Comparative phylogenomics and evolution of the brucellae reveal a path to virulence

Journal of Bacteriology

Volumn 196, Issue 5, 2014, Pages 920-930

  Wattam, Alice R ^a   Foster, Jeffrey T ^b   Mane, Shrinivasrao P ^a   Beckstrom Sternberg, Stephen M ^b,c   Beckstrom Sternberg, James M ^b,c   Dickerman, Allan W ^a   Keim, Paul ^b,c   Pearson, Talima ^b   Shukla, Maulik ^a   Ward, Doyle V ^d   Williams, Kelly P ^a   Sobral, Bruno W ^a   Tsolis, Renee M ^e   Whatmore, Adrian M ^f   O'Callaghan, David ^g,h  

^a VIRGINIA BIOINFORMATICS INSTITUTE   (United States)

^b NORTHERN ARIZONA UNIVERSITY   (United States)

^c TRANSLATIONAL GENOMICS RESEARCH INSTITUTE   (United States)

^d BROAD INSTITUTE OF MIT AND HARVARD   (United States)

^e UNIVERSITY OF CALIFORNIA   (United States)

^f VETERINARY LABORATORIES AGENCY   (United Kingdom)

^g CHU Nîmes   (France)

^h UNIV MONTPELLIER   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEINS; BIOLOGICAL EVOLUTION; BRUCELLACEAE; GENE EXPRESSION REGULATION, BACTERIAL; GENOME, BACTERIAL; GENOMICS; PHYLOGENY; VIRULENCE;

EID: 84893808883     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.01091-13     Document Type: Article

References (71)

