Ecological genomics in Xanthomonas: the nature of genetic adaptation with homologous recombination and host shifts
详细信息    查看全文
  • 作者:Chao-Li Huang (1)
    Pei-Hua Pu (1)
    Hao-Jen Huang (1)
    Huang-Mo Sung (1)
    Hung-Jiun Liaw (1)
    Yi-Min Chen (2)
    Chien-Ming Chen (3)
    Ming-Ban Huang (1)
    Naoki Osada (4)
    Takashi Gojobori (1) (4) (5)
    Tun-Wen Pai (3)
    Yu-Tin Chen (1)
    Chi-Chuan Hwang (6)
    Tzen-Yuh Chiang (1)

    1. Department of Life Sciences
    ; National Cheng Kung University ; Tainan ; 701 ; Taiwan
    2. Institute of Biotechnology
    ; National Cheng Kung University ; Tainan ; 701 ; Taiwan
    3. Department of Computer Science and Engineering
    ; National Taiwan Ocean University ; Keelung ; 202 ; Taiwan
    4. National Institute of Genetics
    ; Mishima ; Shizuoka ; 411-8540 ; Yata ; Japan
    5. Computational Bioscience Research Center
    ; Biological and Environmental Sciences and Engineering Division ; King Abdullah University of Science and Technology ; Thuwal ; 23955-6900 ; Kingdom of Saudi Arabia
    6. Department of Engineering Science and Supercomputing Research Center
    ; National Cheng Kung University ; Tainan ; 701 ; Taiwan
  • 关键词:Xanthomonas ; Adaptive diversification ; Host shift ; Parapatric speciation ; Homologous recombination ; Comparative genomics
  • 刊名:BMC Genomics
  • 出版年:2015
  • 出版时间:December 2015
  • 年:2015
  • 卷:16
  • 期:1
  • 全文大小:1,499 KB
  • 参考文献:1. Cadillo-Quiroz, H, Didelot, X, Held, NL, Herrera, A, Darling, A, Reno, ML (2012) Patterns of gene flow define species of thermophilic Archaea. PLoS Biol 10: pp. e1001265 CrossRef
    2. Kopac, S, Wang, Z, Wiedenbeck, J, Sherry, J, Wu, M, Cohan, FM (2014) Genomic heterogeneity and ecological speciation within one subspecies of Bacillus subtilis. Appl Environ Microbiol 80: pp. 4842-53 CrossRef
    3. Vos, M (2011) A species concept for bacteria based on adaptive divergence. Trends Microbiol 19: pp. 1-7 CrossRef
    4. Oakley, BB, Carbonero, F, Gast, CJ, Hawkins, RJ, Purdy, KJ (2010) Evolutionary divergence and biogeography of sympatric niche-differentiated bacterial populations. ISME J 4: pp. 488-97 CrossRef
    5. Sikorski, J, Nevo, E (2005) Adaptation and incipient sympatric speciation of Bacillus simplex under microclimatic contrast at 鈥淓volution Canyons鈥?I and II, Israel. Proc Natl Acad Sci U S A 102: pp. 15924-9 CrossRef
    6. Cohan, FM, Koeppel, AF (2008) The origins of ecological diversity in prokaryotes. Curr Biol 18: pp. R1024-34 CrossRef
    7. Vos, M, Didelot, X (2008) A comparison of homologous recombination rates in bacteria and archaea. ISME J 3: pp. 199-208 CrossRef
    8. Luo, C, Walk, ST, Gordon, DM, Feldgarden, M, Tiedje, JM, Konstantinidis, KT (2011) Genome sequencing of environmental Escherichia coli expands understanding of the ecology and speciation of the model bacterial species. Proc Natl Acad Sci U S A 108: pp. 7200-5 CrossRef
    9. Cohan, FM (1994) Genetic exchange and evolutionary divergence in prokaryotes. Trends Ecol Evol 9: pp. 175-80 CrossRef
    10. Nogueira, T, Rankin, DJ, Touchon, M, Taddei, F, Brown, SP, Rocha, EP (2009) Horizontal gene transfer of the secretome drives the evolution of bacterial cooperation and virulence. Curr Biol 19: pp. 1683-91 CrossRef
    11. Wiedenbeck, J, Cohan, FM (2011) Origins of bacterial diversity through horizontal genetic transfer and adaptation to new ecological niches. FEMS Microbiol Rev 35: pp. 957-76 CrossRef
