Plant-microbe interactions, horizontal gene transfer, symbiotic nitrogen fixation, bacterial genetics and genomics
Clive is a microbial geneticist with primary research interests in how microbes and plants recognise each other and develop a nitrogen-fixing symbiosis, and in microbial evolution by horizontal gene transfer and adaptive mutation. He is one of two international partners of the Centre for Carbohydrate Recognition and Signalling based in Denmark and is a Fellow of the Royal Society of New Zealand.
Professor Ronson's research interests are in the areas of the plant-microbe interactions involved in symbiotic nitrogen fixation, and the role of horizontal gene transfer in microbial evolution. The major research area in the lab focuses on genomic analysis of the bacterium Mesorhizobium loti that is the microsymbiont of the model legume Lotus japonicus. In this research, we collaborate with several overseas groups characterizing the plant’s contribution to the symbiosis using L. japonicus. In particular, we are one of two international partners of the Centre for Carbohydrate Recognition and Signalling, a Centre of Research Excellence headquartered in Aarhus, Denmark, and funded by the Danish National Research Foundation. Carbohydrate signals and extracellular polysaccharides play an important role in cell-to-cell communication processes between the host plant and rhizobial microsymbiont and a major aim of our work is to determine the mechanisms by which these signals are perceived.
An important discovery we made was that new field strains of Lotus-nodulating rhizobia evolve in a single step by lateral transfer of a chromosomally-located symbiotic element from an inoculum strain to indigenous non-symbiotic rhizobia. The 502-kb element integrates into a tRNA gene in a process mediated by a phage-related integrase. The transferable element, which we called a symbiosis island, represents a novel class of genetic element with similarities to pathogenicity islands that differentiate bacterial pathogens from benign isolates of the same species. We sequenced the symbiosis island and have characterised the roles of many of the 424 genes that it encodes. The functional genomics approach we are following involves a combination of mutagenesis and expression analysis. One interesting finding was that the rhizobium translocates specific proteins involved in the symbiosis directly into plant cells. A major current focus is on characterizing the mechanism by which the island is transferred, and how the transfer is regulated. This research is providing novel insight into the role of horizontal gene transfer in microbial evolution.
Ramsay, JP, Tester, LG, Major, AS., Sullivan, JT, Edgar, CD, Kleffmann, T., Patterson-House, JR, Hall, DA, Tate, WP, Hynes, MF, and Ronson, CW (2015). Ribosomal frameshifting and dual-target antiactivation restrict quorum-sensing-activated transfer of a mobile genetic element. Proc Natl Acad Sci USA 112: 4104-4109
Ramsay, JP and Ronson, CW. (2015) Genetic Regulation of Symbiosis Island Transfer in Mesorhizobium loti. Chapter 21 in ‘Biological Nitrogen Fixation’ edited by F. J. de Bruijn. John Wiley & Sons. ISBN: 978-1-118-63704-3
Saeki K. and Ronson CW. (2014) Genome Sequence and Gene Functions in Mesorhizobium loti and Relatives. pp. 41 – 58 In The Lotus japonicus Genome. Tabata, S., and Stougaard, J. (Eds.), Springer-Verlag Berlin Heidelberg. ISBN 978-3-662-44269-2
Kelly, S, Sullivan, J, Ronson, C, Tian, R, Bräu, L, Davenport, K, Daligault, H, Erkkila, T, Goodwin, L, Gu, W, Munk, C, Teshima, H, Xu, Y, Chain, P, Woyke, T, Liolios, K, Pati, A, Mavromatis, K, Markowitz, V, Ivanova, N, Kyrpides, N and Reeve, W. (2014). Genome sequence of the Lotus spp. microsymbiont Mesorhizobium loti strain NZP2037. Standards in Genomic Sciences 9:7.
Kelly, S, Sullivan, J, Ronson, C, Tian, R, Bräu, L, Munk, C, Goodwin, L, Han, C, Woyke, T, Reddy, T, Huntemann, M, Pati, A, Mavromatis, K, Markowitz, V, Ivanova, N, Kyrpides, N and Reeve, W. (2014). Genome sequence of the Lotus spp. microsymbiont Mesorhizobium loti strain R7A. Standards in Genomic Sciences 9:6.
