Publications by authors named "Frank M Aarestrup"

209 Publications

Pandemics- One Health preparedness for the next.

Lancet Reg Health Eur 2021 Oct 7;9:100210. Epub 2021 Oct 7.

Erasmus Medical Centre, Rotterdam, The Netherlands.

The majority of emerging infectious diseases originate in animals. Current routine surveillance is focused on known diseases and clinical syndromes, but the increasing likelihood of emerging disease outbreaks shows the critical importance of early detection of unusual illness or circulation of pathogens - prior to human disease manifestation. In this Viewpoint, we focus on one key pillar of preparedness-the need for early warning surveillance at the human, animal, environmental interface. The COVID-19 pandemic has revolutionized the scale of sequencing of pathogen genomes, and the current investments in global genomic surveillance offer great potential for a novel, truly integrated Disease X (with epidemic or pandemic potential) surveillance arm provided we do not make the mistake of developing them solely for the case at hand. Generic tools include metagenomic sequencing as a catch-all technique, rather than detection and sequencing protocols focusing on what we know. Developing agnostic or more targeted metagenomic sequencing to assess unusual disease in humans and animals, combined with random sampling of environmental samples capturing pathogen circulation is technically challenging, but could provide a true early warning system. Rather than rebuilding and reinforcing the pre-existing silo's, a real step forward would be to take the lessons learned and bring in novel essential partnerships in a One Health approach to preparedness.
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http://dx.doi.org/10.1016/j.lanepe.2021.100210DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8495373PMC
October 2021

Standard Sample Storage Conditions Have an Impact on Inferred Microbiome Composition and Antimicrobial Resistance Patterns.

Microbiol Spectr 2021 Oct 6;9(2):e0138721. Epub 2021 Oct 6.

Research Group for Genomic Epidemiology, National Food Institute, Technical University of Denmarkgrid.5170.3, Kongens Lyngby, Denmark.

Storage of biological specimens is crucial in the life and medical sciences. Storage conditions for samples can be different for a number of reasons, and it is unclear what effect this can have on the inferred microbiome composition in metagenomics analyses. Here, we assess the effect of common storage temperatures (deep freezer, -80°C; freezer, -20°C; refrigerator, 5°C; room temperature, 22°C) and storage times (immediate sample processing, 0 h; next day, 16 h; over weekend, 64 h; longer term, 4, 8, and 12 months) as well as repeated sample freezing and thawing (2 to 4 freeze-thaw cycles). We examined two different pig feces and sewage samples, unspiked and spiked with a mock community, in triplicate, respectively, amounting to a total of 438 samples (777 Gbp; 5.1 billion reads). Storage conditions had a significant and systematic effect on the taxonomic and functional composition of microbiomes. Distinct microbial taxa and antimicrobial resistance classes were, in some situations, similarly affected across samples, while others were not, suggesting an impact of individual inherent sample characteristics. With an increasing number of freeze-thaw cycles, an increasing abundance of , , and eukaryotic microorganisms was observed. We provide recommendations for sample storage and strongly suggest including more detailed information in the metadata together with the DNA sequencing data in public repositories to better facilitate meta-analyses and reproducibility of findings. Previous research has reported effects of DNA isolation, library preparation, and sequencing technology on metagenomics-based microbiome composition; however, the effect of biospecimen storage conditions has not been thoroughly assessed. We examined the effect of common sample storage conditions on metagenomics-based microbiome composition and found significant and, in part, systematic effects. Repeated freeze-thaw cycles could be used to improve the detection of microorganisms with more rigid cell walls, including parasites. We provide a data set that could also be used for benchmarking algorithms to identify and correct for unwanted batch effects. Overall, the findings suggest that all samples of a microbiome study should be stored in the same way. Furthermore, there is a need to mandate more detailed information about sample storage and processing be published together with DNA sequencing data at the International Nucleotide Sequence Database Collaboration (ENA/EBI, NCBI, DDBJ) or other repositories.
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http://dx.doi.org/10.1128/Spectrum.01387-21DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8510183PMC
October 2021

Secrets of the Hospital Underbelly: Patterns of Abundance of Antimicrobial Resistance Genes in Hospital Wastewater Vary by Specific Antimicrobial and Bacterial Family.

