Comparative genomic analysis of coffee-infecting xylella fastidiosa strains isolated from Brazil

Microbiology (United Kingdom)

Volumn 161, Issue , 2015, Pages 1018-1033

  Barbosa, Deibs ^a   Alencar, Valquíria Campos ^a   Santos, Daiene Souza ^a   Oliveira, Ana Cláudia de Freitas ^a   de Souza, Alessandra A ^b   Coletta Filho, Helvecio D ^b   de Oliveira, Regina Costa ^a   Nunes, Luiz R ^c  

^a UNIVERSIDADE DE MOGI DAS CRUZES   (Brazil)

^b INSTITUTO AGRONÔMICO   (Brazil)

^c UNIVERSIDADE FEDERAL DO ABC   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL TOXIN; HOST FACTOR; TRANSPOSON;

ARTICLE; BACTERIAL GENE; BACTERIAL GENOME; BACTERIAL STRAIN; BACTERIUM ISOLATION; BRAZIL; CHROMOSOME STRUCTURE; COFFEE; DNA MICROARRAY; EXPERIMENTATION; GENE SEQUENCE; GENOME ANALYSIS; HYBRIDIZATION; MICROARRAY ANALYSIS; NONHUMAN; OPEN READING FRAME; PHYLOGENY; PRIORITY JOURNAL; XYLELLA FASTIDIOSA; BACTERIAL CHROMOSOME; BIOLOGY; CLASSIFICATION; COFFEA; COMPARATIVE GENOMIC HYBRIDIZATION; GENETICS; GENOMICS; ISOLATION AND PURIFICATION; MICROBIOLOGY; MOLECULAR EVOLUTION; PLANT DISEASE; TRANSPOSON; XYLELLA;

CITRUS; XYLELLA FASTIDIOSA;

BRAZIL; CHROMOSOMES, BACTERIAL; COFFEA; COMPARATIVE GENOMIC HYBRIDIZATION; COMPUTATIONAL BIOLOGY; DNA TRANSPOSABLE ELEMENTS; EVOLUTION, MOLECULAR; GENOME, BACTERIAL; GENOMICS; OPEN READING FRAMES; PHYLOGENY; PLANT DISEASES; XYLELLA;

EID: 84991475163     PISSN: 13500872     EISSN: 14652080     Source Type: Journal    
DOI: 10.1099/mic.0.000068     Document Type: Article

References (82)

