Comparative Analyses Of Xanthomonas And Xylella Complete Genomes

Computational analyses of four bacterial genomes of the Xanthomonadaceae family reveal new unique genes that may be involved in adaptation, pathogenicity, and host specificity. The Xanthomonas genus presents 3636 unique genes distributed in 1470 families, while Xylella genus presents 1026 unique genes distributed in 375 families. Among Xanthomonas-specific genes, we highlight a large number of cell wall degrading enzymes, proteases, and iron receptors, a set of energy metabolism genes, second copy of the type II secretion system, type III secretion system, flagella and chemotactic machinery, and the xanthomonadin synthesis gene cluster. Important genes unique to the Xylella genus are an additional copy of a type IV pili gene cluster and the complete machinery of colicin V synthesis and secretion. Intersections of gene sets from both genera reveal a cluster of genes homologous to Salmonella's SPI-7 island in Xanthomonas axonopodis pv citri and Xylella fastidiosa 9a5c, which might be involved in host specificity. Each genome also presents important unique genes, such as an HMS cluster, the kdgT gene, and O-antigen in Xanthomonas axonopodis pv citri; a number of avrBS genes and a distinct O-antigen in Xanthomonas campestris pv campestris, a type I restriction- modification system and a nickase gene in Xylella fastidiosa 9a5c, and a type II restriction-modification system and two genes related to peptidoglycan biosynthesis in Xylella fastidiosa temecula 1. All these differences imply a considerable number of gene gains and losses during the divergence of the four lineages, and are associated with structural genome modifications that may have a direct relation with the mode of transmission, adaptation to specific environments and pathogenicity of each organism.914376Adachi, J., Hasegawa, M., (1996) MOLPHY Version 2.3: Programs for Molecular Phylogenetics Based on Maximum Likelihood, , J. Adachi, ed. (Institute of Statistical Mathematics, Tokyo)Almra, Mattick, J.S., Genes involved in the biogenesis and function of type-4 fimbriae in Pseudomonas aeruginosa (1997) Gene, 192, pp. 89-98Almeida, R.P., Mann, R., Purcell, A.H., Xylella fastidiosa cultivation on a minimal solid defined medium (2004) Curr Microbiol, 48, pp. 368-372Almeida, R.P., Purcell, A.H., Biological traits of Xylella fastidiosa strains from grapes and almonds (2003) Appl Environ Microbiol, 69, pp. 7447-7452Altschul, S.F., Madden, T.L., Schaffer, A.A., Gapped BLAST and PSI-BLAST: A new generation of protein database search programs (1997) Nucleic Acids Res, 25, pp. 3389-3402Apweiler, R., Attwood, T.K., Bairoch, A., InterPro: An integrated documentation resource for protein families, domains and functional sites (2000) Bioinformatics, 16, pp. 1145-1150Apweiler, R., Bairoch, A., Wu, C.H., UniProt: The Universal Protein knowledgebase (2004) Nucleic Acids Res, 32, pp. D115-D119Araujo, W.L., Marcon, J., Maccheroni Jr., W., Diversity of endophytic bacterial populations and their interaction with Xylella fastidiosa in citrus plants (2002) Appl Environ Microbiol, 68, pp. 4906-4914Barber, C.E., Tang, J.L., Feng, J.X., A novel regulatory system required for pathogenicity of Xanthomonas campestris is mediated by a small diffusible signal molecule (1997) Mol Microbiol, 24, pp. 555-566Bhattacharyya, A., Stilwagen, S., Ivanova, N., Whole-genome