1. Batut J, Andersson SG, O'Callaghan D. 2004. The evolution of chronic infection strategies in the alpha-proteobacteria. Nat. Rev. Microbiol. 2:933-945. http://dx.doi.org/10.1038/nrmicro1044.
2. Andersson SG, Kurland CG. 1998. Reductive evolution of resident genomes. Trends Microbiol. 6:263-268. http://dx.doi.org/10.1016/S0966 -842X(98)01312-2.
3. Losada L, Ronning CM, DeShazer D, Woods D, Fedorova N, Stanley Kim H, Shabalina SA, Pearson TR, Brinkac L, Tan Nandi PT, Crabtree J, Badger J, Beckstrom-Sternberg S, Saqib M, Schutzer SE, Keim P, Nierman WC. 2010. Continuing evolution of Burkholderia mallei through genome reduction and large-scale rearrangements. Genome Biol. Evol. 2:102-116. http://dx.doi.org/10.1093/gbe/evq003.
4. Song H, Hwang J, Yi H, Ulrich RL, Yu Y, Nierman WC, Kim HS 2010. The early stage of bacterial genome-reductive evolution in the host. PLoS Pathog. 6:e1000922. http://dx.doi.org/10.1371/journal.ppat.1000922.
5. O'Callaghan D, Whatmore AM. 2011. Brucella genomics as we enter the multi-genome era. Brief. Funct. Genomics 10:334-341. http://dx.doi.org /10.1093/bfgp/elr026.
6. de Jong MF, Tsolis RM. 2012. Brucellosis and type IV secretion. Future Microbiol. 7:47-58. http://dx.doi.org/10.2217/fmb.11.136.
7. Eisenberg T, Hamann HP, Kaim U, Schlez K, Seeger H, Schauerte N, Melzer F, Tomaso H, Scholz HC, Koylass MS, Whatmore AM, Zschöck M. 2012. Isolation of potentially novel Brucella spp. from frogs. Appl. Environ. Microbiol. 78:3753-3755. http://dx.doi.org/10.1128 /AEM.07509-11.
8. Michaux-Charachon S, Bourg G, Jumas-Bilak E, Guigue-Talet P, Allardet-Servent A, O'Callaghan D, Ramuz M. 1997. Genome structure and phylogeny in the genus Brucella. J. Bacteriol. 179:3244-3249.
9. Moreno E, Cloeckaert A, Moriyon I. 2002. Brucella evolution and taxonomy. Vet. Microbiol., 90:209-227. http://dx.doi.org/10.1016/S0378 -1135(02)00210-9.
10. Bourg G, O'Callaghan D, Boschiroli ML. 2007. The genomic structure of Brucella strains isolated from marine mammals gives clues to evolutionary history within the genus. Vet. Microbiol. 125:375-380. http://dx.doi.org /10.1016/j.vetmic.2007.06.002.
11. Whatmore AM, Murphy TJ, Shankster S, Young E, Cutler SJ, Mac-Millan AP. 2005. Use of amplified fragment length polymorphism to identify and type Brucella isolates of medical and veterinary interest. J. Clin. Microbiol. 43:761-769. http://dx.doi.org/10.1128/JCM.43.2.761 -769.2005.
12. Gillespie JJ, Wattam AR, Cammer SA, Gabbard JL, Shukla MP, Dalay O, Driscoll T, Hix D, Mane SP, Mao Nordberg CEK, Scott M, Schulman JR, Snyder EE, Sullivan DE, Wang C, Warren A, Williams KP, Xue T, Yoo HS, Zhang C, Zhang Y, Will R, Kenyon RW, Sobral BW. 2011. PATRIC: the comprehensive bacterial bioinformatics resource with a focus on human pathogenic species. Infect. Immun. 79:4286-4298. http: //dx.doi.org/10.1128/IAI.00207-11.
13. Wattam AR, Abraham D, Dalay O, Disz TL, Driscoll T, Gabbard JL, Gillespie JJ, Gough R, Hix D, Kenyon R, Machi D, Mao C, Nordberg EK, Olson R, Overbeek R, Pusch GD, Shukla M, Schulman J, Stevens RL, Sullivan DE, Vonstein V, Warren A, Will R, Wilson MJ, Yoo HS, Zhang C, Zhang Y, Sobral BW. 2014. PATRIC, the bacterial bioinformatics database and analysis resource. Nucleic Acids Res. 42:D581-D591. http://dx.doi.org/10.1093/nar/gkt1099.
14. Overbeek R, Olson R, Pusch GD, Olsen GJ, Davis JJ, Disz T, Edwards RA, Gerdes S, Parrello B, Shukla M, Vonstein V, Wattam AR, Xia F, Stevens R. 2014. The SEED and the Rapid Annotation of microbial genomes using Subsystems Technology (RAST). Nucleic Acids Res. 42: D206-D214. http://dx.doi.org/10.1093/nar/gkt1226.
