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Chapter 6 : Black Holes and Antivirulence Genes: Selection for Gene Loss as Part of the Evolution of Bacterial Pathogens
Authors:
William A. Day1,
Anthony T. Maurelli2
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Affiliations:
1: Bacteriology Division, U.S. Army Medical Research Institute of Infectious Diseases, Fort Detrick, MD 21702;
2: Department of Microbiology and Immunology, F. Edward Hébert School of Medicine, Uniformed Services University of the Health Sciences, Bethesda, MD 20814-4799
Content Type: Monograph
Publication Year:
2006
Category: Bacterial Pathogenesis; Microbial Genetics and Molecular Biology
Book DOI:
10.1128/9781555815622
Chapter DOI:
10.1128/9781555815622.ch6
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Abstract:
This chapter discusses the concept of gene loss in the evolution of bacterial pathogens from commensals as a mechanism of fine-tuning pathogen genomes for maximal fitness in new host environments. It describes the nature of antivirulence genes and the pressures that drive selection for gene inactivation, and examines how this process complements the mechanisms of pathogen evolution through gene acquisition. Pathoadaptive mutation via gene loss complements bacterial pathogen evolution by gene acquisition. The evolutionary model of antagonistic pleiotrophy predicts that genes required for fitness in one niche may actually inhibit fitness in another environment that presents new selective pressures. “Black holes” in pathogen genomes are formed by inactivation or loss of ancestral genes that are incompatible with, and even antagonistic to, the pathogenic lifestyle. These incompatible genes are defined as antivirulence genes. Shigella serves as a model for pathoadaptive mutation by gene loss and gene inactivation. Converse Koch’s postulates are proposed as criteria for identification of antivirulence genes. New techniques such as phenotypic arrays, comparative genomic hybridization, and transposon site hybridization will improve the ability to identify pathoadaptive mutations in an organism. Pathoadaptive mutations played a critical role in Bacillus anthracis evolution and provide further evidence of the important contribution of the evolutionary pathway in niche adaptation and the generation of maximally fit pathogen clones.
Citation:
Day W, Maurelli A.
2006.
Black Holes and Antivirulence Genes: Selection for Gene Loss as Part of the Evolution of Bacterial Pathogens,
p 109-122.
In
Seifert H, DiRita V (ed),
Evolution of Microbial Pathogens.
ASM Press, Washington, DC.
doi: 10.1128/9781555815622.ch6
Figures
Black Holes and Antivirulence Genes: Selection for Gene Loss as Part of the Evolution of Bacterial Pathogens
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Citation:
Day W, Maurelli A.
2006.
Black Holes and Antivirulence Genes: Selection for Gene Loss as Part of the Evolution of Bacterial Pathogens,
p 109-122.
In
Seifert H, DiRita V (ed),
Evolution of Microbial Pathogens.
ASM Press, Washington, DC.
doi: 10.1128/9781555815622.ch6
/content/10.1128/9781555815622.ch06.ch06fig01
FIGURE 1
Genetic relationships of commensal E. coli strains to pathogenic E. coli strains and Shigella. The three major clusters of Shigella are shown boxed. S. dysenteriae serotypes 1, 8, and 10 fall outside the three main clusters (but within the population structure of E. coli) and are not shown on this tree. ECOR, E. coli reference strain. Adapted from reference 28.
10.1128/9781555815622/f0113-01_thmb.gif
10.1128/9781555815622/f0113-01.gif
FIGURE 1
Genetic relationships of commensal E. coli strains to pathogenic E. coli strains and Shigella. The three major clusters of Shigella are shown boxed. S. dysenteriae serotypes 1, 8, and 10 fall outside the three main clusters (but within the population structure of E. coli) and are not shown on this tree. ECOR, E. coli reference strain. Adapted from reference 28.
Citation:
Day W, Maurelli A.
2006.
Black Holes and Antivirulence Genes: Selection for Gene Loss as Part of the Evolution of Bacterial Pathogens,
p 109-122.
In
Seifert H, DiRita V (ed),
Evolution of Microbial Pathogens.
ASM Press, Washington, DC.
doi: 10.1128/9781555815622.ch6
/content/10.1128/9781555815622.ch06.ch06fig02
FIGURE 2
Novel genetic organization resulting from the cadA pathoadaptive mutations in four Shigella lineages. Gene loci are depicted as arrows, insertion sequences as black rectangles, and the pheU tRNA locus as an inverted triangle; truncated open reading frames (ORFs) and insertion sequences are indicated by an apostrophe. The chromosomal maps are aligned at the yjdC locus to facilitate comparison. The locations (in kilo-base pairs) of kgtP, dsbD, and ‘ytfA on the E. coli K-12 chromosome are indicated below each ORF. The S. dysenteriae 1 cad operon, which is displaced and not linked to yjdC, is depicted below the region CCW to yjdC. Reprinted from reference
4
.
