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The Yersiniae — a Model Genus to Study the Rapid Evolution of Bacterial Pathogens

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The Yersiniae — a Model Genus to Study the Rapid Evolution of Bacterial Pathogens REVIEWS THE YERSINIAE — A MODEL GENUS TO STUDY THE RAPID EVOLUTION OF BACTERIAL PATHOGENS Brendan W.Wren Yersinia pestis, the causative agent of plague, seems to have evolved from a gastrointestinal pathogen, Yersinia pseudotuberculosis, in just 1,500–20,000 years an ‘eye blink’ in evolutionary time. The third pathogenic Yersinia, Yersinia enterocolitica, also causes gastroenteritis but is distantly related to Y. pestis and Y. pseudotuberculosis. Why do the two closely related species cause remarkably different diseases, whereas the distantly related enteropathogens cause similar symptoms? The recent availability of whole-genome sequences and information on the biology of the pathogenic yersiniae have shed light on this paradox, and revealed ways in which new, highly virulent pathogens can evolve. ENTEROPATHOGENIC The yersiniae are Gram-negative bacteria that belong to This review covers emerging themes from the Describes a pathogen that the family Enterobacteriaceae. They consist of 11 species genome sequences of the pathogenic yersiniae and dis- resides in the gastrointestinal that have traditionally been distinguished by cusses how this information is guiding hypotheses on tract. DNA–DNA hybridization and biochemical analyses1–4. the evolution of this genus. PANDEMIC Three of them are pathogenic to humans: Yersinia pestis The worldwide spread of an and the ENTEROPATHOGENIC yersiniae, Yersinia pseudotu- Yersinia pestis — the causative agent of plague epidemic. berculosis and Yersinia enterocolitica.All three species Y. pestis has been responsible for three human PANDEMICS target the lymph tissues during infection and carry a — the Justinian plague (fifth to seventh centuries), the 70-kb virulence plasmid (pYV), which is essential for Black Death (thirteenth to fifteenth centuries) and infection in these tissues, as well as to overcome host modern plague (1870s to the present day)1,3.The Black defence mechanisms1–4. Death alone is estimated to have claimed the lives of Elegant population genetics studies have indicated one-third of the European population, and has shaped that Y. pestis recently evolved from Y. pseudotuberculosis the development of modern civilization. Plague is still — just 1,500–20,000 years ago5.However,Y. pestis has a with us, circulating in various mammalian species on very different ecology and epidemiology to the entero- most continents (FIG. 1).The recent identification of pathogenic yersiniae, and causes a markedly different multidrug resistant strains6 and the possibility that it disease. From a mammalian enteropathogen that is could be used as an agent of biological warfare, mean widely found in the environment, it has rapidly trans- that plague still poses a significant threat to human formed into a blood-borne pathogen that is also able to health. An effective vaccine that induces long-lived Department of Infectious parasitize insects and cause systemic disease. The varied immunity against bubonic and pneumonic plagues is and Tropical Diseases, ecology, pathogenicity and host range of these related still not available. London School of Hygiene species, together with the availability of mouse models Y. pestis has a complex life cycle involving a mam- and Tropical Medicine, for both gastroenteritis and plague that mimic human malian reservoir (primarily rodents) and a flea vector1,3 London WC1E 7HT,UK. disease, and the relative ease of constructing defined (FIG. 2).The bacterium ensures transmission by forming e-mail: brendan.wren@ lshtm.ac.uk mutants, make the yersiniae a model genus in which to a cohesive aggregate that blocks the foregut of infected doi:10.1038/nrmicro730 study the genetics and evolution of bacterial pathogens. fleas7. This results in futile attempts to feed on a new NATURE REVIEWS | MICROBIOLOGY VOLUME 1 | OCTOBER 2003 | 55 © 2003 Nature PublishingGroup REVIEWS 2 3 Countries that reported plague, 1970–1998 1 Regions where plague occurs in animals 1 Justinian plague (5th–7th century) 2 Black Death (13th–15th century) 3 Modern plague (1870s onwards) Figure 1 | World distribution of plague, 1998. Modified from REF.5 (1999) National Academy of Sciences. host as a blocked flea regurgitates infected blood back contaminated food or water. After ingestion, the bacte- into the bite site, effectively injecting the bacteria under ria pass into the small intestine, where they translocate the animal’s skin7. On infection, some of the bacilli are across the intestinal epithelium through Peyer’s engulfed by macrophages and carried to the regional patches (FIG. 2).They then migrate to the mesenteric lymph nodes, draining the infection site. The bulk of the lymph nodes and are subsequently found in the liver bacteria, protected by plasminogen activator, penetrate and spleen, where they replicate externally to the host tissue, eventually accessing the lymphatic vessels that cells12.After multiplication, rapid inflammation drain regional lymph nodes8,where they multiply, giv- ensues, which gives rise to the symptoms that are