    12. Vauterin, L, Hoste, B, Kersters, K, Swings, J (1995) Reclassification of xanthomonas. Int J Syst Bacteriol 45: pp. 472-89 CrossRef
    13. Dye, D, Bradbury, J, Goto, M, Hayward, A, Lelliott, R, Schroth, MN (1980) International standards for naming pathovars of phytopathogenic bacteria and a list of pathovar names and pathotype strains. Rev Plant Pathol 59: pp. 153-68
    14. Siciliano, F, Torres, P, Send铆n, L, Bermejo, C, Filippone, P, Vellice, G (2006) Analysis of the molecular basis of Xanthomonas axonopodis pv. citri pathogenesis in Citrus limon. Electron J Biotechnol 9: pp. 200-4 CrossRef
    15. Gagnevin, L, Pruvost, O (2001) Epidemiology and control of mango bacterial black spot. Plant Dis 85: pp. 928-35 CrossRef
    16. Mhedbi-Hajri, N, Hajri, A, Boureau, T, Darrasse, A, Durand, K, Brin, C (2013) Evolutionary history of the plant pathogenic bacterium Xanthomonas axonopodis. PLoS One 8: pp. e58474 CrossRef
    17. Bogdanove, AJ, Koebnik, R, Lu, H, Furutani, A, Angiuoli, SV, Patil, PB (2011) Two new complete genome sequences offer insight into host and tissue specificity of plant pathogenic Xanthomonas spp. J Bacteriol 193: pp. 5450-64 CrossRef
    18. Huang, C-L, Ho, C-W, Chiang, Y-C, Shigemoto, Y, Hsu, T-W, Hwang, C-C (2014) Adaptive divergence with gene flow in incipient speciation of Miscanthus floridulus/sinensis complex (Poaceae). Plant J 80: pp. 834-47 CrossRef
    19. Schmidt, H, Greshake, B, Feldmeyer, B, Hankeln, T, Pfenninger, M (2013) Genomic basis of ecological niche divergence among cryptic sister species of non-biting midges. BMC Genomics 14: pp. 384 CrossRef
    20. Lu, H, Patil, P, Sluys, M-A, White, FF, Ryan, RP, Dow, JM (2008) Acquisition and evolution of plant pathogenesis鈥揳ssociated gene clusters and candidate determinants of tissue-specificity in Xanthomonas. PLoS One 3: pp. e3828 CrossRef
    21. Silva, AR, Ferro, JA, Reinach, F, Farah, C, Furlan, L, Quaggio, R (2002) Comparison of the genomes of two Xanthomonas pathogens with differing host specificities. Nature 417: pp. 459-63 CrossRef
    22. Qian, W, Jia, Y, Ren, S-X, He, Y-Q, Feng, J-X, Lu, L-F (2005) Comparative and functional genomic analyses of the pathogenicity of phytopathogen Xanthomonas campestris pv. campestris. Genome Res 15: pp. 757-67 CrossRef
    23. Vorh枚lter, F-J, Schneiker, S, Goesmann, A, Krause, L, Bekel, T, Kaiser, O (2008) The genome of Xanthomonas campestris pv. campestris B100 and its use for the reconstruction of metabolic pathways involved in xanthan biosynthesis. J Biotechnol 134: pp. 33-45 CrossRef
    24. Thieme, F, Koebnik, R, Bekel, T, Berger, C, Boch, J, B眉ttner, D (2005) Insights into genome plasticity and pathogenicity of the plant pathogenic bacterium Xanthomonas campestris pv. vesicatoria revealed by the complete genome sequence. J Bacteriol 187: pp. 7254-66 CrossRef
    25. Jalan, N, Aritua, V, Kumar, D, Yu, F, Jones, JB, Graham, JH (2011) Comparative genomic analysis of xanthomonas axonopodis pv. citrumelo f1, which causes citrus bacterial spot disease, and related strains provides insights into virulence and host specificity. J Bacteriol 193: pp. 6342-57 CrossRef
    26. Pieretti, I, Royer, M, Barbe, V, Carrere, S, Koebnik, R, Cociancich, S (2009) The complete genome sequence of Xanthomonas albilineans provides new insights into the reductive genome evolution of the xylem-limited Xanthomonadaceae. BMC Genomics 10: pp. 616 CrossRef