Front Microbiol 2021 10;12:703560. Epub 2021 Sep 10.

Usher Institute, University of Edinburgh, Edinburgh, United Kingdom.

Hospital wastewater is a major source of antimicrobial resistance (AMR) outflow into the environment. This study uses metagenomics to study how hospital clinical activity impacts antimicrobial resistance genes (ARGs) abundances in hospital wastewater. Sewage was collected over a 24-h period from multiple wastewater collection points (CPs) representing different specialties within a tertiary hospital site and simultaneously from community sewage works. High throughput shotgun sequencing was performed using Illumina HiSeq4000. ARG abundances were correlated to hospital antimicrobial usage (AMU), data on clinical activity and resistance prevalence in clinical isolates. Microbiota and ARG composition varied between CPs and overall ARG abundance was higher in hospital wastewater than in community influent. ARG and microbiota compositions were correlated (Procrustes analysis, =0.014). Total antimicrobial usage was not associated with higher ARG abundance in wastewater. However, there was a small positive association between resistance genes and antimicrobial usage matched to ARG phenotype (IRR 1.11, CI 1.06-1.16, <0.001). Furthermore, analyzing carbapenem and vancomycin resistance separately indicated that counts of ARGs to these antimicrobials were positively associated with their increased usage [carbapenem rate ratio (RR) 1.91, 95% CI 1.01-3.72, =0.07, and vancomycin RR 10.25, CI 2.32-49.10, <0.01]. Overall, ARG abundance within hospital wastewater did not reflect resistance patterns in clinical isolates from concurrent hospital inpatients. However, for clinical isolates of the family and , there was a positive relationship with wastewater ARG abundance [odds ratio (OR) 1.62, CI 1.33-2.00, <0.001, and OR 1.65, CI 1.21-2.30, =0.006 respectively]. We found that the relationship between hospital wastewater ARGs and antimicrobial usage or clinical isolate resistance varies by specific antimicrobial and bacterial family studied. One explanation, we consider is that relationships observed from multiple departments within a single hospital site will be detectable only for ARGs against parenteral antimicrobials uniquely used in the hospital setting. Our work highlights that using metagenomics to identify the full range of ARGs in hospital wastewater is a useful surveillance tool to monitor hospital ARG carriage and outflow and guide environmental policy on AMR.
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http://dx.doi.org/10.3389/fmicb.2021.703560DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8461093PMC
September 2021

Arrangements of Mobile Genetic Elements among Virotype E Subpopulation of Sequence Type 131 Strains with High Antimicrobial Resistance and Virulence Gene Content.

mSphere 2021 08 25;6(4):e0055021. Epub 2021 Aug 25.

Section for Genomic Epidemiology, National Food Institute, Technical University of Denmarkgrid.5170.3, Lyngby, Denmark.