comparative analysis of three phytopathogenic Xylella fastidiosa strains (2002) Proc Natl Acad Sci USA, 99, pp. 12403-12408Bhattacharyya, A., Stilwagen, S., Reznik, G., Draft sequencing and comparative genomics of Xylella fastidiosa strains reveal novel biological insights (2002) Genome Res, 12, pp. 1556-1563Bradley, D.E., Shortening of Pseudomonas aeruginosa pili after RNA-phage adsorption (1972) J Gen Microbiol, 72, pp. 303-319Bradley, D.E., The adsorption of Pseudomonas aeruginosa pilus-dependent bacteriophages to a host mutant with nonretractile pili (1974) Virology, 58, pp. 149-163Braun, V., Braun, M., Iron transport and signaling in Escherichia coll (2002) FEBS Lett, 529, pp. 78-85Braun, V., Hancock, R.E., Hantke, K., Functional organization of the outer membrane of Escherichia coli: Phage and colicin receptors as components of iron uptake systems (1976) J Supramol Struct, 5, pp. 37-58Buyer, J.S., Leong, J., Iron transport-mediated antagonism between plant growth-promoting and plant-deleterious Pseudomonas strains (1986) J Biol Chem, 261, pp. 791-794Campbell, A., Prophage insertion sites (2003) Res Microbiol, 154, pp. 277-282Castresana, J., Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis (2000) Mol Biol Evol, 17, pp. 540-552Chang, C.J., Donaldson, R.C., Nutritional requirements of Xylella fastidiosa, which causes Pierce's disease in grapes (2000) Can J Microbiol, 46, pp. 291-293Chang, C.J., Garner, M., Zreik, L., Culture and serological detection of the xylem-limited bacterium causing citrus variegated chlorosis and identification as a strain of Xylella fastidiosa (1993) Curr Microbiol, 27, pp. 137-142Collmer, A., Badel, J.L., Charkowski, A.O., Pseudomonas syringae Hrp type III secretion system and effector proteins (2000) Proc Natl Acad Sci USA, 97, pp. 8770-8777Cornelis, P., Matthijs, S., Diversity of siderophore-mediated iron uptake systems in fluorescent pseudomonads: Not only pyoverdines (2002) Environ Microbiol, 4, pp. 787-798Crow, J.F., Kimura, M., (1970) An Introduction to Population Genetics Theory, , Harper and Row, New YorkSilva, D.A., Ferro, A.C., Reinach, J.A., Comparison of the genomes of two Xanthomonas pathogens with differing host specificities (2002) Nature, 417, pp. 459-463Silva, D.A., Vettore, F.R., Kemper, A.L., Fastidian gum: The Xylellafastidiosa exopolysaccharide possibly involved in bacterial pathogenicity (2001) FEMS Microbiol Lett, 203, pp. 165-171Daubin, V., Ochman, H., Start-up entities in the origin of new genes (2004) Curr Opin Genet Dev, 14, pp. 616-619Delver, E.P., Kotova, V.U., Zavilgelsky, G.B., Nucleotide sequence of the gene (ard) encoding the antirestriction protein of plasmid colIb-P9 (1991) J Bacteriol, 173, pp. 5887-5892Digiampietrl, L.A., Medeiros, C.B., Setubal, J.C., A data model for comparative genomics (2003) Rev Tecnol Inform, 3, pp. 35-40Dow, J.M., Feng, J.X., Barber, C.E., Novel genes involved in the regulation of pathogenicity factor production within the rpf gene cluster of Xanthomonas campestris (2000) Microbiology, 146, pp. 885-891Fath, M.J., Mahanty, H.K., Kolter, R., Characterization of a purF operon mutation which affects colicin V production (1989) J Bacteriol, 171, pp. 3158-3161Gelfand, M.S., Koonin, E.V., Avoidance of palindromic words in bacterial and archaeal genomes: A close connection with restriction enzymes (1997) Nucleic Acids Res, 25, pp. 2430-2439Gobert, A.P., Cheng, Y., Wang, J.Y., Helicobacter