Defining the phylogenomics of Shigella species: A pathway to diagnostics

Journal of Clinical Microbiology

Volumn 53, Issue 3, 2015, Pages 951-960

  Sahl, Jason W ^a,b,c   Morris, Carolyn R ^a   Emberger, Jennifer ^a   Fraser, Claire M ^a   Ochieng, John Benjamin ^d   Juma, Jane ^d   Fields, Barry ^e   Breiman, Robert F ^e   Gilmour, Matthew ^f,h   Nataro, James P ^g   Rasko, David A ^a  

^a UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

^b TRANSLATIONAL GENOMICS RESEARCH INSTITUTE   (United States)

^c NORTHERN ARIZONA UNIVERSITY   (United States)

^d KEMRI CDC Kisumu ^*  (Kenya)

^e Centers for Disease Control and Prevention Kenya   (Kenya)

^f PUBLIC HEALTH AGENCY OF CANADA   (Canada)

^g UNIVERSITY OF VIRGINIA   (United States)

^h HEALTH SCIENCES CENTRE   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

AMPLICON; ARTICLE; BACTERIAL GENOME; BACTERIUM IDENTIFICATION; BACTERIUM ISOLATE; CLADISTICS; CONTROLLED STUDY; ESCHERICHIA COLI; GENE SEQUENCE; MULTIPLEX POLYMERASE CHAIN REACTION; NONHUMAN; PHYLOGENOMICS; PHYLOGENY; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; SENSITIVITY AND SPECIFICITY; SHIGELLA; SHIGELLA BOYDII; SHIGELLA DYSENTERIAE; SHIGELLA FLEXNERI; SHIGELLA SONNEI; CHEMISTRY; CLASSIFICATION; CLUSTER ANALYSIS; DNA SEQUENCE; DYSENTERY, BACILLARY; GENETIC VARIATION; GENETICS; HUMAN; ISOLATION AND PURIFICATION; MICROBIOLOGY; PROCEDURES;

ESCHERICHIA COLI; SHIGELLA; SHIGELLA BOYDII; SHIGELLA DYSENTERIAE; SHIGELLA FLEXNERI; SHIGELLA SONNEI;

BACTERIAL DNA;

CLUSTER ANALYSIS; DNA, BACTERIAL; DYSENTERY, BACILLARY; GENETIC VARIATION; GENOME, BACTERIAL; HUMANS; MULTIPLEX POLYMERASE CHAIN REACTION; PHYLOGENY; SENSITIVITY AND SPECIFICITY; SEQUENCE ANALYSIS, DNA; SHIGELLA;

EID: 84923342636     PISSN: 00951137     EISSN: 1098660X     Source Type: Journal    
DOI: 10.1128/JCM.03527-14     Document Type: Article

References (60)