Escherichia coli sequence type 131 (ST131) is known for its contribution to multidrug resistance and the worldwide spread of this clone has become a global problem. Understanding the trends among ST131 clades will help design strategies to prevent its rapid dissemination. In this study, 72 ST131 strains were subjected to comparative genomic analysis and 64 clade C strains were compared with clade C strains reported from other regions using publicly available whole-genome sequencing data. C1 ( = 31 [48.4%]) and C2 ( = 33 [%51.5]) strains had the same prevalence in our collection, and C1-M27 ( = 22) strains were closely related, carried a unique plasmid type (F1:A2:B20), and exhibited virotype C. Removal of 11 C2 strains with varied virotype patterns and the heterogeneous IncF type identified 22 closely related virotype E/F strains with replicon type F31/F36:A4:B1, forming what we denote as the "C2-subset." In a global context, the C2-subset constituted a distinct cluster with international virotype E strains and harbored a genomic island, . Association of genes with 1 to 7 mobile genetic elements, mostly IS/IS combination within was identified. The C2-subset accounted for excess resistance/virulence of subclade C2 relative to C1 strains. In addition, a conserved chromosomal IS-mediated composite transposon (IS-IS-- cupin fold metalloprotein-TnIS) was observed in the C2-subset. The local spread of the C2-subset in the hospital studied, with the carriage of higher virulence/resistance markers and a peculiar F-type plasmid, demonstrates the potential for diversification of the ST131 lineage and the emergence of subpopulations with higher survival potential to cause health care-associated outbreaks. Escherichia coli sequence type 131 (ST131) is a globally dominant multidrug-resistant clone that is commonly associated with extraintestinal infections. Specific sublineages have been shown to have emerged and spread within ST131, highlighting the complex nature of ST131 epidemiology. This study systematically compared the Iranian ST131 population to those reported from other countries and found a subpopulation harboring virotype E, a homogeneous profile of plasmid Inc-F type F31/F36:A4:B1 harboring /hemolysin genes on the genomic island , and up to seven mobile genetic elements (MGEs) flanking /hemolysin virulence markers. The results of this study highlight the importance of MGEs for virulence gene acquisition and the formation of new subpopulations among pandemic clones such as E. coli ST131.
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http://dx.doi.org/10.1128/mSphere.00550-21DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8386418PMC
August 2021

Risk Factors for Antimicrobial Resistance in Turkey Farms: A Cross-Sectional Study in Three European Countries.

Antibiotics (Basel) 2021 Jul 6;10(7). Epub 2021 Jul 6.

Institute for Risk Assessment Sciences, Utrecht University, Yalelaan 2, 3584 CM Utrecht, The Netherlands.

Food-producing animals are an important reservoir and potential source of transmission of antimicrobial resistance (AMR) to humans. However, research on AMR in turkey farms is limited. This study aimed to identify risk factors for AMR in turkey farms in three European countries (Germany, France, and Spain). Between 2014 and 2016, faecal samples, antimicrobial usage (AMU), and biosecurity information were collected from 60 farms. The level of AMR in faecal samples was quantified in three ways: By measuring the abundance of AMR genes through (i) shotgun metagenomics sequencing ( = 60), (ii) quantitative real-time polymerase chain reaction (qPCR) targeting , , , and ; ( = 304), and (iii) by identifying the phenotypic prevalence of AMR in isolates by minimum inhibitory concentrations (MIC) ( = 600). The association between AMU or biosecurity and AMR was explored. Significant positive associations were detected between AMU and both genotypic and phenotypic AMR for specific antimicrobial classes. Beta-lactam and colistin resistance (metagenomics sequencing); ampicillin and ciprofloxacin resistance (MIC) were associated with AMU. However, no robust AMU-AMR association was detected by analyzing qPCR targets. In addition, no evidence was found that lower biosecurity increases AMR abundance. Using multiple complementary AMR detection methods added insights into AMU-AMR associations at turkey farms.
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http://dx.doi.org/10.3390/antibiotics10070820DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8300668PMC
July 2021

Genomic evolution of antimicrobial resistance in Escherichia coli.

Sci Rep 2021 07 23;11(1):15108. Epub 2021 Jul 23.

National Food Institute, Technical University of Denmark, Kemitorvet, Building 204, 2800, Kgs. Lyngby, Denmark.