pylori induces macrophage apoptosis by activation of arginase II (2002) J Immunol, 168, pp. 4692-4700Gobert, A.P., Mcgee, D.J., Akhtar, M., Helicobacter pylori arginase inhibits nitric oxide production by eukaryotic cells: A strategy for bacterial survival (2001) Proc Natl Acad Sci USA, 98, pp. 13844-13849Goel, A.K., Rajagopal, L., Nagesh, N., Genetic locus encoding functions involved in biosynthesis and outer membrane localization of xanthomonadin in Xanthomonas oryzae pv. oryzae (2002) J Bacteriol, 184, pp. 3539-3548Gomez, P., Ribas-Aparicio, R.M., Pelaez, A.I., Isolation and nucleotide sequence of the gene encoding the Xaml DNA methyltransferase of Xanthomonas campestris pv. amaranthicola (1997) Biochim Biophys Acta, 1351, pp. 261-266Gottwald, T., Graham, J., Bacteria diseases (2000) Compendium of Citrus Diseases, , L. W. Timmer, S.M. Garnsey, and J.H. Graham, eds. (APS Press, St. Paul)Graham, J.H., Gottwald, T.R., Cubero, J., Xanthomonas axonopodis pv. citri: Factors affecting successful eradiction of citrus canker (2004) Mol Plant Pathol, 5, pp. 1-15Heidelberg, J.F., Eisen, J.A., Nelson, W.C., DNA sequence of both chromosomes of the cholera pathogen Vibrio cholerae (2000) Nature, 406, pp. 477-483Hendricks, E.C., Szerlong, H., Hill, T., Cell division, guillotining of dimer chromosomes and SOS induction in resolution mutants (dif, xerC and xerD) of Escherichia coli (2000) Mol Microbiol, 36, pp. 973-981Hendson, M., Purcell, A.H., Chen, D., Genetic diversity of Pierce's disease strains and other pathotypes of Xylella fastidiosa (2001) Appl Environ Microbiol, 67, pp. 895-903Holt, J.G., (1994) Xylella. Bergey's Manual of Determinative Bacteriology, 9th Ed., pp. 100-115. , J.G. Holt, ed. (Williams and Wilkins, London)Hopkins, D.L., Xylella fastidiosa: Xylem-limited bacaterial pathogen of plants (1989) Annu Rev Phytopathol, 27, pp. 271-290Housby, J.N., Thomas, J.D., Wharam, S.D., Conditional mutations in OutE and OutL block exoenzyme secretion across the Erwinia carotovora outer membrane (1998) FEMS Microbiol Lett, 165, pp. 91-102Hung, C.H., Yang, C.F., Yang, C.Y., Involvement of tonB-exbBD1D2 operon in infection of Xanthomonas campestris nhaee phi L7 (2003) Biochem and Biophys Res Commun, 302, pp. 878-884Jenkins, C.L., Starr, M.P., Formation of halogenated aryl-polyene (xanthomonadin) pigments by the type and other yellow-pigmented strains of Xanthomonas maltophilia (1985) Ann l'Institut Pasteur Microbiol, 136 B, pp. 257-264Kanehisa, M., Goto, S., Kawashima, S., The KEGG resource for deciphering the genome (2004) Nucleic Acids Res, 32, pp. D277-D280Karlin, S., Detecting anomalous gene clusters and pathogenicity islands in diverse bacterial genomes (2001) Trends Microbiol, 9, pp. 335-343Kelly, M.J., Poole, R.K., Yates, M.G., Cloning and mutagenesis of genes encoding the cytochrome bd terminal oxidase complex in Azotobacter vinelandii: Mutants deficient in the cytochrome d complex are unable to fix nitrogen in air (1990) J Bacteriol, 172, pp. 6010-6019Khalil-Rizvi, S., Toth, S.I., Van Der Helm, D., Structures and characteristics of novel siderophores from plant deleterious Pseudomonas fluorescens A225 and Pseudomonas putida ATCC 39167 (1997) Biochemistry, 36, pp. 4163-4171Koide, T., Zaini, P.A., Moreira, L.M., DNA microarray-based genome comparison of a pathogenic and a nonpathogenic strain of Xylella fastidiosa delineates