    27. Ochiai, H, Inoue, Y, Takeya, M, Sasaki, A, Kaku, H (2005) Genome sequence of Xanthomonas oryzae pv. oryzae suggests contribution of large numbers of effector genes and insertion sequences to its race diversity. JARQ-Jpn Agr Res Q 39: pp. 275 CrossRef
    28. Lee, B-M, Park, Y-J, Park, D-S, Kang, H-W, Kim, J-G, Song, E-S (2005) The genome sequence of Xanthomonas oryzae pathovar oryzae KACC10331, the bacterial blight pathogen of rice. Nucleic Acids Res 33: pp. 577-86 CrossRef
    29. Salzberg, SL, Sommer, DD, Schatz, MC, Phillippy, AM, Rabinowicz, PD, Tsuge, S (2008) Genome sequence and rapid evolution of the rice pathogen Xanthomonas oryzae pv. oryzae PXO99A. BMC Genomics 9: pp. 204 CrossRef
    30. Fleischmann, RD, Adams, MD, White, O, Clayton, RA, Kirkness, EF, Kerlavage, AR (1995) Whole-genome random sequencing and assembly of Haemophilus influenzae Rd. Science 269: pp. 496-512 CrossRef
    31. Midha, S, Ranjan, M, Sharma, V, Pinnaka, AK, Patil, PB (2012) Genome sequence of Xanthomonas citri pv. mangiferaeindicae strain LMG 941. J Bacteriol 194: pp. 3031 CrossRef
    32. Ah-You, N, Gagnevin, L, Chiroleu, F, Jouen, E, Neto, JR, Pruvost, O (2007) Pathological variations within Xanthomonas campestris pv. mangiferaeindicae support its separation into three distinct pathovars that can be distinguished by amplified fragment length polymorphism. Phytopathology 97: pp. 1568-77 CrossRef
    33. Du, P, Yang, Y, Wang, H, Liu, D, Gao, G, Chen, C (2011) A large scale comparative genomic analysis reveals insertion sites for newly acquired genomic islands in bacterial genomes. BMC Microbiol 11: pp. 135 CrossRef
    34. Caza, M, Kronstad, JW (2013) Shared and distinct mechanisms of iron acquisition by bacterial and fungal pathogens of humans. Front Cell Infect Microbiol. 3: pp. 80 CrossRef
    35. Gotoh, Y, Eguchi, Y, Watanabe, T, Okamoto, S, Doi, A, Utsumi, R (2010) Two-component signal transduction as potential drug targets in pathogenic bacteria. Curr Opin Microbiol 13: pp. 232-9 CrossRef
    36. Alfano, JR, Collmer, A (2004) Type III secretion system effector proteins: double agents in bacterial disease and plant defense. Annu Rev Phytopathol 42: pp. 385-414 CrossRef
    37. Christie, PJ, Vogel, JP (2000) Bacterial type IV secretion: conjugation systems adapted to deliver effector molecules to host cells. Trends Microbiol 8: pp. 354-60 CrossRef
    38. Brown, JS, Holden, DW (2002) Iron acquisition by gram-positive bacterial pathogens. Microb Infect 4: pp. 1149-56 CrossRef
    39. Marraffini, LA, Sontheimer, EJ (2008) CRISPR interference limits horizontal gene transfer in staphylococci by targeting DNA. Science 322: pp. 1843-5 CrossRef
    40. Chiang, T-Y, Chiang, YC, Pan, C-H, Wang, W-K, Chen, C-N, Hsu, T-W (2004) Comparative genomics of horizontal transfer between chloroplast and nuclear genomes in rice and Arabidopsis. Plant evolutionary genetics and biology of weeds. Endemic Species Research Institute, Nantou, Taiwan, pp. 1-10
    41. Mallet, J (2008) Hybridization, ecological races and the nature of species: empirical evidence for the ease of speciation. Phil Trans R Soc B 363: pp. 2971-86 CrossRef
    42. Didelot, X, Maiden, MCJ (2010) Impact of recombination on bacterial evolution. Trends Microbiol 18: pp. 315-22 CrossRef
    43. Guttman, DS, Dykhuizen, DE (1994) Clonal divergence in Escherichia coli as a result of recombination, not mutation. Science 266: pp. 1380-3 CrossRef
    44. Goldschmidt, R (1940) The material basis of evolution. Yale University Press, New Haven, CT