The emergence of antimicrobial resistance (AMR) is one of the biggest health threats globally. In addition, the use of antimicrobial drugs in humans and livestock is considered an important driver of antimicrobial resistance. The commensal microbiota, and especially the intestinal microbiota, has been shown to have an important role in the emergence of AMR. Mobile genetic elements (MGEs) also play a central role in facilitating the acquisition and spread of AMR genes. We isolated Escherichia coli (n = 627) from fecal samples in respectively 25 poultry, 28 swine, and 15 veal calf herds from 6 European countries to investigate the phylogeny of E. coli at country, animal host and farm levels. Furthermore, we examine the evolution of AMR in E. coli genomes including an association with virulence genes, plasmids and MGEs. We compared the abundance metrics retrieved from metagenomic sequencing and whole genome sequenced of E. coli isolates from the same fecal samples and farms. The E. coli isolates in this study indicated no clonality or clustering based on country of origin and genetic markers; AMR, and MGEs. Nonetheless, mobile genetic elements play a role in the acquisition of AMR and virulence genes. Additionally, an abundance of AMR was agreeable between metagenomic and whole genome sequencing analysis for several AMR classes in poultry fecal samples suggesting that metagenomics could be used as an indicator for surveillance of AMR in E. coli isolates and vice versa.
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http://dx.doi.org/10.1038/s41598-021-93970-7DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8302606PMC
July 2021

Microbiota long-term dynamics and prediction of acute graft-versus-host disease in pediatric allogeneic stem cell transplantation.

Microbiome 2021 06 28;9(1):148. Epub 2021 Jun 28.

Research Group for Genomic Epidemiology, Technical University of Denmark, Kongens Lyngby, Denmark.

Background: Patients undergoing allogeneic hematopoietic stem cell transplantation (HSCT) exhibit changes in their gut microbiota and are experiencing a range of complications, including acute graft-versus-host disease (aGvHD). It is unknown if, when, and under which conditions a re-establishment of microbial and immunological homeostasis occurs. It is also unclear whether microbiota long-term dynamics occur at other body sites than the gut such as the mouth or nose. Moreover, it is not known whether the patients' microbiota prior to HSCT holds clues to whether the patient would suffer from severe complications subsequent to HSCT. Here, we take a holobiont perspective and performed an integrated host-microbiota analysis of the gut, oral, and nasal microbiota in 29 children undergoing allo-HSCT.

Results: The bacterial diversity decreased in the gut, nose, and mouth during the first month and reconstituted again 1-3 months after allo-HSCT. The microbial community composition traversed three phases over 1 year. Distinct taxa discriminated the microbiota temporally at all three body sides, including Enterococcus spp., Lactobacillus spp., and Blautia spp. in the gut. Of note, certain microbial taxa appeared already changed in the patients prior to allo-HSCT as compared with healthy children. Acute GvHD occurring after allo-HSCT could be predicted from the microbiota composition at all three body sites prior to HSCT. The reconstitution of CD4 T cells, T17, and B cells was associated with distinct taxa of the gut, oral, and nasal microbiota.

Conclusions: This study reveals for the first time bacteria in the mouth and nose that may predict aGvHD. Monitoring of the microbiota at different body sites in HSCT patients and particularly through involvement of samples prior to transplantation may be of prognostic value and could assist in guiding personalized treatment strategies. The identification of distinct bacteria that have a potential to predict post-transplant aGvHD might provide opportunities for an improved preventive clinical management, including a modulation of microbiomes. The host-microbiota associations shared between several body sites might also support an implementation of more feasible oral and nasal swab sampling-based analyses. Altogether, the findings suggest that the microbiota and host factors together could provide actionable information to guiding precision medicine. Video Abstract.
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http://dx.doi.org/10.1186/s40168-021-01100-2DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8240369PMC
June 2021

A Peek into the Plasmidome of Global Sewage.

mSystems 2021 Jun 26;6(3):e0028321. Epub 2021 May 26.

Research Group for Genomic Epidemiology, Technical University of Denmark, Kgs. Lyngby, Denmark.