1. Aagesen, A. M. & Häse, C. C. (2012). Sequence analyses of type IV pili from Vibrio cholerae, Vibrio parahaemolyticus, and Vibrio vulnificus. Microb Ecol 64, 509–524
2. Acuña, L. G., Cárdenas, J. P., Covarrubias, P. C., Haristoy, J. J., Flores, R., Nuñez, H., Riadi, G., Shmaryahu, A., Valdés, J. & other authors (2013). Architecture and gene repertoire of the flexible genome of the extreme acidophile Acidithiobacillus caldus. PLoS One 8, e78237
3. Alencar, V. C., Barbosa, D., Santos, D. S., Oliveira, A. C. F., de Oliveira, R. C. & Nunes, L. R. (2014). Genomic sequencing of two coffee-infecting strains of Xylella fastidiosa isolated from Brazil. Genome Announc 2, e01190-13
4. Almeida, R. P., Nascimento, F. E., Chau, J., Prado, S. S., Tsai, C. W., Lopes, S. A. & Lopes, J. R. (2008). Genetic structure and biology of Xylella fastidiosa strains causing disease in citrus and coffee in Brazil. Appl Environ Microbiol 74, 3690–3701
5. Bhattacharyya, A., Stilwagen, S., Ivanova, N., D’Souza, M., Bernal, A., Lykidis, A., Kapatral, V., Anderson, I., Larsen, N. & other authors (2002). Whole-genome comparative analysis of three phytopathogenic Xylella fastidiosa strains. Proc Natl Acad Sci U S A 99, 12403–12408
6. Blumer, C., Kleefeld, A., Lehnen, D., Heintz, M., Dobrindt, U., Nagy, G., Michaelis, K., Emödy, L., Polen, T. (2005). Regulation of type 1 fimbriae synthesis and biofilm formation by the transcriptional regulator LrhA of Escherichia coli. Microbiology 151, 3287–3298
7. Champion, O. L., Gaunt, M. W., Gundogdu, O., Elmi, A., Witney, A. A., Hinds, J., Dorrell, N. & Wren, B. W. (2005). Comparative phylogenomics of the food-borne pathogen Campylobacter jejuni reveals genetic markers predictive of infection source. Proc Natl Acad Sci U S A 102, 16043–16048
8. Chen, J., Groves, R., Civerolo, E. L., Viveros, M., Freeman, M. & Zheng, Y. (2005). Two Xylella fastidiosa genotypes associated with almond leaf scorch disease on the same location in California. Phytopathology 95, 708–714
9. Chen, J., Xie, G., Han, S., Chertkov, O., Sims, D. & Civerolo, E. L. (2010). Whole genome sequences of two Xylella fastidiosa strains (M12 and M23) causing almond leaf scorch disease in California. J Bacteriol 192, 4534
10. Chen, J., Huang, H., Chang, C. J. & Stenger, D. C. (2013). Draft genome sequence of Xylella fastidiosa subsp. multiplex strain Griffin-1 from Quercus rubra in Georgia. Genome Announc 1, e00756-13
11. Ciraulo, M. B., Santos, D. S., Rodrigues, A. C., de Oliveira, M. V., Rodrigues, T., de Oliveira, R. C. & Nunes, L. R. (2010). Transcriptome analysis of the phytobacterium Xylella fastidiosa growing under xylem-based chemical conditions. J Biomed Biotechnol 2010, 781365
12. Clifford, J. C., Rapicavoli, J. N. & Roper, M. C. (2013). A rhamnoserich O-antigen mediates adhesion, virulence, and host colonization for the xylem-limited phytopathogen Xylella fastidiosa. Mol Plant Microbe Interact 26, 676–685
13. Costa, H. S., Guzman, A., Hernandez-Martinez, R., Gispert, C. & Cooksey, D. A. (2006). Detection and differentiation of Xylella fastidiosa strains acquired and retained by glassy-winged sharpshooters (Hemiptera: Cicadellidae) using a mixture of strain-specific primer sets. J Econ Entomol 99, 1058–1064
14. Costa de Oliveira, R., Yanai, G. M., Muto, N. H., Leite, D. B., de Souza, A. A., Coletta Filho, H. D., Machado, M. A. & Nunes, L. R. (2002). Competitive hybridization on spotted microarrays as a tool to conduct comparative genomic analyses of Xylella fastidiosa strains. FEMS Microbiol Lett 216, 15–21
15. Cursino, L., Galvani, C. D., Athinuwat, D., Zaini, P. A., Li, Y., De La Fuente, L., Hoch, H. C., Burr, T. J. & Mowery, P. (2011). Identification of an operon, Pil-Chp, that controls twitching motility and virulence in Xylella fastidiosa. Mol Plant Microbe Interact 24, 1198–1206.