    45. Koeppel, A, Perry, EB, Sikorski, J, Krizanc, D, Warner, A, Ward, DM (2008) Identifying the fundamental units of bacterial diversity: a paradigm shift to incorporate ecology into bacterial systematics. Proc Natl Acad Sci U S A 105: pp. 2504-9 CrossRef
    46. Roohani, R, Najafabadi, MS, Alavi, SM, Farrokhi, N, Shams-bakhsh, M (2012) Transcript analysis of some pathogenicity-related elements in an Iranian A* isolate of Xanthomonas citri subsp. citri. J Crop Prot 1: pp. 337-47
    47. B眉ttner, D, Bonas, U (2010) Regulation and secretion of Xanthomonas virulence factors. FEMS Microbiol Rev 34: pp. 107-33 CrossRef
    48. Ryan, RP, Fouhy, Y, Lucey, JF, Jiang, B-L, He, Y-Q, Feng, J-X (2007) Cyclic di-GMP signalling in the virulence and environmental adaptation of Xanthomonas campestris. Mol Microbiol 63: pp. 429-42 CrossRef
    49. Slater, H, Alvarez-Morales, A, Barber, CE, Daniels, MJ, Dow, JM (2000) A two-component system involving an HD-GYP domain protein links cell鈥揷ell signalling to pathogenicity gene expression in Xanthomonas campestris. Mol Microbiol 38: pp. 986-1003 CrossRef
    50. Ryan, RP, Fouhy, Y, Lucey, JF, Crossman, LC, Spiro, S, He, YW (2006) Cell-cell signaling in Xanthomonas campestris involves an HD-GYP domain protein that functions in cyclic di-GMP turnover. Proc Natl Acad Sci U S A 103: pp. 6712-7 CrossRef
    51. Gupta, SD, Wu, HC, Rick, PD (1997) A Salmonella typhimurium genetic locus which confers copper tolerance on copper-sensitive mutants of Escherichia coli. J Bacteriol 179: pp. 4977-84
    52. Palmieri, ACB, Amaral, AM, Homem, RA, Machado, MA (2010) Differential expression of pathogenicity- and virulence-related genes of Xanthomonas axonopodis pv. citri under copper stress. Genet Mol Biol 33: pp. 348-53 CrossRef
    53. Ritchie, D (2004) Copper-containing fungicides/bactericides and their use in management of bacterial spot on peaches. Southeast Reg Newsl. 4: pp. 1
    54. Katzen, F, Beckwith, J (2003) Role and location of the unusual redox-active cysteines in the hydrophobic domain of the transmembrane electron transporter DsbD. Proc Natl Acad Sci U S A 100: pp. 10471-6 CrossRef
    55. Sella, G, Petrov, DA, Przeworski, M, Andolfatto, P (2009) Pervasive natural selection in the Drosophila genome?. PLoS Genet 5: pp. e1000495 CrossRef
    56. Wu, Q-S, Zou, Y-N, He, X-H (2010) Exogenous putrescine, not spermine or spermidine, enhances root mycorrhizal development and plant growth of trifoliate orange (Poncirus trifoliata) seedlings. Int J Agr Biol 12: pp. 576-80
    57. Erb, M, Lenk, C, Degenhardt, J, Turlings, TC (2009) The underestimated role of roots in defense against leaf attackers. Trends Plant Sci 14: pp. 653-9 CrossRef
    58. Pestana, M, Varennes, A, Goss, M, Abad铆a, J, Faria, E (2004) Floral analysis as a tool to diagnose iron chlorosis in orange trees. Plant Soil 259: pp. 287-95 CrossRef
    59. Hossain, T, Alam, Z, Absar, N (1999) Changes in different nutrients and enzyme contents in mango leaves infected with Colletotrichum glaeosorioides. Ind Phytopayhol 52: pp. 75-6
    60. Cornelis, GR (2006) The type III secretion injectisome. Nat Rev Microbiol 4: pp. 811-25 CrossRef
    61. Cornelis, GR, Gijsegem, F (2000) Assembly and function of type III secretory systems. Annu Rev Microbiol 54: pp. 735-74 CrossRef
    62. Tampakaki, A, Fadouloglou, V, Gazi, A, Panopoulos, N, Kokkinidis, M (2004) Conserved features of type III secretion. Cell Microbiol 6: pp. 805-16 CrossRef