10.1128/9781555815622/f0115-01_thmb.gif
10.1128/9781555815622/f0115-01.gif
FIGURE 2
Novel genetic organization resulting from the cadA pathoadaptive mutations in four Shigella lineages. Gene loci are depicted as arrows, insertion sequences as black rectangles, and the pheU tRNA locus as an inverted triangle; truncated open reading frames (ORFs) and insertion sequences are indicated by an apostrophe. The chromosomal maps are aligned at the yjdC locus to facilitate comparison. The locations (in kilo-base pairs) of kgtP, dsbD, and ‘ytfA on the E. coli K-12 chromosome are indicated below each ORF. The S. dysenteriae 1 cad operon, which is displaced and not linked to yjdC, is depicted below the region CCW to yjdC. Reprinted from reference 4 .
Citation:
Day W, Maurelli A.
2006.
Black Holes and Antivirulence Genes: Selection for Gene Loss as Part of the Evolution of Bacterial Pathogens,
p 109-122.
In
Seifert H, DiRita V (ed),
Evolution of Microbial Pathogens.
ASM Press, Washington, DC.
doi: 10.1128/9781555815622.ch6
/content/10.1128/9781555815622.ch06.ch06fig03
FIGURE 3
Model of the evolution of Shigella from an ancestral E. coli. Horizontal gene transfer and pathoadaptive mutation events are shown. SHI-1 and SHI-2 are the Shigella pathogenicity islands located on the chromosome. cadA and csg represent the genes for lysine decarboxylase and synthesis of curli, respectively.
10.1128/9781555815622/f0119-01_thmb.gif
10.1128/9781555815622/f0119-01.gif
FIGURE 3
Model of the evolution of Shigella from an ancestral E. coli. Horizontal gene transfer and pathoadaptive mutation events are shown. SHI-1 and SHI-2 are the Shigella pathogenicity islands located on the chromosome. cadA and csg represent the genes for lysine decarboxylase and synthesis of curli, respectively.
Citation:
Day W, Maurelli A.
2006.
Black Holes and Antivirulence Genes: Selection for Gene Loss as Part of the Evolution of Bacterial Pathogens,
p 109-122.
In
Seifert H, DiRita V (ed),
Evolution of Microbial Pathogens.
ASM Press, Washington, DC.
doi: 10.1128/9781555815622.ch6
References
/content/book/10.1128/9781555815622.ch06
1.
Bernardini, M. L.,, J. Mounier,, H. d’Hauteville,, M. Coquis-Rondon, and, P. J. Sansonetti. 1989. Identification of icsA, a plasmid locus of Shigella flexneri that governs bacterial intra- and intercellular spread through interaction with F-actin. Proc. Natl. Acad. Sci. USA 86: 3867– 3871.
2.
Brenner, D. J.,, G. R. Fanning,, K. E. Johnson,, R. V. Citarella, and, S. Falkow. 1969. Polynucleotide sequence relationships among members of Enterobacteriaceae. J. Bacteriol. 98: 637– 650.
3.
Cooper, V. S.,, D. Schneider,, M. Blot, and, R. E. Lenski. 2001. Mechanisms causing rapid and parallel losses of ribose catabolism in evolving populations of Escherichia coli B. J. Bacteriol. 183: 2834– 2841.
4.
Day, W. A., Jr.,, R. E. Fernandez, and, A. T. Maurelli. 2001. Pathoadaptive mutations that enhance virulence: genetic organization of the cadA regions of Shigella spp. Infect. Immun. 69: 7471– 7480.
5.
Dobrindt, U.,, F. Agerer,, K. Michaelis,, A. Janka,, C. Buchrieser,, M. Samuelson,, C. Svanborg,, G. Gottschalk,, H. Karch, and, J. Hacker. 2003. Analysis of genome plasticity in pathogenic and commensal Escherichia coli isolates by use of DNA arrays. J. Bacteriol. 185: 1831– 1840.
6.
Dragon, D. C., and, R. P. Rennie. 1995. The ecology of anthrax spores: tough but not invincible. Can. Vet. J. 36: 295– 301.
7.
Ewing, E. H. 1986. Edwards and Ewing’s Identification of Enterobacteriacae, 4th ed. Elsevier Science Publishing Co. Inc., New York, N. Y.
8.
Fernandez, I. M.,, M. Silva,, R. Schuch,, W. A. Walker,, A. M. Siber,, A. T. Maurelli, and, B. A. McCormick. 2001. Cadaverine prevents the escape of Shigella flexneri from the phagolysosome: a connection between bacterial dissemination and neutrophil transepithelial signaling. J. Infect. Dis. 184: 743– 753.
