Genomic comparison between Salmonella Gallinarum and Pullorum: differential pseudogene formation under common host restriction

PLoS One. 2013;8(3):e59427. doi: 10.1371/journal.pone.0059427. Epub 2013 Mar 15.

Abstract

Background: Salmonella serovars Enteritidis and Gallinarum are closely related, but their host ranges are very different: the former is host-promiscuous and the latter can infect poultry only. Comparison of their genomic sequences reveals that Gallinarum has undergone much more extensive degradation than Enteritidis. This phenomenon has also been observed in other host restricted Salmonella serovars, such as Typhi and Paratyphi A. The serovar Gallinarum can be further split into two biovars: Gallinarum and Pullorum, which take poultry as their common host but cause distinct diseases, with the former eliciting typhoid and the latter being a dysentery agent. Genomic comparison of the two pathogens, with a focus on pseudogenes, would provide insights into the evolutionary processes that might have facilitated the formation of host-restricted Salmonella pathogens.

Methodologies/principal findings: We sequenced the complete genome of Pullorum strains and made comparison with Gallinarum and other Salmonella lineages. The gene contents of Gallinarum and Pullorum were highly similar, but their pseudogene compositions differed considerably. About one fourth of pseudogenes had the same inactivation mutations in Gallinarum and Pullorum but these genes remained intact in Enteritidis, suggesting that the ancestral Gallinarum may have already been restricted to poultry. On the other hand, the remaining pseudogenes were either in the same genes but with different inactivation sites or unique to Gallinarum or Pullorum, reflecting unnecessary functions in infecting poultry.

Conclusions: Our results support the hypothesis that the divergence between Gallinarum and Pullorum was initiated and facilitated by host restriction. Formation of pseudogenes instead of gene deletion is the major form of genomic degradation. Given the short divergence history of Gallinarum and Pullorum, the effect of host restriction on genomic degradation is huge and rapid, and such effect seems to be continuing to work. The pseudogenes may reflect the unnecessary functions for Salmonella within the poultry host.

Publication types

  • Comparative Study
  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Bacterial Typing Techniques
  • Base Sequence
  • Chickens / microbiology*
  • Genetic Speciation
  • Genome, Bacterial*
  • Genomics*
  • Host Specificity
  • Humans
  • Molecular Sequence Data
  • Mutation
  • Phylogeny
  • Poultry Diseases / microbiology*
  • Pseudogenes*
  • Salmonella / classification*
  • Salmonella / genetics*
  • Sequence Analysis, DNA
  • Species Specificity

Associated data

  • GENBANK/CP003786

Grants and funding

This work was supported by a grant from the National Science Foundation of China (NSFC81201248) to YF; a grant of National Natural Science Foundation of China (NSFC30970078) and a grant of Natural Science Foundation of Heilongjiang Province of China to GRL; and a start-up grant from Harbin Medical University, grants of the National Natural Science Foundation of China (NSFC30970119, 81030029, 81271786), a grant of the National Natural Science Foundation of China and National Institutes of Health of United States of America (NSFC-NIH 81161120416), and a Specialized Research Fund for the Doctoral Program of Higher Education (SRFDP, 20092307110001) to SLL. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.