    63. Lee, YH, Kolade, OO, Nomura, K, Arvidson, DN, He, SY (2005) Use of dominant-negative HrpA mutants to dissect Hrp pilus assembly and type III secretion in Pseudomonas syringae pv. tomato. J Biol Chem 280: pp. 21409-17 CrossRef
    64. Weber, E, Koebnik, R (2005) Domain structure of HrpE, the Hrp pilus subunit of Xanthomonas campestris pv. vesicatoria. J Bacteriol 187: pp. 6175-86 CrossRef
    65. Weber, E, Koebnik, R (2006) Positive selection of the Hrp pilin HrpE of the plant pathogen Xanthomonas. J Bacteriol 188: pp. 1405-10 CrossRef
    66. Guttman, DS, Gropp, SJ, Morgan, RL, Wang, PW (2006) Diversifying selection drives the evolution of the type III secretion system pilus of Pseudomonas syringae. Mol Biol Evol 23: pp. 2342-54 CrossRef
    67. Jacob, TR, Laia, ML, Moreira, LM, Goncalves, JF, Souza Carvalho, FM, Ferro, MIT (2014) Type IV secretion system is not involved in infection process in citrus. Int J Microbiol 2014: pp. 9 CrossRef
    68. Garnett, JA, Mart铆nez-Santos, VI, Salda帽a, Z, Pape, T, Hawthorne, W, Chan, J (2012) Structural insights into the biogenesis and biofilm formation by the Escherichia coli common pilus. Proc Natl Acad Sci U S A 109: pp. 3950-5 CrossRef
    69. Wong, KKY, Tan, LUL, Saddler, JN (1988) Multiplicity of beta-1,4-xylanase in microorganisms: functions and applications. Microbiol Rev. 52: pp. 305-17
    70. Szczesny, R, Jordan, M, Schramm, C, Schulz, S, Cogez, V, Bonas, U (2010) Functional characterization of the Xcs and Xps type II secretion systems from the plant pathogenic bacterium Xanthomonas campestris pv vesicatoria. New Phytol 187: pp. 983-1002 CrossRef
    71. Rajeshwari, R, Jha, G, Sonti, RV (2005) Role of an in planta-expressed xylanase of Xanthomonas oryzae pv. oryzae in promoting virulence on rice. Mol Plant-Microbe Interact 18: pp. 830-7 CrossRef
    72. Bentley, DR (2006) Whole-genome re-sequencing. Curr Opin Genet Dev 16: pp. 545-52 CrossRef
    73. Simpson, JT, Wong, K, Jackman, SD, Schein, JE, Jones, SJM, Birol, 陌 (2009) ABySS: a parallel assembler for short read sequence data. Genome Res 19: pp. 1117-23 CrossRef
    74. Boetzer, M, Henkel, CV, Jansen, HJ, Butler, D, Pirovano, W (2011) Scaffolding pre-assembled contigs using SSPACE. Bioinforma 27: pp. 578-9 CrossRef
    75. Delcher, AL, Harmon, D, Kasif, S, White, O, Salzberg, SL (1999) Improved microbial gene identification with GLIMMER. Nucleic Acids Res 27: pp. 4636-41 CrossRef
    76. Altschul, SF, Gish, W, Miller, W, Myers, EW, Lipman, DJ (1990) Basic local alignment search tool. J Mol Biol 215: pp. 403-10 CrossRef
    77. Tatusov, RL, Fedorova, ND, Jackson, JD, Jacobs, AR, Kiryutin, B, Koonin, EV (2003) The COG database: an updated version includes eukaryotes. BMC Bioinforma 4: pp. 41 CrossRef
    78. Lowe, TM, Eddy, SR (1997) tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res 25: pp. 0955-64 CrossRef
    79. Lagesen, K, Hallin, P, R酶dland, EA, St忙rfeldt, HH, Rognes, T, Ussery, DW (2007) RNAmmer: consistent and rapid annotation of ribosomal RNA genes. Nucleic Acids Res 35: pp. 3100-8 CrossRef
    80. Fuchsman, CA, Rocap, G (2006) Whole-genome reciprocal BLAST analysis reveals that planctomycetes do not share an unusually large number of genes with Eukarya and Archaea. Appl Environ Microbiol 72: pp. 6841-4 CrossRef
    81. Larkin, M, Blackshields, G, Brown, N, Chenna, R, McGettigan, P, McWilliam, H (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23: pp. 2947-8 CrossRef