9.
Gophna, U.,, M. Barlev,, R. Seijffers,, T. A. Oelschlager,, J. Hacker, and, E. Z. Ron. 2001. Curli fibers mediate internalization of Escherichia coli by eukaryotic cells. Infect. Immun. 69: 2659– 2665.
10.
Grodberg, J. and, J. J. Dunn. 1988. ompT encodes the Escherichia coli outer membrane protease that cleaves T7 RNA polymerase during purification. J. Bacteriol. 170: 1245– 1253.
11.
Groisman, E. A., and, H. Ochman. 1996. Pathogenicity islands: bacterial evolution in quantum leaps. Cell 87: 791– 794.
12.
Helgason, E.,, O. A. Økstad,, D. A. Caugant,, H. A. Johansen,, A. Fouet,, M. Mock,, I. Hegna, and, A.-B. Kolstø. 2000. Bacillus anthracis, Bacillus cereus, and Bacillus thuringiensis—one species on the basis of genetic evidence. Appl. Environ. Microbiol. 66: 2627– 2630.
13.
Ireland, J. A., and, P. C. Hanna. 2002. Amino acid- and purine ribonucleoside-induced germination of Bacillus anthracis ΔSterne endospores: gerS mediates responses to aromatic ring structures. J. Bacteriol. 184: 1296– 1303.
14.
Jin, Q.,, Z. Yuan,, J. Xu,, Y. Wang,, Y. Shen,, W. Lu,, J. Wang,, H. Liu,, J. Yang,, F. Yang,, X. Zhang,, J. Zhang,, G. Yang,, H. Wu,, D. Qu,, J. Dong,, L. Sun,, Y. Xue,, A. Zhao,, Y. Gao,, J. Zhu,, B. Kan,, K. Ding,, S. Chen,, H. Cheng,, Z. Yao,, B. He,, R. Chen,, D. Ma,, B. Qiang,, Y. Wen,, Y. Hou, and, J. Yu. 2002. Genome sequence of Shigella flexneri 2a: insights into pathogenicity through comparison with genomes of Escherichia coli K12 and O157. Nucleic Acids Res. 30: 4432– 4441.
15.
Lan, R., and, P. R. Reeves. 2002. Escherichia coli in disguise: molecular origins of Shigella. Microbes Infect. 4: 1125– 1132.
16.
Lee, C. A. 1996. Pathogenicity islands and the evolution of bacterial pathogens. Infect. Agents Dis. 5: 1– 7.
17.
Lindsey, D. F.,, D. A. Mullin, and, J. R. Walker. 1989. Characterization of the cryptic lambdoid prophage DLP12 of Escherichia coli and overlap of the DLP12 integrase gene with the tRNA gene argU. J. Bacteriol. 171: 6197– 6205.
18.
Maurelli, A. T.,, R. E. Fernandez,, C. A. Bloch,, C. K. Rode, and, A. Fasano. 1998. “Black holes” and bacterial pathogenicity: a large genomic deletion that enhances the virulence of Shigella spp. and enteroinvasive Escherichia coli. Proc. Natl. Acad. Sci. USA 95: 3943– 3948.
19.
McCormick, B. A.,, M. I. Fernandez,, A. M. Siber, and, A. T. Maurelli. 1999. Inhibition of Shigella flexneri-induced transepithelial migration of polymorphonuclear leucocytes by cadaverine. Cell Microbiol. 1: 143– 155.
20.
Mignot, T.,, M. Mock,, D. Robichon,, A. Landier,, D. Lereclus, and, A. Fouet. 2001. The incompatibility between the PlcR- and AtxA-controlled regulons may have selected a nonsense mutation in Bacillus anthracis. Mol. Microbiol. 42: 1189– 1198.
21.
Moore, R. A.,, S. Reckseidler-Zenteno,, H. Kim,, W. Nierman,, Y. Yu,, A. Tuanyok,, J. Warawa,, D. DeShazer, and, D. E. Woods. 2004. Contribution of gene loss to the pathogenic evolution of Burkholderia pseudomallei and Burkholderia mallei. Infect. Immun. 72: 4172– 4187.
22.
Moss, J. E.,, T. J. Cardozo,, A. Zychlinsky, and, E. A. Groisman. 1999. The selC-associated SHI-2 pathogenicity island of Shigella flexneri. Mol. Microbiol. 33: 74– 83.
23.
Nakata, N.,, T. Tobe,, I. Fukuda,, T. Suzuki,, K. Komatsu,, M. Yoshikawa, and, C. Sasakawa. 1993. The absence of a surface protease, OmpT, determines the intercellular spreading ability of Shigella: the relationship between the ompT and kcpA loci. Mol. Microbiol. 9: 459– 468.
24.