15. Meyer F, Overbeek R, Rodriguez A. 2009. FIGfams: yet another set of protein families. Nucleic Acids Res. 37:6643-6654. http://dx.doi.org/10 .1093/nar/gkp698.
16. Li L, Stoeckert CJ, Jr, Roos, DS. 2003. OrthoMCL: identification of ortholog groups for eukaryotic genomes. Genome Res. 13:2178-2189. http://dx.doi.org/10.1101/gr.1224503.
17. Delcher AL, Phillippy A, Carlton J, Salzberg SL. 2002. Fast algorithms for large-scale genome alignment and comparison. Nucleic Acids Res. 30:2478-2483. http://dx.doi.org/10.1093/nar/30.11.2478.
18. Kurtz S, Phillippy A, Delcher AL, Smoot M, Shumway M, Antonescu C, Salzberg SL. 2004. Versatile and open software for comparing large genomes. Genome Biol. 5:R12. http://dx.doi.org/10.1186/gb-2004-5-2-r12.
19. Wilgenbusch JC, Swofford D. 2003. Inferring evolutionary trees with PAUP*. Curr.Protoc. Bioinformatics Chapter 6:Unit 6 4.
20. Williams KP, Gillespie JJ, Sobral BW, Nordberg EK, Snyder EE, Shallom JM, Dickerman AW. 2010. Phylogeny of gammaproteobacteria. J. Bacteriol. 192:2305-2314. http://dx.doi.org/10.1128/JB.01480-09.
21. Williams KP, Sobral BW, Dickerman AW. 2007. A robust species tree for the alphaproteobacteria. J. Bacteriol. 189:4578-4586. http://dx.doi.org /10.1128/JB.00269-07.
22. Edgar RC. 2004. MUSCLE: a multiple sequence alignment method with reduced time and space complexity.BMCBioinformatics. 5:113. http://dx .doi.org/10.1186/1471-2105-5-113.
23. Castresana J. 2000. Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol. Biol. Evol. 17:540-552. http://dx.doi.org/10.1093/oxfordjournals.molbev.a026334.
24. Stamatakis A. 2006. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics. 22:2688-2690. http://dx.doi.org/10.1093/bioinformatics/btl446.
25. Mardis E, McPherson J, Martienssen R, Wilson RK, McCombie WR. 2002. What is finished, and why does it matter. Genome Res. 12:669-671. http://dx.doi.org/10.1101/gr.032102.
26. De Ley J, Mannheim W, Segers P, Lievens A, Denijn M, Vanhoucke M, Gillis M. 1987. Ribosomal ribonucleic acid cistron similarities and taxonomic neighborhood of Brucella and CDC group Vd. Int. J. Syst. Bacteriol. 37:35-42. http://dx.doi.org/10.1099/00207713-37-1-35.
27. De BK, Stauffer L, Koylass MS, Sharp SE, Gee JE, Helsel LO, Steigerwalt AG, Vega R, Clark TA, Daneshvar MI, Wilkins PP, Whatmore AM. 2008. Novel Brucella strain (BO1) associated with a prosthetic breast implant infection. J. Clin. Microbiol. 46:43-49. http://dx.doi.org/10.1128 /JCM.01494-07.
28. Tiller RV, Gee JE, Lonsway DR, Gribble S, Bell SC, Jennison AV, Bates J, Coulter C, Hoffmaster AR, De BK. 2010. Identification of an unusual Brucella strain (BO2) from a lung biopsy in a 52 year-old patient with chronic destructive pneumonia. BMC Microbiol. 10:23. http://dx.doi.org /10.1186/1471-2180-10-23.
29. Celli J. 2006. Surviving inside a macrophage: the many ways of Brucella. Res. Microbiol. 157:93-98. http://dx.doi.org/10.1016/j.resmic.2005.10 .002.
30. Barbier T, Nicolas C, Letesson JJ. 2011. Brucella adaptation and survival at the crossroad of metabolism and virulence. FEBS Lett. 585:2929-2934. http://dx.doi.org/10.1016/j.febslet.2011.08.011.
31. Verger JM, Grimont F, Grimont PAD, Grayon M. 1985. Brucella, a monospecific genus as shown by deoxyribonucleic acid hybridization. Int. J. Syst. Bacteriol. 35:292-295. http://dx.doi.org/10.1099/00207713-35-3 -292.
