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Genomic Analysis Uncovers Three Salmonella Enteritidis Lineages

NEW YORK (GenomeWeb) – Different Salmonella Enteritidis lineages are behind the enterocolitis it causes in high-income areas and the invasive disease it causes in low-income areas, a new genomic analysis suggests.

Researchers from the Wellcome Trust Sanger Institute and elsewhere analyzed the whole-genome sequences of 675 Salmonella enterica serovar Enteritidis from 45 countries to find three epidemic clades, one that's global and two that are restricted to certain parts of Africa. As they reported in Nature Genetics today, the researchers found that this global clade is linked to poultry-associated enterocolitis, mostly in wealthier regions of the world, and the African clades are linked to invasive disease among poorer, often immune-compromised individuals. The African clades further exhibit genomic degradation and increased drug resistance.

"Using whole-genome sequencing of S. Enteritidis bacteria from different settings we have revealed three distinct types of this bacteria, which was previously thought to have only one type," first author Nicholas Feasey from Liverpool School of Tropical Medicine and the Sanger Institute said in a statement.

Feasey and his colleagues sequenced 675 isolates of S. Enteritidis that were collected between 1948 and 2013. Of these samples, 496 were from Africa, mostly from sub-Saharan Africa, but also some from North Africa.

The researchers mapped these S. Enteritidis sequences and one Salmonella enterica serovar Gallinarum genome to an S. Enteritidis reference strain genome. Through a phylogenic analysis, they uncovered three S. Enteritidis clades: a global clade that included the reference, a clade of mostly West African isolates, and a clade of primarily Central or East African isolates. The remaining 58 isolates were phylogenetically, geographically, and temporally diverse, the researchers added.

The global clade, the researchers reported, contained 250 isolates, and of the 144 isolates tested, 104 were susceptible to all antimicrobials tried, five were multi-drug resistant, and one was resistant to nalidixic acid.

All but one of the isolates in the West African clade, meanwhile, came from that region; one hailed from the US. This clade was highly drug resistant, with 94 percent of the isolates resistant to at least one class of antimicrobials. The Central/East African clade also largely came from that region; only two isolates came from outside that area, in South Africa. A good portion of these isolates, 82 percent, was multi-drug resistant.

With these sequenced S. Enteritidis genomes, Feasey and his colleagues uncovered a core genome of some 4,000 genes and an accessory genome of 14,000 predicted genes. Fifty-seven of those predicted genes were specific to the global clade, and those were all associated with prophage phiSE20, which is needed to invade chicken eggs and mice.

Meanwhile, the West African clade harbored 15 predicted genes that other clades lacked, 11 of which were associated with plasmids, and the Central/East African clade had 77 specific predicted genes of which 33 were associated with virulence plasmids and 40 were linked with a new prophage region. The two African clades also shared 102 genes, including one linked to a new prophage region.

At the same time, the researchers also reconstructed the S. Enteritidis virulence plasmid and found that its phylogeny largely followed that of the main chromosome, indicating that each lineage has stably maintained the plasmid and that the plasmid diversified with the chromosome.

The African clades also had signatures of differential host adaptation, the researchers noted. For instance, isolate D7795, which was from an infected individual in Malawi, harbored 42 putative disrupted genes, and many of these disruptions were of genes involved in the colonization of the gut and shedding in stool as well as of genes involved in metabolic processes like the biosynthesis of cobalamin. This suggested to the researchers that this clade underwent reductive evolution.

"This study highlights a very important issue: that a relatively mild version of a bacterium can evolve into a more dangerous pathogen under the right conditions," author Nick Thomson from the Sanger Institute said in a statement.

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