16. da Silva, V. S., Shida, C. S., Rodrigues, F. B., Ribeiro, D. C., de Souza, A. A., Coletta-Filho, H. D., Machado, M. A., Nunes, L. R. & de Oliveira, R. C. (2007). Comparative genomic characterization of citrusassociated Xylella fastidiosa strains. BMC Genomics 8, 474
17. Darling, A. E., Mau, B. & Perna, N. T. (2010). progressiveMauve: multiple genome alignment with gene gain, loss and rearrangement. PLoS One 5, e11147
18. Davis, M. J., Purcell, A. & Thomson, S. V. (1980). Isolation medium for the Pierce’s disease bacterium. Phytopathology 70, 425–429.
19. de Lima, J. E. O., Miranda, V. S., Hartung, J. S., Brlansky, R. H., Coutinho, A., Roberto, S. R. & Carlos, E. F. (1998). Coffee leaf scorch bacterium: Axenic culture, pathogenicity, and comparison with Xylella fastidiosa of citrus. Plant Dis 82, 94–97.
20. de Mello Varani, A., Souza, R. C., Nakaya, H. I., de Lima, W. C., Paula de Almeida, L. G., Kitajima, E. W., Chen, J., Civerolo, E., Vasconcelos, A. T. & Van Sluys, M. A. (2008). Origins of the Xylella fastidiosa prophage-like regions and their impact in genome differentiation. PLoS One 3, e4059.
21. de Souza, A. A., Takita, M. A., Coletta-Filho, H. D., Caldana, C., Goldman, G. H., Yanai, G. M., Muto, N. H., de Oliveira, R. C., Nunes, L. R. & Machado, M. A. (2003). Analysis of gene expression in two growth states of Xylella fastidiosa and its relationship with pathogenicity. Mol Plant Microbe Interact 16, 867–875.
22. de Souza, A. A., Takita, M. A., Coletta-Filho, H. D., Caldana, C., Yanai, G. M., Muto, N. H., de Oliveira, R. C., Nunes, L. R. & Machado, M. A. (2004). Gene expression profile of the plant pathogen Xylella fastidiosa during biofilm formation in vitro. FEMS Microbiol Lett 237, 341–353
23. Doddapaneni, H., Yao, J., Lin, H., Walker, M. A. & Civerolo, E. L. (2006). Analysis of the genome-wide variations among multiple strains of the plant pathogenic bacterium Xylella fastidiosa. BMC Genomics 7, 225
24. Doddapaneni, H., Francis, M., Yao, J., Lin, H. & Civerolo, E.L. (2007). Genome-wide analysis of Xylella fastidiosa: implications for detection and strain relationships. Afr J Biotechnol 6, 55–66
25. Dorrell, N., Hinchliffe, S. J. & Wren, B. W. (2005). Comparative phylogenomics of pathogenic bacteria by microarray analysis. Curr Opin Microbiol 8, 620–626
26. Felsenstein, J. (1989). PHYLIP –Phylogeny Inference Package (Version 3.2). Cladistics 5, 164–166
27. Fernández-Gómez, B., Fernàndez-Guerra, A., Casamayor, E. O., González, J. M., Pedrós-Alió, C. & Acinas, S. G. (2012). Patterns and architecture of genomic islands inmarine bacteria. BMCGenomics 13, 347
28. Fronzes, R., Remaut, H. & Waksman, G. (2008). Architectures and biogenesis of non-flagellar protein appendages in Gram-negative bacteria. EMBO J 27, 2271–2280
29. Gal-Mor, O. & Finlay, B. B. (2006). Pathogenicity islands: a molecular toolbox for bacterial virulence. Cell Microbiol 8, 1707–1719
30. Goris, J., Konstantinidis, K. T., Klappenbach, J. A., Coenye, T., Vandamme, P. & Tiedje, J. M. (2007). DNA–DNA hybridization values and their relationship to whole-genome sequence similarities. Int J Syst Evol Microbiol 57, 81–91
31. Greenfield, L. K. & Whitfield, C. (2012). Synthesis of lipopolysaccharide O-antigens by ABC transporter-dependent pathways. Carbohydr Res 356, 12–24
32. Gu, X., Glushka, J., Yin, Y., Xu, Y., Denny, T., Smith, J., Jiang, Y. & Bar- Peled, M. (2010). Identification of a bifunctional UDP-4-ketopentose/ UDP-xylose synthase in the plant pathogenic bacterium Ralstonia solanacearum strain GMI1000, a distinct member of the 4,6- dehydratase and decarboxylase family. J Biol Chem 285, 9030–9040