32. Paulsen IT, Seshadri R, Nelson KE, Eisen JA, Heidelberg JF, Read TD, Dodson RJ, Umayam L, Brinkac LM, Beanan MJ, Daugherty SC, Deboy RT, Durkin AS, Kolonay JF, Madupu R, Nelson WC, Ayodeji B, Kraul M, Shetty J, Malek J, Van Aken SE, Riedmuller S, Tettelin H, Gill SR, White O, Salzberg SL, Hoover DL, Lindler LE, Halling SM, Boyle SM, Fraser CM. 2002. The Brucella suis genome reveals fundamental similarities between animal and plant pathogens and symbionts. Proc. Nat. Acad. Sci. U. S. A. 99:13148-13153. http://dx.doi.org/10.1073/pnas.192319099.
33. Overbeek R, Larsen N, Pusch GD, D'Souza M, Selkov E, Jr, Kyrpides N, Fonstein M, Maltsev N, Selkov E. 2000. WIT: integrated system for high-throughput genome sequence analysis and metabolic reconstruction. Nucleic Acids Res. 28:123-125. http://dx.doi.org/10.1093/nar/28.1 .123.
34. O'Callaghan D, Cazevieille C, Allardet-Servent A, Boschiroli ML, Bourg G, Foulongne V, Frutos P, Kulakov Y, Ramuz M. 1999. A homologue of the Agrobacterium tumefaciens VirB and Bordetella pertussis Ptl type IV secretion systems is essential for intracellular survival of Brucella suis. Mol. Microbiol. 33:1210-1220.
35. Schneiker S, Keller M, Droge M, Lanka E, Puhler A, Selbitschka W. 2001. The genetic organization and evolution of the broad host range mercury resistance plasmid pSB102 isolated from a microbial population residing in the rhizosphere of alfalfa. Nucleic Acids Res. 29:5169-5181. http://dx.doi.org/10.1093/nar/29.24.5169.
36. Vizcaino N, Cloeckaert A, Zygmunt MS, Fernandez-Lago L. 2001. Characterization of a Brucella species 25-kilobase DNA fragment deleted from Brucella abortus reveals a large gene cluster related to the synthesis of a polysaccharide. Infect. Immun. 69:6738-6748. http://dx.doi.org/10 .1128/IAI.69.11.6738-6748.2001.
37. Banerji S, Flieger A. 2004. Patatin-like proteins: a new family of lipolytic enzymes present in bacteria. Microbiology 150:522-525. http://dx.doi.org /10.1099/mic.0.26957-0.
38. Buttner D, Noel L, Stuttmann J, Bonas U. 2007. Characterization of the nonconserved hpaB-hrpF region in the hrp pathogenicity island from Xanthomonas campestris pv. vesicatoria. Mol. Plant Microbe Interact. 20: 1063-1074. http://dx.doi.org/10.1094/MPMI-20-9-1063.
39. Porte F, Liautard JP, Kohler S. 1999. Early acidification of phagosomes containing Brucella suis is essential for intracellular survival in murine macrophages. Infect. Immun. 67:4041-4047.
40. Boschiroli ML, Ouahrani-Bettache S, Foulongne V, Michaux-Charachon S, Bourg G, Allardet-Servent A, Cazevieille C, Liautard JP, Ramuz M, O'Callaghan D. 2002. The Brucella suis virB operon is induced intracellularly in macrophages. Proc. Nat. Acad. Sci. U. S. A. 99:1544-1549. http://dx.doi.org/10.1073/pnas.032514299.
41. Valderas MW, Alcantara RB, Baumgartner JE, Bellaire BH, Robertson GT, Ng WL, Richardson JM, Winkler ME, Roop RM, II. 2005. Role of HdeA in acid resistance and virulence in Brucella abortus 2308. Vet. Microbiol. 107:307-312. http://dx.doi.org/10.1016/j.vetmic.2005.01.018.
42. Occhialini A, Jimenez de Bagues MP, Saadeh B, Bastianelli D, Hanna N, De Biase D, Kohler S. 2012. The glutamic acid decarboxylase system of the new species Brucella microti contributes to its acid resistance and to oral infection of mice. J. Infect. Dis. 206:1424-1432. http://dx.doi.org/10 .1093/infdis/jis522.
43. Godfroid F, Cloeckaert A, Taminiau B, Danese I, Tibor A, de Bolle X, Mertens P, Letesson JJ. 2000. Genetic organisation of the lipopolysaccharide O-antigen biosynthesis region of Brucella melitensis 16M (wbk). Res. Microbiol. 151:655-668. http://dx.doi.org/10.1016/S0923-2508(00)90130-X.
44. Zygmunt MS, Blasco JM, Letesson JJ, Cloeckaert A, Moriyon I. 2009. DNA polymorphism analysis of Brucella lipopolysaccharide genes reveals marked differences in O-polysaccharide biosynthetic genes between smooth and rough Brucella species and novel species-specific markers. BMC Microbiol. 9:92. http://dx.doi.org/10.1186/1471-2180-9-92.