1. Niyogi SK. 2005. Shigellosis. J Microbiol 43:133-143.
2. Kotloff KL, Winickoff JP, Ivanoff B, Clemens JD, Swerdlow DL, Sansonetti PJ, Adak GK, Levine MM. 1999. Global burden of Shigella infections: implications for vaccine development and implementation of control strategies. Bull World Health Organ 77:651-666.
3. WHO. 2009, posting date. Initiative for vaccine research (IVR): diarrhoeal diseases. WHO, Geneva, Switzerland.
4. Kotloff KL, Nataro JP, Blackwelder WC, Nasrin D, Farag TH, Panchalingam S, Wu Y, Sow SO, Sur D, Breiman RF, Faruque AS, Zaidi AK, Saha D, Alonso PL, Tamboura B, Sanogo D, Onwuchekwa U, Manna B, Ramamurthy T, Kanungo S, Ochieng JB, Omore R, Oundo JO, Hossain A, Das SK, Ahmed S, Qureshi S, Quadri F, Adegbola RA, Antonio M, Hossain MJ, Akinsola A, Mandomando I, Nhampossa T, Acacio S, Biswas K, O'Reilly CE, Mintz ED, Berkeley LY, Muhsen K, Sommerfelt H, Robins-Browne RM, Levine MM. 2013. Burden and aetiology of diarrhoeal disease in infants and young children in developing countries (the Global Enteric Multicenter Study, GEMS): a prospective, case-control study. Lancet 382:209-222. http://dx.doi.org/10.1016/S0140-6736 (13) 60844-2.
5. Kotloff KL, Blackwelder WC, Nasrin D, Nataro JP, Farag TH, Van Eijk A, Adegbola RA, Alonso PL, Breiman RF, Faruque AS, Saha D, Sow SO, Sur D, Zaidi AK, Biswas K, Panchalingam S, Clemens JD, Cohen D, Glass RI, Mintz ED, Sommerfelt H, Levine MM. 2012. The Global Enteric Multicenter Study (GEMS) of diarrheal disease in infants and young children in developing countries: epidemiologic and clinical methods of the case/control study. Clin Infect Dis 55(Suppl 4):S232-S245. http://dx.doi.org/10.1093/cid/cis753.
6. Farag TH, Faruque AS, Wu Y, Das SK, Hossain A, Ahmed S, Ahmed D, Nasrin D, Kotloff KL, Panchilangam S, Nataro JP, Cohen D, Blackwelder WC, Levine MM. 2013. Housefly population density correlates with shigellosis among children in Mirzapur, Bangladesh: a time series analysis. PLoS Negl Trop Dis 7:e2280. http://dx.doi.org/10.1371/journal.pntd.0002280.
7. Ewing WH. 1949. Shigella nomenclature. J Bacteriol 57:633-638.
8. Johnson JR. 2000. Shigella and Escherichia coli at the crossroads: Machiavellian masqueraders or taxonomic treachery? J Med Microbiol 49:583-585.
9. Liu B, Knirel YA, Feng L, Perepelov AV, Senchenkova SN, Wang Q, Reeves PR, Wang L. 2008. Structure and genetics of Shigella O antigens. FEMS Microbiol Rev 32:627-653. http://dx.doi.org/10.1111/j.1574-6976.2008.00114.x.
10. Lefebvre J, Gosselin F, Ismail J, Lorange M, Lior H, Woodward D. 1995. Evaluation of commercial antisera for Shigella serogrouping. J Clin Microbiol 33:1997-2001.
11. Faruque SM, Haider K, Rahman MM, Abdul Alim AR, Ahmad QS, Albert MJ, Sack RB. 1992. Differentiation of Shigella flexneri strains by rRNA gene restriction patterns. J Clin Microbiol 30:2996-2999.
12. Liu PY, Lau YJ, Hu BS, Shyr JM, Shi ZY, Tsai WS, Lin YH, Tseng CY. 1995. Analysis of clonal relationships among isolates of Shigella sonnei by different molecular typing methods. J Clin Microbiol 33:1779-1783.
13. Yang J, Nie H, Chen L, Zhang X, Yang F, Xu X, Zhu Y, Yu J, Jin Q. 2007. Revisiting the molecular evolutionary history of Shigella spp. J Mol Evol 64:71-79. http://dx.doi.org/10.1007/s00239-006-0052-8.
14. Gorgé O, Lopez S, Hilaire V, Lisanti O, Ramisse V, Vergnaud G. 2008. Selection and validation of a multilocus variable-number tandem-repeat analysis panel for typing Shigella spp. J Clin Microbiol 46:1026-1036. http://dx.doi.org/10.1128/JCM.02027-07.
15. Pupo GM, Lan R, Reeves PR. 2000. Multiple independent origins of Shigella clones of Escherichia coli and convergent evolution of many of their characteristics. Proc Natl Acad Sci U S A 97:10567-10572. http://dx.doi.org/10.1073/pnas.180094797.