33. Guan, W., Shao, J., Davis, R. E., Zhao, T. & Huang, Q. (2014a). Genome sequence of a Xylella fastidiosa strain causing sycamore leaf scorch disease in Virginia. Genome Announc 2, e00773-14
34. Guan, W., Shao, J., Zhao, T. & Huang, Q. (2014b). Genome sequence of a Xylella fastidiosa strain causing mulberry leaf scorch disease in Maryland. Genome Announc 2, e00916-13
35. Hagemann, M., Hasse, D. & Berg, G. (2006). Detection of a phage genome carrying a zonula occludens like toxin gene (zot) in clinical isolates of Stenotrophomonas maltophilia. Arch Microbiol 185, 449–458
36. Hopkins, D. L. (1989). Xylella fastidiosa: xylem-limited bacterial pathogen of plants. Annu Rev Phytopathol 27, 271–290
37. Hopkins, D. L. & Purcell, A. H. (2002). Xylella fastidiosa: cause of Pierce’s disease of grapevine and other emergent diseases. Plant Dis 86, 1056–1066
38. Howard, S. L., Gaunt, M. W., Hinds, J., Witney, A. A., Stabler, R. & Wren, B. W. (2006). Application of comparative phylogenomics to study the evolution of Yersinia enterocolitica and to identify genetic differences relating to pathogenicity. J Bacteriol 188, 3645–3653
39. Kannenberg, E. L. & Carlson, R. W. (2001). Lipid A and O-chain modifications cause Rhizobium lipopolysaccharides to become hydrophobic during bacteroid development. Mol Microbiol 39, 379–392
40. Kittichotirat, W., Bumgarner, R. E., Asikainen, S. & Chen, C. (2011). Identification of the pangenome and its components in 14 distinct Aggregatibacter actinomycetemcomitans strains by comparative genomic analysis. PLoS One 6, e22420
41. Konstantinidis, K. T. & Tiedje, J. M. (2005). Genomic insights that advance the species definition for prokaryotes. Proc Natl Acad Sci U S A 102, 2567–2572
42. Kung, S. H. & Almeida, R. P. (2011). Natural competence and recombination in the plant pathogen Xylella fastidiosa. Appl Environ Microbiol 77, 5278–5284
43. Kung, S. H., Retchless, A. C., Kwan, J. Y. & Almeida, R. P. (2013). Effects of DNA size on transformation and recombination efficiencies in Xylella fastidiosa. Appl Environ Microbiol 79, 1712–1717
44. Larkin, M. A., Blackshields, G., Brown, N. P., Chenna, R., McGettigan, P. A., McWilliam, H., Valentin, F., Wallace, I. M., Wilm, A. (2007). CLUSTAL W and CLUSTAL X version 2.0 Bioinformatics 23, 2947–2948
45. Lerouge, I., Verreth, C., Michiels, J., Carlson, R. W., Datta, A., Gao, M. Y. & Vanderleyden, J. (2003). Three genes encoding for putative methyl- and acetyltransferases map adjacent to the wzm and wzt genes and are essential for O-antigen biosynthesis in Rhizobium etli CE3 Mol Plant Microbe Interact 16, 1085–1093
46. Letunic, I. & Bork, P. (2007). Interactive Tree Of Life (iTOL): an online tool for phylogenetic tree display and annotation. Bioinformatics 23, 127–128
47. Li, W. B., Pria, W. D., Jr, Teixeira, D. C., Miranda, V. S., Ayres, A. J., Franco, C. F., Costa, M. G., He, C.-X., Costa, P. I. & Hartung, J. S. (2001). Coffee leaf scorch caused by a strain of Xylella fastidiosa from citrus. Plant Dis 85, 501–505
48. Li, Y., Hao, G., Galvani, C. D., Meng, Y., De La Fuente, L., Hoch, H. C. & Burr, T. J. (2007). Type I and type IV pili of Xylella fastidiosa affect twitching motility, biofilm formation and cell–cell aggregation. Microbiology 153, 719–726
49. Margulies, M., Egholm, M., Altman, W. E., Attiya, S., Bader, J. S., Bemben, L. A., Berka, J., Braverman, M. S., Chen, Y. J. 2005. Genome sequencing in microfabricated high-density picolitre reactors. Nature 437, 376–380
50. Marttinen, P., Hanage, W. P., Croucher, N. J., Connor, T. R., Harris, S. R., Bentley, S. D. & Corander, J. (2012). Detection of recombination events in bacterial genomes from large population samples. Nucleic Acids Res 40, e6
51. Mehta, A. & Rosato, Y. B. (2001). Phylogenetic relationships of Xylella fastidiosa strains from different hosts, based on 16S rDNA and 16S–23S intergenic spacer sequences. Int J Syst Evol Microbiol 51, 311–318