45. Wattam AR, Williams KP, Snyder EE, Almeida NF, Jr, Shukla M, Dickerman AW, Crasta OR, Kenyon R, Lu JShallom Yoo JMH, Ficht TA, Tsolis RM, Munk C, Tapia R, Han CS, Detter JC, Bruce D, Brettin TS, Sobral BW, Boyle SM, Setubal JC. 2009. Analysis of ten Brucella genomes reveals evidence for horizontal gene transfer despite a preferred intracellular lifestyle. J. Bacteriol. 191:3569-3579. http://dx.doi.org/10 .1128/JB.01767-08.
46. Rajashekara G, Glasner JD, Glover DA, Splitter GA. 2004. Comparative whole-genome hybridization reveals genomic islands in Brucella species. J. Bacteriol. 186:5040-5051. http://dx.doi.org/10.1128/JB.186.15 .5040-5051.2004.
47. Vizcaino N, Caro-Hernandez P, Cloeckaert A, Fernandez-Lago L. 2004. DNA polymorphism in the omp25/omp31 family of Brucella spp.: identification of a 17-kb inversion in Brucella cetaceae and of a 151-kb genomic island, absent from Brucella ovis, related to the synthesis of smooth lipopolysaccharide. Microbes Infect. 6:821-834. http://dx.doi.org/10.1016/j .micinf.2004.04.009.
48. Wattam AR, Inzana TJ, Williams KP, Mane SP, Shukla M, Almeida NF, Dickerman AW, Mason S, Moriyon I, O'Callaghan D, Whatmore AM, Sobral BW, Tiller RV, Hoffmaster AR, Frace MA, De Castro C, Molinaro A, Boyle SM, De BK, Setubal JC. 2012. Comparative genomics of early-diverging Brucella strains reveals a novel lipopolysaccharide biosynthesis pathway. mBio. 3(5):e00246 -12. http://dx.doi.org/10.1128/mBio .00388-12.
49. Bellaire BH, Elzer PH, Baldwin CL, Roop RM, II. 1999. The siderophore 2,3-dihydroxybenzoic acid is not required for virulence of Brucella abortus in BALB/c mice. Infect. Immun. 67:2615-2618.
50. Bellaire BH, Elzer PH, Hagius S, Walker J, Baldwin CL, Roop RM, II. 2003. Genetic organization and iron-responsive regulation of the Brucella abortus 2,3-dihydroxybenzoic acid biosynthesis operon, a cluster of genes required for wild-type virulence in pregnant cattle. Infect. Immun. 71: 1794-1803. http://dx.doi.org/10.1128/IAI.71.4.1794-1803.2003.
51. Bellaire BH, Elzer PH, Baldwin CL, Roop RM, II. 1999. The siderophore 2,3-dihydroxybenzoic acid is not required for virulence of Brucella abortus in BALB/c mice. Infect. Immun. 67:2615-2618.
52. Gonzalez Carrero MI, Sangari FJ, Aguero J, Garcia Lobo JM. 2002. Brucella abortus strain 2308 produces brucebactin, a highly efficient catecholic siderophore. Microbiology 148:353-360.
53. Anderson ES, Paulley JT, Roop RM, II. 2008. The AraC-like transcriptional regulator DhbR is required for maximum expression of the 2,3-dihydroxybenzoic acid biosynthesis genes in Brucella abortus 2308 in response to iron deprivation. J. Bacteriol. 190:1838-1842. http://dx.doi.org /10.1128/JB.01551-07.
54. Blanc-Potard AB, Lafay B. 2003. MgtC as a horizontally-acquired virulence factor of intracellular bacterial pathogens: evidence from molecular phylogeny and comparative genomics. J. Mol. Evol. 57:479-486. http://dx .doi.org/10.1007/s00239-003-2496-4.
55. Zhang Y, Rodionov DA, Gelfand MS, Gladyshev VN. 2009. Comparative genomic analyses of nickel, cobalt and vitamin B12 utilization. BMC Genomics 10:78. http://dx.doi.org/10.1186/1471-2164-10-78.
56. Sangari FJ, Cayon AM, Seoane A, Garcia-Lobo JM. 2010. Brucella abortus ure2 region contains an acid-activated urea transporter and a nickel transport system. BMC Microbiol. 10:107. http://dx.doi.org/10 .1186/1471-2180-10-107.