16. Maiden MC, Bygraves JA, Feil E, Morelli G, Russell JE, Urwin R, Zhang Q, Zhou J, Zurth K, Caugant DA, Feavers IM, Achtman M, Spratt BG. 1998. Multilocus sequence typing: a portable approach to the identification of clones within populations of pathogenic microorganisms. Proc Natl Acad Sci U S A 95:3140-3145. http://dx.doi.org/10.1073/pnas.95.6.3140.
17. Sahl JW, Steinsland H, Redman JC, Angiuoli SV, Nataro JP, Sommerfelt H, Rasko DA. 2011. A comparative genomic analysis of diverse clonal types of enterotoxigenic Escherichia coli reveals pathovar-specific conservation. Infect Immun 79:950-960. http://dx.doi.org/10.1128/IAI.00932-10.
18. Dykhuizen DE, Green L. 1991. Recombination in Escherichia coli and the definition of biological species. J Bacteriol 173:7257-7268.
19. O'Reilly CE, Jaron P, Ochieng B, Nyaguara A, Tate JE, Parsons MB, Bopp CA, Williams KA, Vinje J, Blanton E, Wannemuehler KA, Vulule J, Laserson KF, Breiman RF, Feikin DR, Widdowson MA, Mintz E. 2012. Risk factors for death among children less than 5 years old hospitalized with diarrhea in rural western Kenya, 2005-2007: a cohort study. PLoS Med 9:e1001256. http://dx.doi.org/10.1371/journal.pmed.1001256.
20. Fullá N, Prado V, Durán C, Lagos R, Levine MM. 2005. Surveillance for antimicrobial resistance profiles among Shigella species isolated from a semirural community in the northern administrative area of Santiago, Chile. Am J Trop Med Hyg 72:851-854.
21. Prado V, Lagos R, Nataro JP, San Martin O, Arellano C, Wang JY, Borczyk AA, Levine MM. 1999. Population-based study of the incidence of Shigella diarrhea and causative serotypes in Santiago, Chile. Pediatr Infect Dis J 18:500-505. http://dx.doi.org/10.1097/00006454-199906000-00005.
22. Myers EW, Sutton GG, Delcher AL, Dew IM, Fasulo DP, Flanigan MJ, Kravitz SA, Mobarry CM, Reinert KH, Remington KA, Anson EL, Bolanos RA, Chou HH, Jordan CM, Halpern AL, Lonardi S, Beasley EM, Brandon RC, Chen L, Dunn PJ, Lai Z, Liang Y, Nusskern DR, Zhan M, Zhang Q, Zheng X, Rubin GM, Adams MD, Venter JC. 2000. A whole-genome assembly of Drosophila. Science 287:2196-2204. http://dx.doi.org/10.1126/science.287.5461.2196.
23. Pop M, Phillippy A, Delcher AL, Salzberg SL. 2004. Comparative genome assembly. Brief Bioinform 5:237-248. http://dx.doi.org/10.1093/bib/5.3.237.
24. Assefa S, Keane TM, Otto TD, Newbold C, Berriman M. 2009. ABACAS: algorithm-based automatic contiguation of assembled sequences. Bioinformatics 25:1968-1969. http://dx.doi.org/10.1093/bioinformatics/btp347.
25. Tsai IJ, Otto TD, Berriman M. 2010. Improving draft assemblies by iterative mapping and assembly of short reads to eliminate gaps. Genome Biol 11:R41. http://dx.doi.org/10.1186/gb-2010-11-4-r41.
26. Li H, Durbin R. 2009. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25:1754-1760. http://dx.doi.org/10.1093/bioinformatics/btp324.
27. Zerbino DR, Birney E. 2008. Velvet: algorithms for de novo short read assembly using de Bruijn graphs. Genome Res 18:821-829. http://dx.doi.org/10.1101/gr.074492.107.
28. Otto TD, Sanders M, Berriman M, Newbold C. 2010. Iterative correction of reference nucleotides (iCORN) using second generation sequencing technology. Bioinformatics 26:1704-1707. http://dx.doi.org/10.1093/bioinformatics/btq269.
29. Angiuoli SV, Salzberg SL. 9 December 2010, posting date. Mugsy: fast multiple alignment of closely related whole genomes. Bioinformatics http://dx.doi.org/10.1093/bioinformatics/btq665.
30. Sahl JW, Matalka MN, Rasko DA. 2012. Phylomark, a tool to identify conserved phylogenetic markers from whole-genome alignments. Appl Environ Microbiol 78:4884-4892. http://dx.doi.org/10.1128/AEM.00929-12.
31. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. 1990. Basic local alignment search tool. J Mol Biol 215:403-410. http://dx.doi.org/10.1016/S0022-2836 (05) 80360-2.
32. Edgar RC. 2004. MUSCLE: a multiple sequence alignment with reduced time and space complexity. BMC Bioinformatics 5:113. http://dx.doi.org/10.1186/1471-2105-5-113.
33. Price MN, Dehal PS, Arkin AP. 2010. FastTree 2-approximately maximumlikelihood trees for large alignments. PLoS One 5:e9490. http://dx.doi.org/10.1371/journal.pone.0009490.
34. Wirth T, Falush D, Lan R, Colles F, Mensa P, Wieler LH, Karch H, Reeves PR, Maiden MC, Ochman H, Achtman M. 2006. Sex and virulence in Escherichia coli: an evolutionary perspective. Mol Microbiol 60:1136-1151. http://dx.doi.org/10.1111/j.1365-2958.2006.05172.x.
35. Bruen TC, Philippe H, Bryant D. 2006. A simple and robust statistical test for detecting the presence of recombination. Genetics 172:2665-2681.
36. Rozen S, Skaletsky HJ. 2000. Primer3 on the WWW for general users and for biologist programmers. Methods Mol Biol 132:365-386.
37. Ochman H, Selander RK. 1984. Standard reference strains of Escherichia coli from natural populations. J Bacteriol 157:690-693.
38. Hazen TH, Sahl JW, Redman JC, Morris CR, Daugherty SC, Chibucos MC, Sengamalay NA, Fraser-Liggett CM, Steinsland H, Whittam TS, Whittam B, Manning SD, Rasko DA. 2012. Draft genome sequences of the diarrheagenic Escherichia coli collection. J Bacteriol 194:3026-3027. http://dx.doi.org/10.1128/JB.00426-12.
39. Hazen TH, Sahl JW, Fraser CM, Donnenberg MS, Scheutz F, Rasko DA. 15 July 2013, posting date. Refining the pathovar paradigm via phylogenomics of the attaching and effacing Escherichia coli. Proc Natl Acad Sci U S A http://dx.doi.org/10.1073/pnas.1306836110.
40. Rasko DA, Myers GS, Ravel J. 2005. Visualization of comparative genomic analyses by BLAST score ratio. BMC Bioinformatics 6:2. http://dx.doi.org/10.1186/1471-2105-6-2.
41. Hyatt D, Chen GL, Locascio PF, Land ML, Larimer FW, Hauser LJ. 2010. Prodigal: prokaryotic gene recognition and translation initiation site identification. BMC Bioinformatics 11:119. http://dx.doi.org/10.1186/1471-2105-11-119.
42. Cock PJ, Antao T, Chang JT, Chapman BA, Cox CJ, Dalke A, Friedberg I, Hamelryck T, Kauff F, Wilczynski B, De Hoon MJ. 2009. Biopython: freely available Python tools for computational molecular biology and bioinformatics. Bioinformatics 25:1422-1423. http://dx.doi.org/10.1093/bioinformatics/btp163.
43. Edgar RC. 2010. Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26:2460-2461. http://dx.doi.org/10.1093/bio informatics/btq461.
44. Rasko DA, Rosovitz MJ, Myers GS, Mongodin EF, Fricke WF, Gajer P, Crabtree J, Sebaihia M, Thomson NR, Chaudhuri R, Henderson IR, Sperandio V, Ravel J. 2008. The pangenome structure of Escherichia coli: comparative genomic analysis of E. Coli commensal and pathogenic isolates. J Bacteriol 190:6881-6893. http://dx.doi.org/10.1128/JB.00619-08.
45. Sahl JW, Caporaso JG, Rasko DA, Keim P. 2014. The large-scale blast score ratio (LS-BSR) pipeline: a method to rapidly compare genetic content between bacterial genomes. PeerJ 2:e332. http://dx.doi.org/10.7717/peerj.332.
46. Touchon M, Hoede C, Tenaillon O, Barbe V, Baeriswyl S, Bidet P, Bingen E, Bonacorsi S, Bouchier C, Bouvet O, Calteau A, Chiapello H, Clermont O, Cruveiller S, Danchin A, Diard M, Dossat C, Karoui ME, Frapy E, Garry L, Ghigo JM, Gilles AM, Johnson J, Le Bouguenec C, Lescat M, Mangenot S, Martinez-Jehanne V, Matic I, Nassif X, Oztas S, Petit MA, Pichon C, Rouy Z, Ruf CS, Schneider D, Tourret J, Vacherie B, Vallenet D, Medigue C, Rocha EP, Denamur E. 2009. Organised genome dynamics in the Escherichia coli species results in highly diverse adaptive paths. PLoS Genet 5:e1000344. http://dx.doi.org/10.1371/journal.pgen. 1000344.