genes important for bacterial virulence (2004) J Bacteriol, 186, pp. 5442-5449Koster, M., Ovaa, W., Bitter, W., Multiple outer membrane receptors for uptake of ferric pseudobactins in Pseudomonas putida WCS358 (1995) Mol Gen Genet, 248, pp. 735-743Lacava, P.T., Araujo, W.L., Marcon, J., Interaction between endophytic bacteria from citrus plants and the phytopathogenic bacteria Xylella fastidiosa, causal agent of citrus-variegated chlorosis (2004) Lett Appl Microbiol, 39, pp. 55-59Lazdunski, C.J., Bouveret, E., Rigal, A., Colicin import into Escherichia coli cells (1998) J Bacteriol, 180, pp. 4993-5002Lee, H.M., Chen, J.R., Lee, H.L., Functional dissection of the XpsN (GspC) protein of the Xanthomonas campestris pv. campestris type II secretion machinery (2004) J Bacteriol, 186, pp. 2946-2955Lee, H.M., Wang, K.C., Liu, Y.L., Association of the cytoplasmic membrane protein XpsN with the outer membrane protein XpsD in the type II protein secretion apparatus of Xanthomonas campestris pv. campestris (2000) J Bacteriol, 182, pp. 1549-1557Lee, R.F.E.A., Beretta, M.J.G., Hartung, J.H., Citrus variegated chlorosis: Confirmation of a Xylella fastidiosa as the causal agent (1993) Summa Phytopathol, pp. 123-125. , 19.2Leite, B., Andersen, P.C., Ishida, M.L., Colony aggregation and biofilm formation in xylem chemistry-based media for Xylella fastidiosa (2004) FEMS Microbiol Lett, 230, pp. 283-290Lerat, E., Daubin, V., Moran, N.A., From gene trees to organismal phylogeny in prokaryotes: The case of the gamma-Proteobacteria (2003) PLoS Biol, 1, pp. E19Lima, W.C., Paquola, A.C.M., Van Sluys, M.-A., Non-gamma proteobacteria gene islands contribution to Xanthomonas genome (2005) OMICS, , this issueLin, R.J., Capage, M., Hill, C.W., A repetitive DNA sequence, rhs, responsible for duplications within the Escherichia coli K-12 chromosome (1984) J Mol Biol, 177, pp. 1-18Lobry, J.R., Asymmetric substitution patterns in the two DNA strands of bacteria (1996) Mol Biol Evol, 13, pp. 660-665Long, S.R., Staskawicz, B.J., Prokaryotic plant parasites (1993) Cell, 73, pp. 921-935Lopes, J.R.S., Beretta, M.J.G., Harakava, R., Confirmação da transmissão por cigarrinhas do agente causal da clorose variegada dos citros, Xylella fastidiosa (1996) Fitopatol Brasil, 21 (SUPPL.), p. 343Lopez, N.I., Haedo, A.S., Mendez, B.S., Evaluation of Xanthomonas campestris survival in a soil microcosm system (1999) Int Microbiol, 2, pp. 111-114Minet, A.D., Chiquet-Ehrismann, R., Phylogenetic analysis of teneurin genes and comparison to the rearrangement hot spot elements of E. coli (2000) Gene, 257, pp. 87-97Moreira, L.M., De Souza, R.F., Almeida, N.F., Comparative genomics analyses of citrus-associated bacteria (2004) Annu Rev Phytopathol, 42, pp. 163-184Noel, L., Thieme, F., Gabler, J., XopC and XopJ, two novel type III effector proteins from Xanthomonas campestris pv. vesicatoria (2003) J Bacteriol, 185, pp. 7092-7102Nunes, L.R., Rosato, Y.B., Muto, N.H., Microarray analyses of Xylella fastidiosa provide evidence of coordinated transcription control of laterally transferred elements (2003) Genome Res, 13, pp. 570-578Page, R.D., Charleston, M.A., From gene to organismal phylogeny: Reconciled trees and the gene tree/species tree problem (1997) Mol Phylogenet Evol, 7, pp. 231-240Pashalidis, S., Moreira, L.M., Zaini, P.A., Whole-genome expression profiling of Xylella fastidiosa in response to growth on