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Molecular Population Genetic Analysis of Emerged Bacterial Pathogens: Selected Insights James M Perspective Molecular Population Genetic Analysis of Emerged Bacterial Pathogens: Selected Insights James M. Musser, M.D., Ph.D. Department of Pathology, Baylor College of Medicine, Houston, Texas, USA Research in bacterial population genetics has increased in the last 10 years. Population genetic theory and tools and related strategies have been used to investigate bacterial pathogens that have contributed to recent episodes of temporal variation in disease fre- quency and severity. A common theme demonstrated by these analyses is that distinct bacterial clones are responsible for disease outbreaks and increases in infection frequency. Many of these clones are characterized by unique combinations of virulence genes or alleles of virulence genes. Because substantial interclonal variance exists in relative virulence, molecular population genetic studies have led to the concept that the unit of bacterial pathogenicity is the clone or cell line. Continued new insights into host–parasite interactions at the molecular level will be achieved by combining clonal analysis of bacterial pathogens with large-scale comparative sequencing of virulence genes. To avert the threat of resurgent and new micro- students of the molecular evolutionary processes bial diseases, it is critical to gain insight into the in higher eukaryotic organisms. Bacteria were an molecular mechanisms contributing to temporal attractive group of experimental organisms be- variation in disease frequency and severity. Al- cause of their phenotypic diversity, short genera- though comprehensive, unambiguous under- tion times, haploid chromosomal genomes, and standing of the host and parasite factors accessory genetic elements. Hence, bacterial mediating these processes is not available for any population genetic research was originated by infectious agent, population genetic research in population geneticists interested in bacteria, the last 10 years has provided noteworthy new rather than bacterial geneticists or medical micro- information about the bacterial side of the equa- biologists interested in population genetics (1, 2). tion. This review will summarize the insights ac- In spite of its important implications for how the crued from population genetic analysis of bacteria field has developed over the last decade, this on- responsible for disease outbreaks or increases in togeny will not be discussed in detail here. How- infection frequency and severity. One of the pri- ever, the reader should recognize that bacterial mary themes emerging from this research is that population genetics is a discipline separate and distinct bacterial clones have been responsible for distinct from the study of the molecular epidemiol- several infection outbreaks (Table 1). Moreover, ogy of infectious agents. The research tools, meth- the distinct clones are frequently characterized by ods of data analysis, and general thought unique combinations of virulence genes or alleles of virulence genes. These observations have im- processes are very different from the typological portant implications for our understanding of in- thinking used by investigators of disease out- fectious diseases and the public health measures breaks or microbial pathogenesis (3-6). required to reduce their detrimental and poten- Early work on the clonal nature of bacterial tially devastating effect on society. pathogens was conducted largely with Escherichia coli, through a framework supplied by serotyping of one or a few polymorphic surface antigens (7, 8). Population Genetics and Clonal Analysis of Only a few of the many possible O and H antigen Bacterial Pathogens: Basic Concepts serotypes were frequently associated with out- Population genetic study of bacterial pathogens breaks of infantile diarrhea in the United arose largely as an offshoot of research designed Kingdom and other countries, which suggested to address questions of longstanding interest to that isolates expressing these traits had special virulence properties (7-9). Because serotype Address for correspondence: James M. Musser, M.D., Ph.D., Department of Pathology, Baylor College of Medicine, One analysis of relatively few surface structures does Baylor Plaza, Houston, TX 77030 USA; fax 713-798-4595; not provide robust data for estimating overall Vol. 2, No. 1 — January-March 1996 1 Emerging Infectious Diseases Perspective Table 1. Representative Emerged Bacterial Pathogens Investigated with Molecular Population and other microbial Genetic Strategies pathogens provides a convenient strategy Organism Disease Reference for indexing overall Borrelia species Lyme disease 146-149,150,151 levels of chromosomal Escherichia coli O157:H7 hemorrhagic colitis; diversity in the sample hemolytic