Plasmids can provide a selective advantage for microorganisms to survive and adapt to new environmental conditions. Plasmid-encoded traits, such as antimicrobial resistance (AMR) or virulence, impact the ecology and evolution of bacteria and can significantly influence the burden of infectious diseases. Insight about the identity and functions encoded on plasmids on the global scale are largely lacking. Here, we investigate the plasmidome of 24 samples (22 countries, 5 continents) from the global sewage surveillance project. We obtained 105-Gbp Oxford Nanopore and 167-Gbp Illumina NextSeq DNA sequences from plasmid DNA preparations and assembled 165,302 contigs (159,322 circular). Of these, 58,429 carried genes encoding for plasmid-related and 11,222 for virus/phage-related proteins. About 90% of the circular DNA elements did not have any similarity to known plasmids. Those that exhibited similarity had similarity to plasmids whose hosts were previously detected in these sewage samples (e.g., Acinetobacter, Escherichia, , Enterobacter, , and Klebsiella). Some AMR classes were detected at a higher abundance in plasmidomes (e.g., macrolide-lincosamide-streptogramin B, macrolide, and quinolone) compared to the respective complex sewage samples. In addition to AMR genes, a range of functions were encoded on the candidate plasmids, including plasmid replication and maintenance, mobilization, and conjugation. In summary, we describe a laboratory and bioinformatics workflow for the recovery of plasmids and other potential extrachromosomal DNA elements from complex microbiomes. Moreover, the obtained data could provide further valuable insight into the ecology and evolution of microbiomes, knowledge about AMR transmission, and the discovery of novel functions. This is, to the best of our knowledge, the first study to investigate plasmidomes at a global scale using long read sequencing from complex untreated domestic sewage. Previous metagenomic surveys have detected AMR genes in a variety of environments, including sewage. However, it is unknown whether the AMR genes were present on the microbial chromosome or located on extrachromosomal elements, such as plasmids. Using our approach, we recovered a large number of plasmids, of which most appear novel. We identified distinct AMR genes that were preferentially located on plasmids, potentially contributing to their transmissibility. Overall, plasmids are of great importance for the biology of microorganisms in their natural environments (free-living and host-associated), as well as for molecular biology and biotechnology. Plasmidome collections may therefore be valuable resources for the discovery of fundamental biological mechanisms and novel functions useful in a variety of contexts.
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http://dx.doi.org/10.1128/mSystems.00283-21DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8269221PMC
June 2021

Monitoring SARS-CoV-2 Circulation and Diversity through Community Wastewater Sequencing, the Netherlands and Belgium.

Emerg Infect Dis 2021 05;27(5):1405-1415

Severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) has rapidly become a major global health problem, and public health surveillance is crucial to monitor and prevent virus spread. Wastewater-based epidemiology has been proposed as an addition to disease-based surveillance because virus is shed in the feces of ≈40% of infected persons. We used next-generation sequencing of sewage samples to evaluate the diversity of SARS-CoV-2 at the community level in the Netherlands and Belgium. Phylogenetic analysis revealed the presence of the most prevalent clades (19A, 20A, and 20B) and clustering of sewage samples with clinical samples from the same region. We distinguished multiple clades within a single sewage sample by using low-frequency variant analysis. In addition, several novel mutations in the SARS-CoV-2 genome were detected. Our results illustrate how wastewater can be used to investigate the diversity of SARS-CoV-2 viruses circulating in a community and identify new outbreaks.
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http://dx.doi.org/10.3201/eid2705.204410DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8084483PMC
May 2021

Economic evaluation of whole genome sequencing for pathogen identification and surveillance - results of case studies in Europe and the Americas 2016 to 2019.

Euro Surveill 2021 Mar;26(9)

Friedrich-Loeffler-Institut, Greifswald, Germany.