glucose (2005) OMICS, , this issuePendrak, M.L., Perry, R.D., Characterization of a hemin-storage locus of Yersinia pestis (1991) Biol Met, 4, pp. 41-47Plckard, D., Wain, J., Baker, S., Composition, acquisition, and distribution of the Vi exopolysaccharide- encoding Salmonella enterica pathogenicity island SPI-7 (2003) J Bacteriol, 185, pp. 5055-5065Poplawsky, A.R., Chun, W., pigB determines a diffusible factor needed for extracellular polysaccharide slime and xanthomonadin production in Xanthomonas campestris pv. campestris (1997) J Bacteriol, 179, pp. 439-444Poplawsky, A.R., Urban, S.C., Chun, W., Biological role of xanthomonadin pigments in Xanthomonas campestris pv. campestris (2000) Appl Environ Microbiol, 66, pp. 5123-5127Purcell, A.H., Almond leaf scorch: Leafhooper and spittle bug vectors (1980) J Econ Entomol, 73, pp. 834-838Rajagopal, L., Sundari, C.S., Balasubramanian, D., The bacterial pigment xanthomonadin offers protection against photodamage (1997) FEBS Lett, 415, pp. 125-128Rossetti, V., Garnier, M., Bové, J.M., Presence de bacteries dans le xyleme d'oranges atteints de chlorose variegee, une nouvelle maladie des agrumes au Bresil (1990) CRAcad Paris, 310, pp. 345-349Scarpari, L.M., Lambais, M.R., Silva, D.S., Expression of putative pathogenicity-related genes in Xylella fastidiosa grown at low and high cell density conditions in vitro (2003) FEMS Microbiol Lett, 222, pp. 83-92Schaad, N.W., Alvarez, A., Xanthomonas campestris pv. campestris: Cause of black rot of crucifers (1993) Xanthomonas, 1st Ed., pp. 51-53. , J.G. Swings and E.L. Civerolo, eds. London: Chapman & HallSchaad, N.W., Postnikova, E., Lacy, G., Xylella fastidiosa subspecies: X. fastidiosa subsp piercei, subsp. nov., and X. fastidiosa subsp. multiplex subsp. nov., and X. fastidiosa subsp. pauca subsp. nov (2004) Syst Appl Microbiol, 27, pp. 290-300Schubert, S., Rakln, A., Karch, H., Prevalence of the "high-pathogenicity island" of Yersinia species among Escherichia coli strains that are pathogenic to humans (1998) Infect Immun, 66, pp. 480-485Sekizaki, T., Otani, Y., Osaki, M., Evidence for horizontal transfer of SsuDAT1I restriction-modification genes to the Streptococcus suis genome (2001) J Bacteriol, 183, pp. 500-511Sharp, P.M., Kelleher, J.E., Daniel, A.S., Roles of selection and recombination in the evolution of type I restriction-modification systems in enterobacteria (1992) Proc Natl Acad Sci USA, 89, pp. 9836-9840Simpson, A.J., Reinach, F.C., Arruda, P., The genome sequence of the plant pathogen Xylella fastidiosa (2000) Nature, 406, pp. 151-157. , The Xylella fastidiosa Consortium of the Organization for Nucleotide Sequencing and AnalysisSivonen, K., Namikoshi, M., Evans, W.R., Three new microcystins, cyclic heptapeptide hepatotoxins, from Nostoc sp. strain 152 (1992) Chem Res Toxicol, 5, pp. 464-469Starr, M.P., Jenkins, C.L., Bussey, L.B., Chemotaxonomic significance of the xanthomonadins, novel brominated aryl-polyene pigments produced by bacteria of the genus Xanthomonas (1977) Arch Microbiol, 113, pp. 1-9Steinmann, D., Koplin, R., Puhler, A., Xanthomonas campestris pv. campestris 1psI and 1psJ genes encoding putative proteins with sequence similarity to the alpha- and beta-subunits of 3-oxoacid CoA-transferases are involved in LPS biosynthesis (1997) Arch Microbiol, 168, pp. 441-447Stock, J., Surette, M., Bacterial chemotaxis. The motor connection (1994) Curr