    82. Suyama, M, Torrents, D, Bork, P (2006) PAL2NAL: robust conversion of protein sequence alignments into the corresponding codon alignments. Nucleic Acids Res 34: pp. W609-12 CrossRef
    83. Stamatakis, A (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinforma 22: pp. 2688-90 CrossRef
    84. Darriba, D, Taboada, GL, Doallo, R, Posada, D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 9: pp. 772 CrossRef
    85. Guindon, S, Gascuel, O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52: pp. 696-704 CrossRef
    86. Padidam, M, Sawyer, S, Fauquet, CM (1999) Possible emergence of new geminiviruses by frequent recombination. Virol 265: pp. 218-25 CrossRef
    87. Bruen, TC, Philippe, H, Bryant, D (2006) A simple and robust statistical test for detecting the presence of recombination. Genet 172: pp. 2665-81 CrossRef
    88. Yang, Z (2007) PAML 4: phylogenetic analysis by maximum likelihood. Mol Biol Evol 24: pp. 1586-91 CrossRef
    89. Yang, Z, Wong, WS, Nielsen, R (2005) Bayes empirical Bayes inference of amino acid sites under positive selection. Mol Biol Evol 22: pp. 1107-18 CrossRef
  • 刊物主题:Life Sciences, general; Microarrays; Proteomics; Animal Genetics and Genomics; Microbial Genetics and Genomics; Plant Genetics & Genomics;
  • 出版者:BioMed Central
  • ISSN:1471-2164
文摘
Background Comparative genomics provides insights into the diversification of bacterial species. Bacterial speciation usually takes place with lasting homologous recombination, which not only acts as a cohering force between diverging lineages but brings advantageous alleles favored by natural selection, and results in ecologically distinct species, e.g., frequent host shift in Xanthomonas pathogenic to various plants. Results Using whole-genome sequences, we examined the genetic divergence in Xanthomonas campestris that infected Brassicaceae, and X. citri, pathogenic to a wider host range. Genetic differentiation between two incipient races of X. citri pv. mangiferaeindicae was attributable to a DNA fragment introduced by phages. In contrast to most portions of the genome that had nearly equivalent levels of genetic divergence between subspecies as a result of the accumulation of point mutations, 10% of the core genome involving with homologous recombination contributed to the diversification in Xanthomonas, as revealed by the correlation between homologous recombination and genomic divergence. Interestingly, 179 genes were under positive selection; 98 (54.7%) of these genes were involved in homologous recombination, indicating that foreign genetic fragments may have caused the adaptive diversification, especially in lineages with nutritional transitions. Homologous recombination may have provided genetic materials for the natural selection, and host shifts likely triggered ecological adaptation in Xanthomonas. To a certain extent, we observed positive selection nevertheless contributed to ecological divergence beyond host shifting. Conclusion Altogether, mediated with lasting gene flow, species formation in Xanthomonas was likely governed by natural selection that played a key role in helping the deviating populations to explore novel niches (hosts) or respond to environmental cues, subsequently triggering species diversification.

© 2004-2018 中国地质图书馆版权所有 京ICP备05064691号 京公网安备11010802017129号

地址:北京市海淀区学院路29号 邮编:100083

电话:办公室:(+86 10)66554848;文献借阅、咨询服务、科技查新:66554700