ing rise to the classical symptoms of infection and then associated with gastroenteritis, such as mesenteric BACTERAEMIA1,3.This is known as bubonic plague. If the lymphadentis and terminal ileitis. infection then progresses to the lungs, pneumonic plague Y. enterocolitica comprises a biochemically and genet- develops, which is highly infectious and rapidly fatal. ically heterogeneous collection of organisms that has There are three recognized subgroups, or BIOVARS,of been divided into six biogroups — known as 1A, 1B, 2, 3, Y. pestis:Antiqua, Mediaevalis and Orientalis. They are 4 and 5 — that can be differentiated by biochemical tests. differentiated by their abilities to ferment glycerol and to These can be placed into three lineages: a non-pathogenic reduce nitrate, but these differences do not seem to cor- group (biogroup 1A); a weakly pathogenic group that is relate with virulence. Based on epidemiological obser- unable to kill mice (biogroups 2 to 5); and a highly path- vations and historical records, each biovar has been ogenic, mouse-lethal group (biogroup 1B). Biogroup 1A BACTERAEMIA associated with one of the three pandemics. Biovar lacks the Yersinia virulence plasmid pYV and seems to be A bacterial infection of the Antiqua is resident in Africa and is descended from bac- distantly related to the other biogroups, whereas bio- blood and/or lymphatic system. teria that caused the Justinian plague; biovar Mediaevalis group 1B forms a geographically distinct group of is resident in central Asia and is descended from bacteria strains13 that are frequently isolated in North America BIOVAR The phenotypical distinction that caused the Black Death; and biovar Orientalis, (the so-called ‘New-World’strains) and biogroups 2 to 5 of bacteria in the same species which at present is widespread, is associated with mod- are predominantly isolated in Europe and Japan (‘Old- based on biological tests, such as ern plague9.The factors influencing the rise and fall of World’ strains). Y. pseudotuberculosis is subgrouped into simple biochemical and/or plague EPIDEMICS remain obscure, but it is possible that 21 different serological groups based on variations in the enzymatic differences. severe epidemics could be preceded by subtle genetic O-ANTIGEN of its lipopolysaccharide (LPS). All Y. pestis EPIDEMIC changes in Y. pestis that result in a highly virulent strain. strains fail to express an O-antigen. The rapid spread of an One of the aims of the Y. pestis CO92 biovar Orientalis infectious disease in a defined and Y. pestis KIM10 biovar Mediaevalis genome The Yersinia pestis genome recipe geographical area. projects10,11 was to identify these key genetic changes. The first Yersinia strain to be sequenced was Y. pestis 10 O-ANTIGEN CO92 biovar Orientalis .The CO92 strain was origi- The lipopolysaccharide surface Enteropathogenic yersiniae nally isolated in 1992 from a veterinarian in Colorado, antigen that is present in most The enteropathogenic yersiniae are found widely in the USA, who was infected by a sneezing cat. The genome Gram-negative bacteria. It is environment — for example, in soil — and are a com- consists of a 4.65-Mb chromosome and three plasmids often used as a convenient mon cause of animal infections, affecting several — pMT1 or pFra (96.2 kb), pYV or pCD (70.3 kb), and immunological test to 2,4 distinguish between bacteria of mammalian and avian species .In humans, the infec- pPla or pPCP1 (9.6 kb) (TABLE 1).Close inspection of the the same species. tion causes gastroenteritis after the consumption of chromosome sequence indicates that it has undergone 56 | OCTOBER 2003 | VOLUME 1 www.nature.com/reviews/micro © 2003 Nature PublishingGroup REVIEWS genetic material that is acquired often contributes to an Bite from organism’s virulence — for example, by broadening its infected host range, improving its ability to overcome host flea defences or to cause tissue damage. The proceess of LATERAL GENE TRANSFER allows microbial pathogens to Y. pestis evolve extremely rapidly, in ‘quantum leaps’. Lymph node Plasmid acquisition seems to be a key element in the Lymph node evolutionary jump of Y. pestis from an enteric pathogen Mesenteric lymph nodes to a flea-transmitted systemic pathogen. In addition to the virulence plasmid pYV that is common to all patho- Bubonic plague Ingested Y. enterocolitica genic yersiniae, most Y. pestis strains have two further or Y. pseudotuberculosis plasmids — pPla that encodes the plasminogen activa- tor Pla14, and pMT1 that encodes the putative murine toxin Ymt and the F1 capsule. The precise role of these determinants in host adaptation and virulence is unclear, but there are several indications that they are Blood M cell in small involved in transmission. Pla, for example, is important intestine for dissemination of Y. pestis after subcutaneous injec- tion into a mammalian host15, and although capsule- Macrophage deficient mutants can still cause disease in humans16, Y. pestis Y. pestis strains that lack the entire pMT1 plasmid are in respiratory unable to colonize fleas17.Recently, Hinnebusch et al. droplets Lymph node have shown that the murine toxin Ymt acts as an intra- cellular phospholipase D and is required for the survival of Y.
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