manipulates bacterial metabolism to maximize growth.