Comparative genomics reveals different population structures associated with host and geographic origin in antimicrobial‐resistant <scp><i>Salmonella enterica</i></scp>

Liao, Jingqiu; Orsi, Renato H.; Carroll, Laura M.

doi:10.1111/1462-2920.15014

Cited by 14 publications

(13 citation statements)

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“…Geography plays an important role in shaping bacterial pathogen population structure, including that of Salmonella enterica , and different geographic regions may harbor their own endemic lineages ( Achtman, 2008 ; Strachan et al, 2015 ; Carroll et al, 2017 ; Palma et al, 2018 ; Fenske et al, 2019 ; Liao et al, 2020 ). Here, we observed numerous endemic Salmonella enterica lineages circulating among animals and animal products in South Africa, some of which encompassed human clinical isolates.…”

Section: Discussionmentioning

confidence: 99%

Genomic Characterization of Endemic and Ecdemic Non-typhoidal Salmonella enterica Lineages Circulating Among Animals and Animal Products in South Africa

et al. 2021

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In Africa, the burden of illness caused by non-typhoidal Salmonella enterica is disproportionally high; however, whole-genome sequencing (WGS) efforts are overwhelmingly concentrated in world regions with lower burdens. While WGS is being increasingly employed in South Africa to characterize Salmonella enterica, the bulk of these efforts have centered on characterizing human clinical strains. Thus, very little is known about lineages circulating among animals in the country on a genomic scale. Here, we used WGS to characterize 63 Salmonella enterica strains isolated from livestock, companion animals, wildlife, and animal products in South Africa over a 60-year period. Genomes were assigned to serotypes Dublin, Hadar, Enteritidis, and Typhimurium (n = 18, 8, 13, and 24 strains, respectively) and sequence types (STs) ST10 (all S. Dublin), ST33 (all S. Hadar), ST11/ST366 (n = 12 and 1 S. Enteritidis, respectively), and ST19/ST34 (n = 23 and 1 S. Typhimurium, respectively; via seven-gene multi-locus sequence typing). Within-ST phylogenies were constructed using genomes sequenced in this study, plus publicly available genomes representative of each ST’s (i) global (n = 2,802 and 1,569 S. Dublin and Hadar genomes, respectively) and (ii) African (n = 716 and 343 S. Enteritidis and Typhimurium genomes, respectively) population. For S. Dublin ST10, a largely antimicrobial-susceptible, endemic lineage circulating among humans, animals, and food in South Africa was identified, as well as a lineage that was likely recently introduced from the United States. For S. Hadar ST33, multiple South African lineages harboring streptomycin and tetracycline resistance-conferring genes were identified. African S. Enteritidis ST11 could be primarily partitioned into one largely antimicrobial-susceptible and one largely multidrug-resistant (MDR) clade, with South African isolates confined to the largely antimicrobial-susceptible clade. S. Typhimurium ST19/ST34 strains sequenced here were distributed across the African S. Typhimurium ST19/ST34 phylogeny, representing a diverse range of lineages, including numerous MDR lineages. Overall, this study provides critical insights into endemic and ecdemic non-typhoidal Salmonella enterica lineages circulating among animals, foods, and humans in South Africa and showcases the utility of WGS in characterizing animal-associated strains from a world region with a high salmonellosis burden.

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Section: Discussionmentioning

confidence: 99%

Genomic Characterization of Endemic and Ecdemic Non-typhoidal Salmonella enterica Lineages Circulating Among Animals and Animal Products in South Africa

et al. 2021

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“…Geography plays an important role in shaping bacterial pathogen population structure, including that of Salmonella enterica , and different geographic regions may harbor their own endemic lineages (31, 34–38). Here, we observed numerous endemic Salmonella enterica lineages circulating among animals and animal products in South Africa, some of which encompassed human clinical isolates.…”

Section: Discussionmentioning

confidence: 99%

Genomic characterization of endemic and ecdemic non-typhoidalSalmonella entericalineages circulating among animals and animal products in South Africa

Carroll¹,

Pierneef

Mathole

et al. 2021

Preprint

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Non-typhoidal Salmonella enterica imposes a significant burden on human and animal health in South Africa. However, very little is known about lineages circulating among animals and animal products in the country on a genomic scale. Here, we used whole-genome sequencing (WGS) to characterize 63 Salmonella enterica strains (n = 18, 8, 13, and 24 strains assigned to serotypes Dublin, Hadar, Enteritidis, and Typhimurium, respectively) isolated from livestock, companion animals, wildlife, and animal products in South Africa over a 60-year period. Within-serotype phylogenies were constructed using genomes sequenced in this study, as well as publicly available genomes representative of each respective serotype's (i) global (n = 2,802 and 1,569 S. Dublin and Hadar genomes, respectively) and (ii) African (n = 716 and 343 S. Enteritidis and Typhimurium genomes, respectively) population. For S. Dublin, the approaches used here identified a largely antimicrobial-susceptible, endemic lineage circulating among humans, animals, and food in South Africa, as well as a lineage that was likely recently introduced from the United States. For S. Hadar, multiple South African lineages harboring streptomycin and tetracycline resistance-conferring genes were identified. African S. Enteritidis could be primarily partitioned into one largely antimicrobial-susceptible and one largely multidrug-resistant (MDR) clade, with South African isolates confined to the largely antimicrobial-susceptible clade. S. Typhimurium strains sequenced here were distributed across the African S. Typhimurium phylogeny, representing a diverse range of lineages, including numerous MDR lineages. Overall, this study provides insight into the evolution, population structure, and antimicrobial resistome composition of Salmonella enterica in Africa. IMPORTANCE Globally, Salmonella enterica is estimated to be responsible for more than 93 million illnesses and 150,000 deaths annually. In Africa, the burden of salmonellosis is disproportionally high; however, WGS efforts are overwhelmingly concentrated in world regions with lower salmonellosis burdens. While WGS is being increasingly employed in South Africa to characterize Salmonella enterica, the bulk of these efforts have centered on characterizing human clinical strains. WGS data derived from non-typhoidal Salmonella enterica serotypes isolated from non-human sources in South Africa is extremely limited. To our knowledge, the genomes sequenced here represent the largest collection of non-typhoidal Salmonella enterica isolate genomes from non-human sources in South Africa to date. Furthermore, this study provides critical insights into endemic and ecdemic non-typhoidal Salmonella enterica lineages circulating among animals, foods, and humans in South Africa and showcases the utility of WGS in characterizing animal-associated strains from a world region with a high salmonellosis burden.