47. Gordienko EN, Kazanov MD, Gelfand MS. 2013. Evolution of pangenomes of Escherichia coli, Shigella spp., and Salmonella enterica. J Bacteriol 195:2786-2792. http://dx.doi.org/10.1128/JB.02285-12.
48. Day WA, Jr, Fernandez RE, Maurelli AT. 2001. Pathoadaptive mutations that enhance virulence: genetic organization of the cadA regions of Shigella spp. Infect Immun 69:7471-7480. http://dx.doi.org/10.1128/IAI.69.12.7471-7480.2001.
49. Payne SM, Wyckoff EE, Murphy ER, Oglesby AG, Boulette ML, Davies NM. 2006. Iron and pathogenesis of Shigella: iron acquisition in the intracellular environment. Biometals 19:173-180. http://dx.doi.org/10.1007/s10534-005-4577-x.
50. Hershberg R, Tang H, Petrov DA. 2007. Reduced selection leads to accelerated gene loss in Shigella. Genome Biol 8:R164. http://dx.doi.org/10.1186/gb-2007-8-8-r164.
51. Walters LL, Raterman EL, Grys TE, Welch RA. 2012. Atypical Shigella boydii 13 encodes virulence factors seen in attaching and effacing Escherichia coli. FEMS Microbiol Lett 328:20-25. http://dx.doi.org/10.1111/j.1574-6968.2011.02469.x.
52. Ogura Y, Ooka T, Iguchi A, Toh H, Asadulghani M, Oshima K, Kodama T, Abe H, Nakayama K, Kurokawa K, Tobe T, Hattori M, Hayashi T. 2009. Comparative genomics reveal the mechanism of the parallel evolution of O157 and non-O157 enterohemorrhagic Escherichia coli. Proc Natl Acad Sci U S A 106:17939-17944. http://dx.doi.org/10.1073/pnas.0903585106.
53. Sims GE, Kim SH. 2 May 2011, posting date. Whole-genome phylogeny of Escherichia coli/Shigella group by feature frequency profiles (FFPs). Proc Natl Acad Sci U S A http://dx.doi.org/10.1073/pnas.1105168108.
54. Wiley EO. 1978. The evolutionary species concept reconsidered. Syst Zool 27(1):17-26.
55. Frankel G, Riley L, Giron JA, Valmassoi J, Friedmann A, Strockbine N, Falkow S, Schoolnik GK. 1990. Detection of Shigella in feces using DNA amplification. J Infect Dis 161:1252-1256. http://dx.doi.org/10.1093/infdis/161.6.1252.
56. Farfán MJ, Garay TA, Prado CA, Filliol I, Ulloa MT, Toro CS. 2010. A new multiplex PCR for differential identification of Shigella flexneri and Shigella sonnei and detection of Shigella virulence determinants. Epidemiol Infect 138:525-533. http://dx.doi.org/10.1017/S0950268809990823.
57. Vu DT, Sethabutr O, Von Seidlein L, Tran VT, Do GC, Bui TC, Le HT, Lee H, Houng HS, Hale TL, Clemens JD, Mason C, Dang DT. 2004. Detection of Shigella by a PCR assay targeting the ipaH gene suggests increased prevalence of shigellosis in Nha Trang, Vietnam. J Clin Microbiol 42:2031-2035. http://dx.doi.org/10.1128/JCM.42.5.2031-2035.2004.
58. Lindsay B, Ochieng JB, Ikumapayi UN, Toure A, Ahmed D, Li S, Panchalingam S, Levine MM, Kotloff K, Rasko DA, Morris CR, Juma J, Fields BS, Dione M, Malle D, Becker SM, Houpt ER, Nataro JP, Sommerfelt H, Pop M, Oundo J, Antonio M, Hossain A, Tamboura B, Stine OC. 2013. Quantitative PCR for detection of Shigella improves ascertainment of Shigella burden in children with moderate-to-severe diarrhea in low-income countries. J Clin Microbiol 51:1740-1746. http://dx.doi.org/10.1128/JCM.02713-12.
59. Moran NA. 2002. Microbial minimalism: genome reduction in bacterial pathogens. Cell 108:583-586. http://dx.doi.org/10.1016/S0092-8674 (02) 00665-7.
60. Lan R, Reeves PR. 2002. Escherichia coli in disguise: molecular origins of Shigella. Microbes Infect 4:1125-1132. http://dx.doi.org/10.1016/S1286-4579 (02) 01637-4.