Reeve, W, Sullivan, J, Ronson, C, Tian, R, Bräu, L, Davenport, K, Goodwin, L, Chain, P, Woyke, T, Lobos, E, Huntemann, M, Pati, A, Mavromatis, K, Markowitz, V, Ivanova, N, and Kyrpides, N. (2014). Genome sequence of the Lotus corniculatus microsymbiont Mesorhizobium loti strain R88B. Standards in Genomic Sciences 9:3.
Dam S, Dyrlund TF, Ussatjuk A, Jochimsen B, Nielsen K, Goffard N, Ventosa M, Lorentzen A, Gupta V, Andersen SU, Enghild JJ, Ronson CW, Roepstorff P, and Stougaard, J. (2014). Proteome reference maps of the Lotus japonicus nodule and root. Proteomics 14: 230-240.
Maolanon NN, Blaise M, Sørensen KK, Cló E, Sullivan JT, Ronson CW, Stougaard J, Blixt O, Jensen KJ. (2014). Lipochitin oligosaccharides immobilized through oximes in glycan microarrays bind LysM proteins. ChemBioChem, 15:425-34.
Sullivan JT, Brown, SD, Ronson CW. (2013) The NifA-RpoN regulon of Mesorhizobium loti strain R7A and its symbiotic activation by a novel LacI/GalR-family regulator. PLOS ONE 8(1):e53762
Kelly SJ, Muszynski, A., Kawaharada, Y, Hubber, AM, Sullivan, JT, Sandal, N, Carlson, RW, Stougaard, J, Ronson, CW. (2013) Conditional requirement for exopolysaccharide in the Mesorhizobium-Lotus symbiosis. Molecular Plant-Microbe Interactions, 26(3), 319-329
Ramsay JP, Major AS, Komarovsky VM, Sullivan JT, Dy RL, Hynes MF, Salmond GP, Ronson CW. (2013) A widely conserved molecular switch controls quorum sensing and symbiosis island transfer in Mesorhizobium loti through expression of a novel antiactivator. Molecular Microbiology 87(1):1-13
Sheen TR, O'Callaghan M, Smalley DJ, Ronson CW, Hurst MR. (2013) Serratia entomophila bet gene induction and the impact of glycine betaine accumulation on desiccation tolerance. J Appl Microbiol. 114(2):470-81
Broghammer, A., Krusell, L., Blaise, M., Sauer, J., Sullivan, J.T., Maolanon, N., Vinther, M., Lorentzen, A., Madsen, E.B., Jensen, K.J., Roepstorff, P., Thirup, S., Ronson, C.W., Thygesen, M.B., Stougaard., J. (2012). Legume receptors perceive the rhizobial lipochito-oligosaccharide signal molecules by direct binding. Proc. Natl. Acad. Sci. USA, 109: 13859-13864.
Vanga, B.R., Butler, R.C., Toth, I.K., Ronson, C.W., Pitman, A.R. (2012). Inactivation of PbTopo IIIß causes hyper-excision of the Pathogenicity Island HAI2 resulting in reduced virulence of Pectobacterium atrosepticum. Molecular Microbiology 84:648-63.
Madsen, L.H., Tirichine, L., Jurkiewicz, A., Sullivan, J.T., Heckmann, A.B., Bek, A.S., Ronson, C.W., James, E.K., Stougaard, J. (2010). The molecular network governing nodule organogenesis and infection in the model legume, Lotus japonicus. Nature Communications 1:10 DOI: 10.1038/ncomms1009
Noisangiam, R., Nuntagij, A., Pongsilp, N., Boonkerd, N., Denduangboripant, J., Ronson, C., & Teaumroong, N. (2010). Heavy metal tolerant Metalliresistens boonkerdii gen. nov., sp. nov., a new genus in the familyBradyrhizobiaceae isolated from soil in Thailand. Systematic and Applied Microbiology 33, 374-382.