BackgroundWhole genome sequencing (WGS) is increasingly used for pathogen identification and surveillance.AimWe evaluated costs and benefits of routine WGS through case studies at eight reference laboratories in Europe and the Americas which conduct pathogen surveillance for avian influenza (two laboratories), human influenza (one laboratory) and food-borne pathogens (five laboratories).MethodsThe evaluation focused on the institutional perspective, i.e. the 'investment case' for implementing WGS compared with conventional methods, based on costs and benefits during a defined reference period, mostly covering at least part of 2017. A break-even analysis estimated the number of cases of illness (for the example of surveillance) that would need to be avoided through WGS in order to 'break even' on costs.ResultsOn a per-sample basis, WGS was between 1.2 and 4.3 times more expensive than routine conventional methods. However, WGS brought major benefits for pathogen identification and surveillance, substantially changing laboratory workflows, analytical processes and outbreaks detection and control. Between 0.2% and 1.1% (on average 0.7%) of reported salmonellosis cases would need to be prevented to break even with respect to the additional costs of WGS.ConclusionsEven at cost levels documented here, WGS provides a level of additional information that more than balances the additional costs if used effectively. The substantial cost differences for WGS between reference laboratories were due to economies of scale, degree of automation, sequencing technology used and institutional discounts for equipment and consumables, as well as the extent to which sequencers are used at full capacity.
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http://dx.doi.org/10.2807/1560-7917.ES.2021.26.9.1900606DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7934224PMC
March 2021

Metagenomics-Based Approach to Source-Attribution of Antimicrobial Resistance Determinants - Identification of Reservoir Resistome Signatures.

Front Microbiol 2020 15;11:601407. Epub 2021 Jan 15.

Division of Genomic Epidemiology, National Food Institute, Technical University of Denmark, Kgs Lyngby, Denmark.

Metagenomics can unveil the genetic content of the total microbiota in different environments, such as food products and the guts of humans and livestock. It is therefore considered of great potential to investigate the transmission of foodborne hazards as part of source-attribution studies. Source-attribution of antimicrobial resistance (AMR) has traditionally relied on pathogen isolation, while metagenomics allows investigating the full span of AMR determinants. In this study, we hypothesized that the relative abundance of fecal resistome components can be associated with specific reservoirs, and that resistomes can be used for AMR source-attribution. We used shotgun-sequences from fecal samples of pigs, broilers, turkeys- and veal calves collected across Europe, and fecal samples from humans occupationally exposed to livestock in one country (pig slaughterhouse workers, pig and broiler farmers). We applied both hierarchical and flat forms of the supervised classification ensemble algorithm Random Forests to classify resistomes into corresponding reservoir classes. We identified country-specific and -independent AMR determinants, and assessed the impact of country-specific determinants when attributing AMR resistance in humans. Additionally, we performed a similarity percentage analysis with the full spectrum of AMR determinants to identify resistome signatures for the different reservoirs. We showed that the number of AMR determinants necessary to attribute a resistome into the correct reservoir increases with a larger reservoir heterogeneity, and that the impact of country-specific resistome signatures on prediction varies between countries. We predicted a higher occupational exposure to AMR determinants among workers exposed to pigs than among those exposed to broilers. Additionally, results suggested that AMR exposure on pig farms was higher than in pig slaughterhouses. Human resistomes were more similar to pig and veal calves' resistomes than to those of broilers and turkeys, and the majority of these resistome dissimilarities can be explained by a small set of AMR determinants. We identified resistome signatures for each individual reservoir, which include AMR determinants significantly associated with on-farm antimicrobial use. We attributed human resistomes to different livestock reservoirs using Random Forests, which allowed identifying pigs as a potential source of AMR in humans. This study thus demonstrates that it is possible to apply metagenomics in AMR source-attribution.
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http://dx.doi.org/10.3389/fmicb.2020.601407DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7843941PMC
January 2021

Metagenomics analysis of bacteriophages and antimicrobial resistance from global urban sewage.

Sci Rep 2021 01 15;11(1):1600. Epub 2021 Jan 15.

Research Group for Genomic Epidemiology, National Food Institute, Technical University of Denmark, Building 204, 2800, Kemitorvet, Kgs. Lyngby, Denmark.