57. Jubier-Maurin V, Rodrigue A, Ouahrani-Bettache S, Layssac M, Mandrand-Berthelot MA, Kohler S, Liautard JP. 2001. Identification of the nik gene cluster of Brucella suis: regulation and contribution to urease activity. J. Bacteriol. 183:426-434. http://dx.doi.org/10.1128/JB.183.2 .426-434.2001.
58. Corbel MJ, Hendry DM. 1985. Urease activity of Brucella species. Res. Vet. Sci. 38:252-253.
59. Foster JT, Beckstrom-Sternberg SM, Pearson T, Beckstrom-Sternberg JS, Chain PS, Roberto FF, Hnath J, Brettin T, Keim P. 2009. Wholegenome-based phylogeny and divergence of the genus Brucella. J. Bacteriol. 191:2864-2870. http://dx.doi.org/10.1128/JB.01581-08.
60. Tiller RV, Gee JE, Frace MA, Taylor TK, Setubal JC, Hoffmaster AR, De BK. 2010. Characterization of novel Brucella strains originating from wild native rodent species in North Queensland, Australia. Appl. Environ. Microbiol. 76:5837-5845. http://dx.doi.org/10.1128/AEM.00620-10.
61. Whatmore AM. 2009. Current understanding of the genetic diversity of Brucella, an expanding genus of zoonotic pathogens. Infect. Genet. Evol. 9:1168-1184. http://dx.doi.org/10.1016/j.meegid.2009.07.001.
62. Whatmore AM, Perrett LL, MacMillan AP. 2007. Characterisation of the genetic diversity of Brucella by multilocus sequencing. BMC Microbiol. 7:34. http://dx.doi.org/10.1186/1471-2180-7-34.
63. Audic S, Lescot M, Claverie JM, Cloeckaert A, Zygmunt MS 2011. The genome sequence of Brucella pinnipedialis B2/94 sheds light on the evolutionary history of the genus Brucella.BMCEvol. Biol. 11:200. http://dx.doi .org/10.1186/1471-2148-11-200.
64. Audic S, Lescot M, Claverie JM, Scholz HC. 2009. Brucella microti: the genome sequence of an emerging pathogen. BMC Genomics 10:352. http: //dx.doi.org/10.1186/1471-2164-10-352.
65. Chaudhary A, Ganguly K, Cabantous S, Waldo GS, Micheva-Viteva SN, Nag K, Hlavacek WS, Tung CS. 2012. The Brucella TIR-like protein TcpB interacts with the death domain of MyD88. Biochem. Biophys. Res. Commun. 417:299-304. http://dx.doi.org/10.1016/j.bbrc.2011.11.104.
66. Radhakrishnan GK, Harms JS, Splitter GA. 2011. Modulation of microtubule dynamics by a TIR domain protein from the intracellular pathogen Brucella melitensis. Biochem. J. 439:79-83. http://dx.doi.org/10.1042 /BJ20110577.
67. Radhakrishnan GK, Splitter GA. 2010. Biochemical and functional analysis of TIR domain containing protein from Brucella melitensis. Biochem. Biophys. Res. Commun. 397:59-63. http://dx.doi.org/10.1016/j.bbrc .2010.05.056.
68. Radhakrishnan GK, Yu Q, Harms JS, Splitter GA. 2009. Brucella TIR domain-containing protein mimics properties of the Toll-like receptor adaptor protein TIRAP. J. Biol. Chem. 284:9892-9898. http://dx.doi.org /10.1074/jbc.M805458200.
69. Sengupta D, Koblansky A, Gaines J, Brown T, West AP, Zhang D, Nishikawa T, Park SG, Roop RM, II, Ghosh S. 2010. Subversion of innate immune responses by Brucella through the targeted degradation of the TLR signaling adapter, MAL. J. Immunol. 184:956-964. http://dx.doi .org/10.4049/jimmunol.0902008.
70. Salcedo SP, Marchesini MI, Lelouard H, Fugier E, Jolly G, Balor S, Muller A, Lapaque N, Demaria O, Alexopoulou L, Comerci DJ, Ugalde RA, Pierre P, Gorvel JP. 2008. Brucella control of dendritic cell maturation is dependent on the TIR-containing protein Btp1. PLoS Pathog. 4:e21. http://dx.doi.org/10.1371/journal.ppat.0040021.
71. Cirl C, Wieser A, Yadav M, Duerr S, Schubert S, Fischer H, Stappert D, Wantia N, Rodriguez N, Wagner H, Svanborg C, Miethke T. 2008. Subversion of Toll-like receptor signaling by a unique family of bacterial Toll/interleukin-1 receptor domain-containing proteins. Nat. Med. 14: 399-406. http://dx.doi.org/10.1038/nm1734.