Loss and Gain in the Evolution of the Salmonella enterica Serovar Gallinarum Biovar Pullorum Genome

Abstract

Salmonella entericasubspeciesentericaserovar Gallinarum biovar Pullorum (S. Pullorum) is the etiological agent of pullorum disease, causing white diarrhea with high mortality in chickens. There are many unsolved issues surrounding the epidemiology ofS. Pullorum, including its origin and transmission history as well as the discordance between its phenotypic heterogeneity and genetic monomorphism. In this paper, we report the results of whole-genome sequencing of a panel of 97S. Pullorum strains isolated between 1962 and 2014 from four countries across three continents. We utilized 6,795 core genome single nucleotide polymorphisms (SNPs) to reconstruct a phylogenetic tree within a spatiotemporal Bayesian framework, estimating that the most recent common ancestor ofS. Pullorum emerged in ∼914 CE (95% confidence interval [95%CI], 565 to 1273 CE). The extantS. Pullorum strains can be divided into four distinct lineages, each of which is significantly associated with geographical distribution. The intercontinental transmissions of lineages III and IV can be traced to the mid-19th century and are probably related to the “Hen Fever” prevalent at that time. Further genomic analysis indicated that the loss or pseudogenization of functional genes involved in metabolism and virulence inS. Pullorum has been ongoing since before and after divergence from the ancestor. In contrast, multiple prophages and plasmids have been acquired byS. Pullorum, and these have endowed it with new characteristics, especially the multidrug resistance conferred by two large plasmids in lineage I. The results of this study provide insight into the evolution ofS. Pullorum and prove the efficiency of whole-genome sequencing in epidemiological surveillance of pullorum disease.IMPORTANCEPullorum disease, an acute poultry septicemia caused bySalmonellaGallinarum biovar Pullorum, is fatal for young chickens and is a heavy burden on poultry industry. The pathogen is rare in most developed countries but still extremely difficult to eliminate in China. Efficient epidemiological surveillance necessitates clarifying the origin of the isolates from different regions and their phylogenic relationships. Genomic epidemiological analysis of 97S. Pullorum strains was carried out to reconstruct the phylogeny and transmission history ofS. Pullorum. Further analysis demonstrated that functional gene loss and acquisition occurred simultaneously throughout the evolution ofS. Pullorum, both of which reflected adaptation to the changing environment. The result of our study will be helpful in surveillance and prevention of pullorum disease.

Comparative genome analysis of Salmonella enterica serovar Gallinarum biovars Pullorum and Gallinarum decodes strain specific genes

“…enterica comprises of both host-adapted and host-promiscuous pathotypes that causes a spectrum of diseases depending on the serovar or host (Jajere 2019;Cheng et al 2019). Pullorum Disease (PD) and Fowl Typhoid (FT) caused by S. Gallinarum biovars Pullorum (bvP) and Gallinarum (bvG) respectively are endemic in countries of Asia and South America leading to huge economic losses to poultry industry (Shivaprasad 2000;De Carli et al 2017;Hu et al 2019). It is interesting to note that as compared to FT, the PD reports have been low in India (Rajagopal and Mini, 2013).…”

“…It is interesting to note that as compared to FT, the PD reports have been low in India (Rajagopal and Mini, 2013). On the other hand, PD is frequent in China, being prevalent in every province (Hu et al 2019). Biosecurity and vaccinations applied in combination are important strategies to prevent and control these diseases in commercial and breeding ocks.…”

“…analysis of host-adapted salmonellae genomes have elucidated various evolutionary and virulence themes (Langridge et al 2015;Hu et al 2019), this is the rst report for the assessment of genotypic differences, which includes an Indian strain among the investigated strains from America and China.…”

“…Pullorum disease (PD) occurs in young birds and persists for long periods in spleen and reproductive tract which leads to high mortality (Wigley et al 2001). The disease is characterised by white diarrhoea chaperoned with increased antimicrobial resistance (AMR) and high infection rates (Hu et al 2019;Guo et al 2019). On the other hand, FT can affect birds of all ages but primarily occurs in adult birds and results in variable morbidity depending on the age, species, and breed of the bird (Barrow & Freitas Neto 2011).…”

AvrA Exerts Inhibition of NF-κB Pathway in Its Naïve Salmonella Serotype through Suppression of p-JNK and Beclin-1 Molecules

“…Additionally, we analyzed AvrA sequences in 96 sequenced S. Pullorum isolates, and the results confirm that the AvrA in all of the detected S. Pullorum strains lose the C-terminal ten amino acids ( Figure S1). To identify the effect of SP-AvrA on anti-inflammatory response, the reference strain C79-13 representing the dominant lineage of S. Pullorum based on SNP analysis of core-genome sequences was used in the construction of avrA mutants and complementary strains [14]. S. Enteritidis P125109 was used as the control strain with complete AvrA sequence.…”