Comparative genomics of plant-associated Pseudomonas spp.: Insights into diversity and inheritance of traits involved in multitrophic interactions

Authors: Loper, Joyce; HASSAN, KARL - Macquarie University; MAVRODI, DMITRI - Washington State University; Davis, Edward; LIM, CHEE KENT - Macquarie University; Shaffer, Brenda; ELBOURNE, LIAM D - Macquarie University; STOCKWELL, VIRGINIA - Oregon State University; HARTNEY, SIERRA - Oregon State University; BREAKWELL, KATY - Macquarie University; HENKELS, MARCELLA - Retired ARS Employee; TETU, SASHA - Macquarie University; RANGEL, LORENA - Oregon State University; Kidarsa, Teresa; WILSON, NEIL - Macquarie University; VAN MORTEL, JUDITH - Wageningen University; SONG, CHUNXU - Wageningen University; BLUMHAGEN, RACHEL - Former ARS Employee; RADUNE, DIANA - J Craig Venter Institute; HOSTETLER, JESSICA - J Craig Venter Institute; BRINKAC, LAUREN - J Craig Venter Institute; DURKIN, A SCOTT - J Craig Venter Institute; Kluepfel, Daniel; Wechter, William - Pat; ANDERSON, ANNE - Utah State University; KIM, YOUNG CHEOL - Chonnam National University; PIERSON III, LELAND - Texas A&M University; PIERSON, ELIZABETH - Texas A&M University; LINDOW, STEVEN - University Of California; RAAIJMAKERS, JOS - Wageningen University; Weller, David; Thomashow, Linda; ALLEN, ANDREW - J Craig Venter Institute; PAULSEN, IAN - Macquarie University

Submitted to: PLoS Genetics
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 5/10/2012
Publication Date: 7/5/2012
Citation: Loper, J.E., Hassan, K.A., Mavrodi, D., Davis, E.W., Lim, C., Shaffer, B.T., Elbourne, L.H., Stockwell, V.O., Hartney, S.L., Breakwell, K., Henkels, M.D., Tetu, S.G., Rangel, L.I., Kidarsa, T.A., Wilson, N.L., Van Mortel, J., Song, C., Blumhagen, R., Radune, D., Hostetler, J.B., Brinkac, L.M., Durkin, A., Kluepfel, D.A., Wechter, W.P., Anderson, A.J., Kim, Y., Pierson Iii, L.S., Pierson, E.A., Lindow, S.E., Raaijmakers, J.M., Weller, D.M., Thomashow, L.S., Allen, A.E., Paulsen, I.I. 2012. Comparative genomics of plant-associated Pseudomonas spp.: Insights into diversity and inheritance of traits involved in multitrophic interactions. PLoS Genetics. 8(7):e1002784.

Interpretive Summary: Pseudomonas fluorescens is a well-recognized group of bacteria that are ubiquitous in the environment, including water, soil, and plant surfaces. Because of their diversity, these bacteria are referred to as the Pseudomonas fluorescens group, rather than a species. Members of this group have the capacity to function in the biological control of plant disease, and they have been a focus of research in the field of biological control. In this study, we sequenced the genomes of seven strains within the Pseudomonas fluorescens group and compared them to three previously-sequenced genomes. This comparison of ten genomes reinforced our concepts of the diversity of this group of bacteria, as the ten strains shared less than 40% of their genes. Furthermore, each of the ten strains has several hundred genes that are unique to itself. Almost all of the genes that contribute to biological control of plant diseases map to genomic regions present in only a subset of the strains or unique to a specific strain. From these regions, we identified several gene clusters that are likely to encode the biosynthesis of new compounds with antibiotic properties. The results of this study highlight the enormous heterogeneity of the Pseudomonas genus and the importance of the variable genome in tailoring individual strains to specific functions, such as biological control of plant disease.

Technical Abstract: We provide here a comparative genome analysis of the Pseudomonas fluorescens group, including seven new genomic sequences for plant-associated strains. These strains exhibit a diverse spectrum of traits involved in biological control and other multitrophic interactions with plants, microbes, and insects. Multilocus sequence analysis placed the strains in three sub-clades, which was reinforced by high levels of synteny, size of core genomes, and relatedness of orthologous genes between strains within a subclade. The heterogeneity of the P. fluorescens group was reflected in the large size of its pan-genome (13,872 genes), which makes up approximately 54% of the pan-genome of the genus as a whole. The core genome, at 1491 genes, represents only 24-36% of any individual genome. We discovered genes for traits that were not known previously to exist within the strains, including genes for the biosynthesis of the siderophores achromobactin and pseudomonine and the antibiotic 2-hexyl-5-propylalkylresorcinol; novel bacteriocins; type II, III and VI secretion systems; and insect toxins. Certain gene clusters, such as those for type III secretion systems, are present only in specific sub-clades, suggesting vertical inheritance. Almost all of the genes associated with multitrophic interactions map to genomic regions present in only a subset of the strains or unique to a specific strain. To explore the evolutionary origin of these genes, we mapped their distributions relative to the locations of mobile genetic elements and repetitive extragenic palindromic (REP) elements in each genome. The mobile genetic elements and many strain-specific loci fall into regions devoid of REP elements (i.e., REP deserts) and regions displaying atypical tri-nucleotide composition, possibly indicating relatively recent acquisition of these loci. Collectively, the results of this study highlight the enormous heterogeneity of the Pseudomonas genus and the importance of the variable genome in tailoring individual strains to their specific lifestyles and functional repertoire.