Ramsay JP, Sullivan JT, Jambari N, Ortori CA, Heeb S, Williams P, Barrett DA, Lamont IL, Ronson CW. (2009) A LuxRI-family regulatory system controls excision and transfer of the Mesorhizobium loti strain R7A symbiosis island by activating expression of two conserved hypothetical genes. Molecular Microbiology 73, 1141–1155.
Rodpothong, P., Sullivan, J. T., Songsrirote, K., Sumpton, D., Cheung, K. W. J.-T., Thomas-Oates, J., Radutoiu, S., Stougaard, J. and Ronson, C.W. (2009) Nodulation gene mutants of Mesorhizobium lotiR7A – nodZ and nolL mutants have host-specific phenotypes on Lotus species. Molecular Plant-Microbe Interactions 22, 1546-1554.
Ott T, Sullivan J, James EK, Flemetakis E, Günther C, Gibon Y, Ronson C, Udvardi M. (2009). Absence of symbiotic leghemoglobins alters bacteroid and plant cell differentiation during development ofLotus japonicus root nodules. Mol Plant Microbe Interact. 22, 800-880.
Hubber AM, Sullivan JT, Ronson CW. (2007) Symbiosis-induced cascade regulation of theMesorhizobium loti R7A VirB/D4 type IV secretion system. Mol Plant Microbe Interact. 20, 255-61.
McIntyre HJ, Davies H, Hore TA, Miller SH, Dufour JP, Ronson CW. (2007) Trehalose biosynthesis inRhizobium leguminosarum bv. trifolii and its role in desiccation tolerance. Appl Environ Microbiol. 73, 3984-92.
Miller SH, Elliot RM, Sullivan JT, Ronson CW. (2007) Host-specific regulation of symbiotic nitrogen fixation in Rhizobium leguminosarum biovar trifolii. Microbiology 153, 3184-95.
Carlton TM, Sullivan JT, Stuart GS, Hutt K, Lamont IL, Ronson CW. (2007). Ferrichrome utilization in a mesorhizobial population: microevolution of a three-locus system. Environ Microbiol. 9, 2923-32.
Ramsay, J.P., Sullivan, J.T., Stuart, G.S., Lamont, I.L., and Ronson, C.W. (2006). Excision and transfer of the Mesorhizobium loti R7A symbiosis island requires an integrase IntS, a novel recombination directionality factor RdfS, and a putative relaxase RlxS. Molecular Microbiology 62:723-734.
Dodd, S.J., Hurst, M.R., Glare, T.R., O’Callaghan, M., and Ronson, C.W. (2006). Occurrence of sep insecticidal toxin complex genes in Serratia spp. and Yersinia frederiksenii. Applied and Environmental Microbiology 72:6584-92
Hubber, A., Vergunst, A. C., Sullivan, J. T., Hooykaas, P. J. and Ronson, C. W. (2004). Symbiotic phenotypes and translocated effector proteins of the Mesorhizobium loti strain R7A VirB/D4 type IV secretion system. Molecular Microbiology 54:561-574.
Sullivan, J. T., J. R. Trzebiatowski, R. W. Cruickshank, J. Gouzy, S. D. Brown, R. M. Elliot, D. J. Fleetwood, N. G. McCallum, U. Rossbach, G. S. Stuart, J. E. Weaver, R. J. Webby, F. J. de Bruijn, and C. W. Ronson. (2002). Comparative sequence analysis of the symbiosis island of Mesorhizobium loti strain R7A. Journal of Bacteriology 184:3086-3095.
Sullivan, J. T. & Ronson, C. W. (1998) Evolution of rhizobia by acquisition of a 500- kb symbiosis island that integrates into a phe-tRNA gene. Proceedings of the National Academy of Sciences of the United States of America 95, 5145-5149.
Sullivan, J.T., Patrick, H.N., Lowther, W.L., Scott, D.B., and Ronson, C.W. (1995) Nodulating strains ofRhizobium loti arise through chromosomal symbiotic gene transfer in the environment. Proceedings of the National Academy of Sciences of the United States of America. 92:8985-8989.
Chair in Genetics
Research in the laboratory is supported by grants from the Danish National Research Foundation, the Ministry of Business, Innovation and Employment (MBIE), and the University of Otago.