For the first time, researchers have studied the Black Death bacterium's entire family tree to fully understand how some of the family members evolve to become harmful.
Yersinia enterocolitica colonies growing on XLD agar plates [Credit: CDC]
Contrary to popular belief, the team found pathogenic members of this bacterial family do not share a recent common disease-causing ancestor, but instead, have followed parallel evolutionary paths to become harmful.
The Yersinia family of bacteria has many sub species, some of which are harmful and others not.
Two of the most feared members of this bacterial family are Yersinia pestis, the bacterium responsible for the bubonic plague or the Black Death, and Yersinia enterocolitica, a major cause of gastroenteritis.
Previous studies of this family of bacteria have focused on the harmful or pathogenic species, fragmenting our full understanding of the evolution of these species.
"In order to understand how an organism becomes dangerous or pathogenic, we need to understand their non-pathogenic family members to see what makes them different to the pathogenic forms," says Dr Sandra Reuter, first author from the Wellcome Trust Sanger Institute.
"Our dataset has allowed us to redefine the family structure of this unique set of bacteria and give us a full view of how an individual bacterial species can become harmful." The team sequenced 224 strains of different Yersinia family members from across the world to fully understand of how specific species evolve to become harmful, while others remain harmless.
This unique and detailed dataset describes the parallel evolution of Yersinia pestis and Yersinia enterocolitica; two major disease-causing pathogens in people.
The researchers showed that both species, independently of each other, acquired a segment of DNA known as plasmids, as well as the gene ail that allowed them to become pathogenic.
It appears that only these two virulence factors are present in all of the pathogenic Yersinia species.
"Before this study, there was uncertainty about what path these species took to become pathogenic: had they split from a shared common pathogenic ancestor?
Or had they evolved independently" says Professor Nicholas Thomson, senior author from the Wellcome Trust Sanger Institute.
"What we found were signatures in their genomes which plot the evolutionary path they took. "Surprisingly they emerged as human pathogens independently from a background of non-pathogenic close relatives.
These genetic signatures mark foothold moments of the emergence of these infamous disease-causing bacteria."
The team found that it was not only the acquisition of genes that has proven important to this family of bacteria, but also the loss of genes and the streamlining of metabolic pathways seems to be an important trait for the pathogenic species.
By examining the whole genomes of both the pathogenic and non-pathogenic species, they were able to determine that many of the metabolic functions, lost by the pathogenic species, were ancestral.
These functions were probably important for growth in a range of niches, and have been lost rather than gained in specific family lines in the Yersinia family.
"We commonly think bacteria must gain genes to allow them to become pathogens. However, we now know that the loss of genes and the streamlining of the pathogen's metabolic capabilities are key features in the evolution of these disease-causing bacteria," says Dr Alan McNally, senior author from Nottingham Trent University. "This study is shifting our view of the evolution and relationship between species within one family of bacteria."
The study has been published by the Proceedings of the National Academy of Sciences*.
Source: Wellcome Trust Sanger Institute [April 21, 2014]
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*Parallel independent evolution of pathogenicity within the genus Yersinia
- Sandra Reutera,b,1,
- Thomas R. Connorb,c,1,
- Lars Barquistb,
- Danielle Walkerb,
- Theresa Feltwellb,
- Simon R. Harrisb,
- Maria Fookesb,
- Miquette E. Halla,
- Nicola K. Pettyb,d,
- Thilo M. Fuchse,
- Jukka Coranderf,
- Muriel Dufourg,
- Tamara Ringwoodh,
- Cyril Savini,
- Christiane Bouchierj,
- Liliane Martini,
- Minna Miettinenf,
- Mikhail Shubinf,
- Julia M. Riehmk,
- Riikka Laukkanen-Niniosl,
- Leila M. Sihvonenm,
- Anja Siitonenm,
- Mikael Skurnikn,
- Juliana Pfrimer Falcãoo,
- Hiroshi Fukushimap,
- Holger C. Scholzk,
- Michael B. Prenticeh,
- Brendan W. Wrenq,
- Julian Parkhillb,
- Elisabeth Carnieli,
- Mark Achtmanr,s,
- Alan McNallya, and
- Nicholas R. Thomsonb,q,2
- Edited by Ralph R. Isberg, Howard Hughes Medical Institute and Tufts University School of Medicine, Boston, MA, and approved March 21, 2014 (received for review October 2, 2013)
Significance
Our past understanding of pathogen evolution has been fragmented because of tendencies to study human clinical isolates. To understand the evolutionary trends of pathogenic bacteria though, we need the context of their nonpathogenic relatives. Our unique and detailed dataset allows description of the parallel evolution of two key human pathogens: the causative agents of plague and Yersiniadiarrhea. The analysis reveals an emerging pattern where few virulence-related functions are found in all pathogenic lineages, representing key “foothold” moments that mark the emergence of these pathogens. Functional gene loss and metabolic streamlining are equally complementing the evolution of Yersinia across the pathogenic spectrum.
Abstract
The genus Yersinia has been used as a model system to study pathogen evolution. Using whole-genome sequencing of all Yersinia species, we delineate the gene complement of the whole genus and define patterns of virulence evolution. Multiple distinct ecological specializations appear to have split pathogenic strains from environmental, nonpathogenic lineages. This split demonstrates that contrary to hypotheses that all pathogenic Yersinia species share a recent common pathogenic ancestor, they have evolved independently but followed parallel evolutionary paths in acquiring the same virulence determinants as well as becoming progressively more limited metabolically. Shared virulence determinants are limited to the virulence plasmid pYV and the attachment invasion locus ail. These acquisitions, together with genomic variations in metabolic pathways, have resulted in the parallel emergence of related pathogens displaying an increasingly specialized lifestyle with a spectrum of virulence potential, an emerging theme in the evolution of other important human pathogens.
Footnotes
- 1S.R. and T.R.C. contributed equally to this work.
- 2To whom correspondence should be addressed. E-mail: nrt@sanger.ac.uk.
- Author contributions: S.R., T.R.C., B.W.W., J.P., M.A., A.M., and N.R.T. designed research; S.R., T.R.C., L.B., D.W., T.F., S.R.H., M.F., M.E.H., N.K.P., J.C., M.M., M. Shubin, and N.R.T. performed research; T.M.F., M.D., T.R., C.S., C.B., L.M., J.M.R., R.L.-N., L.M.S., A.S., J.P.F., H.F., and H.C.S. were involved in isolate collection and typing; S.R., T.R.C., L.B., D.W., S.R.H., M.F., M.E.H., N.K.P., J.C., M.M., M. Shubin, and N.R.T. analyzed data; and S.R., T.R.C., L.B., S.R.H., T.M.F., M. Skurnik, M.B.P., B.W.W., J.P., E.C., M.A., A.M., and N.R.T. wrote the paper.
- The authors declare no conflict of interest.
- This article is a PNAS Direct Submission.
- This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1317161111/-/DCSupplemental.
Freely available online through the PNAS open access option.