Ochman, H.,, J. G. Lawrence, and, E. A. Groisman. 2000. Lateral gene transfer and the nature of bacterial innovation. Nature 405: 299– 304.
25.
Ochman, H.,, T. S. Whittam,, D. A. Caugant, and, R. K. Selander. 1983. Enzyme polymorphism and genetic population structure in Escherichia coli and Shigella. J. Gen. Microbiol. 129(Pt. 9): 2715– 2726.
26.
Olsen, A.,, A. Arnqvist,, M. Hammar,, S. Sukupolvi, and, S. Normark. 1993. The RpoS sigma factor relieves H-NS-mediated transcriptional repression of csgA, the subunit gene of fibronectin-binding curli in Escherichia coli. Mol. Microbiol. 7: 523– 536.
27.
Olsen, A.,, A. Jonsson, and, S. Normark. 1989. Fibronectin binding mediated by a novel class of surface organelles on Escherichia coli. Nature 338: 652– 655.
28.
Pupo, G. M.,, D. K. Karaolis,, R. Lan, and, P. R. Reeves. 1997. Evolutionary relationships among pathogenic and nonpathogenic Escherichia coli strains inferred from multilocus enzyme electrophoresis and mdh sequence studies. Infect. Immun. 65: 2685– 2692.
29.
Pupo, G. M.,, R. Lan, and, P. R. Reeves. 2000. Multiple independent origins of Shigella clones of Escherichia coli and convergent evolution of many of their characteristics. Proc. Natl. Acad. Sci. USA 97: 10567– 10572.
30.
Purdy, G. E., and, S. M. Payne. 2001. The SHI-3 iron transport island of Shigella boydii 0-1392 carries the genes for aerobactin synthesis and transport. J. Bacteriol. 183: 4176– 4182.
31.
Rajakumar, K.,, C. Sasakawa, and, B. Adler. 1997. Use of a novel approach, termed island probing, identifies the Shigella flexneri she pathogenicity island which encodes a homolog of the immunoglobulin A protease-like family of proteins. Infect. Immun. 65: 4606– 4614.
32.
Rolland, K.,, N. Lambert-Zechovsky,, B. Picard, and, E. Denamur. 1998. Shigella and enteroinvasive Escherichia coli strains are derived from distinct ancestral strains of E. coli. Microbiology 144(Pt. 9): 2667– 2672.
33.
Rose, M., and, B. Charlesworth. 1980. A test of evolutionary theories of senescence. Nature 287: 141– 142.
34.
Sakellaris, H.,, N. K. Hannink,, K. Rajakumar,, D. Bulach,, M. Hunt,, C. Sasakawa, and, B. Adler. 2000. Curli loci of Shigella spp. Infect. Immun. 68: 3780– 3783.
35.
Sansonetti, P. J.,, J. Arondel,, M. Huerre,, A. Harada, and, K. Matsushima. 1999. Interleukin-8 controls bacterial transepithelial translocation at the cost of epithelial destruction in experimental shigellosis. Infect. Immun. 67: 1471– 1480.
36.
Sansonetti, P. J.,, T. L. Hale,, G. J. Dammin,, C. Kapfer,, H. H. Collins, Jr., and, S. B. Formal. 1983. Alterations in the pathogenicity of Escherichia coli K-12 after transfer of plasmid and chromosomal genes from Shigella flexneri. Infect. Immun. 39: 1392– 1402.
37.
Sassetti, C. M.,, D. H. Boyd, and, E. J. Rubin. 2001. Comprehensive identification of conditionally essential genes in mycobacteria. Proc. Natl. Acad. Sci. USA 98: 12712– 12717.
38.
Silva, R. M.,, M. R. Toledo, and, L. R. Trabulsi. 1980. Biochemical and cultural characteristics of invasive Escherichia coli. J. Clin. Microbiol. 11: 441– 444.
39.
Sokurenko, E. V.,, D. L. Hasty, and, D. E. Dykhuizen. 1999. Pathoadaptive mutations: gene loss and variation in bacterial pathogens. Trends Microbiol. 7: 191– 195.
40.
Vokes, S. A.,, S. A. Reeves,, A. G. Torres, and, S. M. Payne. 1999. The aerobactin iron transport system genes in Shigella flexneri are present within a pathogenicity island. Mol. Microbiol. 33: 63– 73.
41.
Woods, D. E. 2002. The use of animal infection models to study the pathogenesis of melioidosis and glanders. Trends Microbiol. 10: 483– 484.
42.
Woods, D. E.,, D. DeShazer,, R. A. Moore,, P. J. Brett,, M. N. Burtnick,, S. L. Reckseidler, and, M. D. Senkiw. 1999. Current studies on the pathogenesis of melioidosis. Microbes Infect. 1: 157– 162.