Biol, 4, pp. 143-144Stock, J., Surette, M., Park, P., Chemosensing and signal transduction in bacteria (1994) Curr Opin Neurobiol, 4, pp. 474-480Stock, J.B., Surette, M.G., Mccleary, W.R., Signal transduction in bacterial chemotaxis (1992) J Biol Chem, 267, pp. 19753-19756Strom, M.S., Lory, S., Structure-function and biogenesis of the type IV pili (1993) Annu Rev Microbiol, 47, pp. 565-596Swings, J.G., Civerolo, E.L., (1993) Xanthomonas, 1st Ed., , Chapman & Hall, LondonTang, J.L., Liu, Y.N., Barber, C.E., Genetic and molecular analysis of a cluster of rpf genes involved in positive regulation of synthesis of extracellular enzymes and polysaccharide in Xanthomonas campestris pathovar campestris (1991) Mol Gen Genet, 226, pp. 409-417Tatusov, R.L., Natale, D.A., Garkavtsev, I.V., The COG database: New developments in phylogenetic classification of proteins from complete genomes (2001) Nucleic Acids Res, 29, pp. 22-28Thomas, J.D., Reeves, P.J., Salmond, G.P., The general secretion pathway of Erwinia carotovora subsp. carotovora: Analysis of the membrane topology of OutC and OutF (1997) Microbiology, 143, pp. 713-720Thompson, J.D., Higgins, D.G., Gibson, T.J., CLUSTAL W: Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice (1994) Nucleic Acids Res, 22, pp. 4673-4680Van Sluys, M.A., De Oliveira, M.C., Monteiro-Vitorello, C.B., Comparative analyses of the complete genome sequences of Pierce's disease and citrus variegated chlorosis strains of Xylella fastidiosa (2003) J Bacteriol, 185, pp. 1018-1026Van Sluys, M.A., Monteiro-Vitorello, C.B., Camargo, L.E., Comparative genomic analysis of plant-associated bacteria (2002) Annu Rev Phytopathol, 40, pp. 169-189Vojnov, A.A., Slater, H., Newman, M.A., Regulation of the synthesis of cyclic glucan in Xanthomonas campestris by a diffusible signal molecule (2001) Arch Microbiol, 176, pp. 415-420Vorholter, F.J., Niehaus, K., Puhler, A., Lipopolysaccharide biosynthesis in Xanthomonas campestris pv. campestris: A cluster of 15 genes is involved in the biosynthesis of the LPS O-antigen and the LPS core (2001) Mol Genet Genomics, 266, pp. 79-95Waters, V.L., Crosa, J.H., Colicin V virulence plasmids (1991) Microbiol Rev, 55, pp. 437-450Wells, J.M., Raju, B.C., Hung, H.Y., Xylella fastidiosa gen. nov., sp. nov.: Gram-negative, xylem-limited, fastidious plant bacteria related to Xanthomonas spp (1987) Int J Syst Bacteriol, 37, pp. 136-143Wells, J.M., Raju, B.C., Thompson, J.M., Etiology of phony peach and plum leaf scald diseases (1981) Phytopathology, 71, pp. 1156-1161Wiggerich, H.G., Klauke, B., Koplin, R., Unusual structure of the tonB-exb DNA region of Xanthomonas campestris pv. campestris: tonB, exbB, and exbD1 are essential for ferric iron uptake, but exbD2 is not (1997) J Bacteriol, 179, pp. 7103-7110Wiggerich, H.G., Puhler, A., The exbD2 gene as well as the iron-uptake genes tonB, exbB and exbD1 of Xanthomonas campestris pv. campestris are essential for the induction of a hypersensitive response on pepper (Capsicum annuum) (2000) Microbiology, 146, pp. 1053-1060Williams, K.P., Integration sites for genetic elements in prokaryotic tRNA and tmRNA genes: Sublocation preference of integrase subfamilies (2002) Nucleic Acids Res, 30, pp. 866-875Woolfit, M., Bromham, L., Increased rates of sequence evolution in endosymbiotic bacteria and fungi with small effective population sizes (2003) Mol Biol Evol, 20, pp. 1545-155