uremic syndrome 33-35 and for inferring ge- Haemophilus influenzae Invasive disease 156 netic relationships H. influenzae among strains. Be- biogroup aegyptius Brazilian purpuric fever 25,26 cause of the strong cor- Listeria monocytogenes Food-borne invasive disease 157, 158 relation of chromo- Mycobacterium tuberculosis Tuberculosis 91,105 somal divergence in- Neisseria meningitidis Sepsis, meningitis 52-63,66,69-73 dexed by multilocus Salmonella species Food-borne illness 159-161 enzyme electro- Staphylococcus aureus Toxic shock syndrome; phoretic data and methicillin resistant strains 47,143,144 DNA-DNA hybridiza- Streptococcus pyogenes Invasive disease, tion studies (15-18), toxic-shock-like syndrome 82,83,85 several cryptic species S.pneumoniae Otitis, pneumonia, sepsis, have been identified meningitis 125-131,136 once their existence Vibrio cholerae Cholera 153-155 was initially discov- ered by population ge- netic analyses that levels of chromosomal diversity and relationships employed starch gel electrophoresis (16, 19-21). In among strains, the primary research tool used to most bacterial species, the number of allelic vari- examine the population genetics of emerging bac- ants is large, and it is unlikely that recombina- terial pathogens has been multilocus enzyme elec- tional processes would, by chance, frequently trophoresis (10, 11). This technique indexes allelic generate strains with the identical electromorph variation in sets of randomly selected structural profile. Hence, organisms with the same electro- genes located on the chromosome and provides a morph profile are generally thought to be similar basis for estimating overall levels of genotypic by descent, rather than by convergence through variation in populations, i.e., the sample of bacte- lateral gene flow. ria chosen for analysis. The key concept underly- Recently, convenient, rapid, and relatively inex- ing use of starch gel-based protein electrophoresis pensive large-scale DNA sequencing techniques in population genetics is that electromorphs (mo- have also been adopted by several laboratories. bility variants) of an enzyme can be directly Large-scale automated DNA sequencing has been equated with alleles of the corresponding struc- used to rapidly and unambiguously identify a tural gene. Moreover, electromorph profiles over a causative infectious agent and confirm or refute sample of different enzymes, therefore, correspond the identity of isolates recovered from temporally- to multilocus enzyme genotypes and are fre- linked patients thought to be involved in a disease quently referred to as electrophoretic types or ETs. outbreak. In addition, sequence-based studies The proteins analyzed are usually metabolic en- have been employed to define the nature and zymes expressed by virtually all isolates of a spe- extent of allelic variation in toxin and other viru- cies under the growth conditions used. The allelic lence factor genes and to rapidly identify muta- variation detected is unaltered by environmental tions associated with antimicrobial agent conditions such as culture conditions, laboratory resistance (22). storage, anatomic site of recovery, or specific clini- Unless noted, data on the population genetic cal disease. Allelic variation in these metabolic analysis of emerging bacterial pathogens summa- enzymes is selectively neutral, or nearly so, which rized in this article were generated by multilocus means that convergence to the same allele through enzyme electrophoresis, sometimes performed in adaptive evolution is unlikely (4, 12-14). As a con- concert with automated DNA sequencing. sequence, this approach to the study of bacterial Emerging Infectious Diseases 2 Vol. 2, No. 1 — January-March 1996 Perspective Representative Insights spawned from a much larger base population of diverse nonpathogenic precursor clones. Accord- ing to this hypothesis, acquisition or loss of one or Brazilian Purpuric Fever more genes (or, perhaps, a shift in ecological niche) Brazilian purpuric fever (BPF), a serious inva- may produce a pathogenic form with the charac- sive disease of children, was first characterized in teristic viscerotropism for human conjunctivae. 1984 after an outbreak in Promissao, Sao Paulo Although population genetic analysis did not State, Brazil. Children with BPF have acute onset provide a simple reason for the BPF outbreak, the of fever and usually die within 48 h with dissemi- demonstration that the causative clone of bi- nated purpura, vascular collapse, and hypotensive ogroup aegyptius was highly differentiated from shock (23). BPF is caused by Haemophilus influ- other phenotypically similar organisms provided enzae biogroup aegyptius, an organism associated an explanation for the unique infection manifesta- with sporadic or epidemic conjunctivitis (24). Mul-
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