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“…However, core-genomic based analysis can preclude the identification of cryptic variants circulating in a population, such as in the case of S. Enteritidis cryptic lineages capable of causing gastroenteritis and bloodstream-invasion (Feasey et al, 2016;Klemm et al, 2016), or in the case of S. Typhimurium lineages capable of causing Non-Typhoidal Salmonellosis (NTS) (Kingsley et al, 2009;Bawn et al, 2020). Recent studies have also demonstrated the usefulness of enhanced genotypic granularity from inclusion of accessory genomic data (Abudahab et al, 2019;Liao et al, 2020), and such granularity can indeed enhance epidemiological investigations (McNally et al, 2016). Mining of accessory genomes has also proven to be applicable for identifying phylogeographical signatures for S. Dublin (Fenske et al, 2019), and for structuring of S. Infantis population while predicting the existence of discrete lineages linked to unique prophages (Gymoese et al, 2019).…”

Section: Using Whole Genome For Population-based Analysis Can Be Epidemiologically and Ecologically Relevantmentioning

confidence: 99%

Heuristic and Hierarchical-Based Population Mining of Salmonella enterica Lineage I Pan-Genomes as a Platform to Enhance Food Safety

Gomes-Neto

Pavlovikj

Cano

et al. 2021

Front. Sustain. Food Syst.

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The recent incorporation of bacterial whole-genome sequencing (WGS) into Public Health laboratories has enhanced foodborne outbreak detection and source attribution. As a result, large volumes of publicly available datasets can be used to study the biology of foodborne pathogen populations at an unprecedented scale. To demonstrate the application of a heuristic and agnostic hierarchical population structure guided pan-genome enrichment analysis (PANGEA), we used populations of S. enterica lineage I to achieve two main objectives: (i) show how hierarchical population inquiry at different scales of resolution can enhance ecological and epidemiological inquiries; and (ii) identify population-specific inferable traits that could provide selective advantages in food production environments. Publicly available WGS data were obtained from NCBI database for three serovars of Salmonella enterica subsp. enterica lineage I (S. Typhimurium, S. Newport, and S. Infantis). Using the hierarchical genotypic classifications (Serovar, BAPS1, ST, cgMLST), datasets from each of the three serovars showed varying degrees of clonal structuring. When the accessory genome (PANGEA) was mapped onto these hierarchical structures, accessory loci could be linked with specific genotypes. A large heavy-metal resistance mobile element was found in the Monophasic ST34 lineage of S. Typhimurium, and laboratory testing showed that Monophasic isolates have on average a higher degree of copper resistance than the Biphasic ones. In S. Newport, an extra sugE gene copy was found among most isolates of the ST45 lineage, and laboratory testing of multiple isolates confirmed that isolates of S. Newport ST45 were on average less sensitive to the disinfectant cetylpyridimium chloride than non-ST45 isolates. Lastly, data-mining of the accessory genomic content of S. Infantis revealed two cryptic Ecotypes with distinct accessory genomic content and distinct ecological patterns. Poultry appears to be the major reservoir for Ecotype 1, and temporal analysis further suggested a recent ecological succession, with Ecotype 2 apparently being displaced by Ecotype 1. Altogether, the use of a heuristic hierarchical-based population structure analysis that includes bacterial pan-genomes (core and accessory genomes) can (1) improve genomic resolution for mapping populations and accessing epidemiological patterns; and (2) define lineage-specific informative loci that may be associated with survival in the food chain.

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Comparative genomics reveals different population structures associated with host and geographic origin in antimicrobial‐resistant Salmonella enterica

Cited by 14 publications

References 77 publications

Genomic Characterization of Endemic and Ecdemic Non-typhoidal Salmonella enterica Lineages Circulating Among Animals and Animal Products in South Africa

Genomic Characterization of Endemic and Ecdemic Non-typhoidal Salmonella enterica Lineages Circulating Among Animals and Animal Products in South Africa

Genomic characterization of endemic and ecdemic non-typhoidalSalmonella entericalineages circulating among animals and animal products in South Africa

Heuristic and Hierarchical-Based Population Mining of Salmonella enterica Lineage I Pan-Genomes as a Platform to Enhance Food Safety

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