52. Mehta, A., Pereira Leite, R., Jr & Bomura Rosato, Y. (2001). Assessment of the genetic diversity of Xylella fastidiosa isolated from citrus in Brazil by PCR-RFLP of the 16S rDNA and 16S–23S intergenic spacer and rep-PCR fingerprinting. Antonie van Leeuwenhoek 79, 53–59
53. Meng, Y., Li, Y., Galvani, C. D., Hao, G., Turner, J. N., Burr, T. J. & Hoch, H. C. (2005). Upstream migration of Xylella fastidiosa via pilus-driven twitching motility. J Bacteriol 187, 5560–5567
54. Nguyen, L. C., Taguchi, F., Tran, Q. M., Naito, K., Yamamoto, M., Ohnishi-Kameyama, M., Ono, H., Yoshida, M., Chiku, K. & other authors (2012). Type IV pilin is glycosylated in Pseudomonas syringae pv. tabaci 6605 and is required for surface motility and virulence. Mol Plant Pathol 13, 764–774
55. Nunes, L. R., Rosato, Y. B., Muto, N. H., Yanai, G. M., da Silva, V. S., Leite, D. B., Gonçalves, E. R., de Souza, A. A., Coletta-Filho, H. D. (2003). Microarray analyses of Xylella fastidiosa provide evidence of coordinated transcription control of laterally transferred elements. Genome Res 13, 570–578
56. Nunney, L., Yuan, X., Bromley, R., Hartung, J., Montero-Astúa, M., Moreira, L., Ortiz, B. & Stouthamer, R. (2010). Population genomic analysis of a bacterial plant pathogen: novel insight into the origin of Pierce’s disease of grapevine in the U.S. PLoS One 5, e15488
57. Nunney, L., Yuan, X., Bromley, R. E. & Stouthamer, R. (2012). Detecting genetic introgression: high levels of intersubspecific recombination found in Xylella fastidiosa in Brazil. Appl Environ Microbiol 78, 4702–4714
58. Ochman, H., Lawrence, J. G. & Groisman, E. A. (2000). Lateral gene transfer and the nature of bacterial innovation. Nature 405, 299–304
59. Oresnik, I. J., Twelker, S. & Hynes, M. F. (1999). Cloning and characterization of a Rhizobium leguminosarum gene encoding a bacteriocin with similarities to RTX toxins. Appl Environ Microbiol 65, 2833–2840
60. Paradela-Filho, O., Sugimori, M. H., Ribeiro, I. J. A. & Garcia, A., Jr Beretta, M. J. G., Harakawa, R., Machado, M. A., Laranjeira, F.F, Rodrigues Neto, J. & Beriam, L. O. S. (1997). Occurrence of Xylella fastidiosa in coffee plants in Brazil. Summa Phytopathol 23, 46–49
61. Pieretti, I., Royer, M., Barbe, V., Carrere, S., Koebnik, R., Cociancich, S., Couloux, A., Darrasse, A., Gouzy, J. & other authors (2009). The complete genome sequence of Xanthomonas albilineans provides new insights into the reductive genome evolution of the xylem-limited Xanthomonadaceae. BMC Genomics 10, 616
62. Pooler, M. R. & Hartung, J. S. (1995). Specific PCR detection and identification of Xylella fastidiosa strains causing citrus variegated chlorosis. Curr Microbiol 31, 377–381
63. Puvirajesinghe, T. M., Elantak, L., Lignon, S., Franche, N., Ilbert, M. & Ansaldi, M. (2012). DnaJ (Hsp40 protein) binding to folded substrate impactsKplE1 prophage excision efficiency. J Biol Chem 287, 14169–14177
64. Richter, M. & Rosselló-Móra, R. (2009). Shifting the genomic gold standard for the prokaryotic species definition. Proc Natl Acad Sci U S A 106, 19126–19131
65. Rocha, J. G., Zambolim, L., Zambolim, E. M., Ribeiro do Vale, F. X., Junior, W. C. J. & Filho, A. B. (2010). Quantification of yield loss due to coffee leaf scorch. Crop Prot 29, 1100–1104
66. Ronquist, F. & Huelsenbeck, J. P. (2003). MrBayes 3: Bayesian phylogenetic inference under mixedmodels. Bioinformatics 19, 1572–1574
67. Roper, M. C., Greve, L. C., Warren, J. G., Labavitch, J. M. & Kirkpatrick, B. C. (2007). Xylella fastidiosa requires polygalacturonase for colonization and pathogenicity in Vitis vinifera grapevines. Mol Plant Microbe Interact 20, 411–419
