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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

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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. 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 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
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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 strains to pathogenic strains and The three major clusters of are shown boxed. serotypes 1, 8, and 10 fall outside the three main clusters (but within the population structure of ) and are not shown on this tree. ECOR, reference strain. Adapted from reference 28.
10.1128/9781555815622/f0113-01_thmb.gif
10.1128/9781555815622/f0113-01.gif
Image of FIGURE 1
FIGURE 1

Genetic relationships of commensal strains to pathogenic strains and The three major clusters of are shown boxed. serotypes 1, 8, and 10 fall outside the three main clusters (but within the population structure of ) and are not shown on this tree. ECOR, 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
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/content/10.1128/9781555815622.ch06.ch06fig02
FIGURE 2
Novel genetic organization resulting from the pathoadaptive mutations in four lineages. Gene loci are depicted as arrows, insertion sequences as black rectangles, and the 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 locus to facilitate comparison. The locations (in kilo-base pairs) of , and ‘ on the K-12 chromosome are indicated below each ORF. The 1 operon, which is displaced and not linked to , is depicted below the region CCW to . Reprinted from reference .
10.1128/9781555815622/f0115-01_thmb.gif
10.1128/9781555815622/f0115-01.gif
Image of FIGURE 2
FIGURE 2

Novel genetic organization resulting from the pathoadaptive mutations in four lineages. Gene loci are depicted as arrows, insertion sequences as black rectangles, and the 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 locus to facilitate comparison. The locations (in kilo-base pairs) of , and ‘ on the K-12 chromosome are indicated below each ORF. The 1 operon, which is displaced and not linked to , is depicted below the region CCW to . Reprinted from reference .

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
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Download as Powerpoint
/content/10.1128/9781555815622.ch06.ch06fig03
FIGURE 3
Model of the evolution of from an ancestral Horizontal gene transfer and pathoadaptive mutation events are shown. SHI-1 and SHI-2 are the pathogenicity islands located on the chromosome. and represent the genes for lysine decarboxylase and synthesis of curli, respectively.
10.1128/9781555815622/f0119-01_thmb.gif
10.1128/9781555815622/f0119-01.gif
Image of FIGURE 3
FIGURE 3

Model of the evolution of from an ancestral Horizontal gene transfer and pathoadaptive mutation events are shown. SHI-1 and SHI-2 are the pathogenicity islands located on the chromosome. and 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
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