68. Saeed, A. I., Sharov, V., White, J., Li, J., Liang, W., Bhagabati, N., Braisted, J., Klapa, M., Currier, T. (2003). TM4: a free, open-source system for microarray data management and analysis. Biotechniques 34, 374–378
69. Schaad, N. W., Postnikova, E., Lacy, G., Fatmi, M. & Chang, C. J. (2004). Xylella fastidiosa subspecies: X. fastidiosa subsp. [correction] fastidiosa [correction] subsp. nov., X. fastidiosa subsp. multiplex subsp. nov., and X. fastidiosa subsp. pauca subsp. nov. Syst Appl Microbiol 27, 290–300
70. Schreiber, I. V., Koiral, H., Lara, M., Ojeda, A., Dowd, M., Bextin, S. E. & Moran, L. (2010). Unraveling the first Xylella fastidiosa subsp. fastidiosa genome from Texas. Southwest Entomologist 35, 479–483
71. Simpson, A. J., Reinach, F. C., Arruda, P., Abreu, F. A., Acencio, M., Alvarenga, R., Alves, L. M., Araya, J. E., Baia, G. S. & other authors (2000). The genome sequence of the plant pathogen Xylella fastidiosa. The Xylella fastidiosa Consortium of the Organization for Nucleotide Sequencing and Analysis. Nature 406, 151–159
72. Su, C. C., Deng, W. L., Jan, F. J., Chang, C. J., Huang, H. & Chen, J. (2014). Draft genome sequence of Xylella fastidiosa pear leaf scorch strain in Taiwan. Genome Announc 2, e00166-14
73. Sun, Q., Greve, L. C. & Labavitch, J. M. (2011). Polysaccharide compositions of intervessel pit membranes contribute to Pierce’s disease resistance of grapevines. Plant Physiol 155, 1976–1987
74. Thanweer, F., Tahiliani, V., Korres, H. & Verma, N. K. (2008). Topology and identification of critical residues of the O-acetyltransferase of serotype-converting bacteriophage, SF6, of Shigella flexneri. Biochem Biophys Res Commun 375, 581–585.
75. van Kessel, J. C., Ulrich, L. E., Zhulin, I. B. & Bassler, B. L. (2013). Analysis of activator and repressor functions reveals the requirements for transcriptional control by LuxR, the master regulator of quorum sensing in Vibrio harveyi. MBio 4, e00378-13
76. Van Sluys, M. A., de Oliveira, M. C., Monteiro-Vitorello, C. B., Miyaki, C. Y., Furlan, L. R., Camargo, L. E., da Silva, A. C., Moon, D. H., Takita, M. A. & other authors (2003). Comparative analyses of the complete genome sequences of Pierce’s disease and citrus variegated chlorosis strains of Xylella fastidiosa. J Bacteriol 185, 1018–1026
77. Varani, A. M., Monteiro-Vitorello, C. B., de Almeida, L. G., Souza, R. C., Cunha, O. L., Lima, W. C., Civerolo, E., Van Sluys, M. A. & Vasconcelos, A. T. (2012). Xylella fastidiosa comparative genomic database is an information resource to explore the annotation, genomic features, and biology of different strains. Genet Mol Biol 35, 149–152
78. Varani, A. M., Monteiro-Vitorello, C. B., Nakaya, H. I. & Van Sluys, M. A. (2013). The role of prophage in plant-pathogenic bacteria. Annu Rev Phytopathol 51, 429–451
79. Weissman, S. J., Chattopadhyay, S., Aprikian, P., Obata-Yasuoka, M., Yarova-Yarovaya, Y., Stapleton, A., Ba-Thein, W., Dykhuizen, D., Johnson, J. R. & Sokurenko, E. V. (2006). Clonal analysis reveals high rate of structural mutations in fimbrial adhesins of extraintestinal pathogenic Escherichia coli. Mol Microbiol 59, 975–988
80. Wells, J. M., Raju, B. C., Hung, H. Y., Weisburg, W. G., Mandelco-Paul, L. & Brenner, D. J. (1987). Xylella fastidiosa gen. nov., sp. nov: Gram negative xylem-limited fastidious plant bacteria related to Xanthomonas spp. Int J Syst Evol Bacteriol 37, 136–143
81. Zhang, S., Flores-Cruz, Z., Kumar, D., Chakrabarty, P., Hopkins, D. L. & Gabriel, D. W. (2011). The Xylella fastidiosa biocontrol strain EB92- 1 genome is very similar and syntenic to Pierce’s disease strains. J Bacteriol 193, 5576–5577
82. Zhou, Y., Liang, Y., Lynch, K. H., Dennis, J. J. & Wishart, D. S. (2011). PHAST: a fast phage search tool. Nucleic Acids Res 39 (Web Server issue), W347–W352.