Bacteriophages, or phages, are ubiquitous bacterial and archaeal viruses with an estimated total global population of 10. It is well-known that wherever there are bacteria, their phage counterparts will be found, aiding in shaping the bacterial population. The present study used metagenomic data from global influent sewage in 79 cities in 60 countries to identify phages associated with bacteria and to explore their potential role in antimicrobial resistance gene (ARG) dissemination. The reads were mapped to known databases for bacteriophages and their abundances determined and correlated to geographic origin and the countries socio-economic status, as well as the abundances of bacterial species and ARG. We found that some phages were not equally distributed on a global scale, but their distribution was rather dictated by region and the socioeconomic status of the specific countries. This study provides a preliminary insight into the global and regional distribution of phages and their potential impact on the transmission of ARGs between bacteria. Moreover, the findings may indicate that phages in sewage could have adopted a lytic lifestyle, meaning that most may not be associated with bacteria and instead may be widely distributed as free-living phages, which are known to persist longer in the environment than their hosts. In addition, a significant correlation between phages and ARGs was obtained, indicating that phages may play a role in ARG dissemination. However, further analyses are needed to establish the true relationship between phages and ARGs due to a low abundance of the phages identified.
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http://dx.doi.org/10.1038/s41598-021-80990-6DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7810828PMC
January 2021

Salmonella enterica serovar Typhi H58 clone has been endemic in Zimbabwe from 2012 to 2019.

J Antimicrob Chemother 2021 04;76(5):1160-1167

Department of Medical Microbiology, University of Pretoria, Pretoria, South Africa.

Background: Typhoid fever, caused by S. enterica ser. Typhi, continues to be a substantial health burden in developing countries. Little is known of the genotypic diversity of S. enterica ser. Typhi in Zimbabwe, but this is key for understanding the emergence and spread of this pathogen and devising interventions for its control.

Objectives: To report the molecular epidemiology of S. enterica ser. Typhi outbreak strains circulating from 2012 to 2019 in Zimbabwe, using comparative genomics.

Methods: A review of typhoid cases records from 2012 to 2019 in Zimbabwe was performed. The phylogenetic relationship of outbreak isolates from 2012 to 2019 and emergence of antibiotic resistance was investigated by whole-genome sequence analysis.

Results: A total 22 479 suspected typhoid cases, 760 confirmed cases were reported from 2012 to 2019 and 29 isolates were sequenced. The majority of the sequenced isolates were predicted to confer resistance to aminoglycosides, β-lactams, phenicols, sulphonamides, tetracycline and fluoroquinolones (including qnrS detection). The qnrS1 gene was associated with an IncN (subtype PST3) plasmid in 79% of the isolates. Whole-genome SNP analysis, SNP-based haplotyping and resistance determinant analysis showed that 93% of the isolates belonged to a single clade represented by multidrug-resistant H58 lineage I (4.3.1.1), with a maximum pair-wise distance of 22 SNPs.

Conclusions: This study has provided detailed genotypic characterization of the outbreak strain, identified as S. Typhi 4.3.1.1 (H58). The strain has reduced susceptibility to ciprofloxacin due to qnrS carried by an IncN (subtype PST3) plasmid resulting from ongoing evolution to full resistance.
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http://dx.doi.org/10.1093/jac/dkaa519DOI Listing
April 2021

Expansion of a Subset Within the C2 Subclade of Sequence Type 131 (ST131) Is Driving the Increasing Rates of Aminoglycoside Resistance.

Open Forum Infect Dis 2020 Nov 8;7(11):ofaa410. Epub 2020 Sep 8.

Section for Genomic Epidemiology, National Food Institute, Technical University of Denmark, Lyngby, Denmark.

Background: Sequence type 131 (ST131) of is a pandemic clone that drives the increasing rates of antibiotic resistance. While the pervasiveness of ST131 clade C, especially subclades C2 and C1-M27, has been demonstrated in numerous global surveys, no report about the ST131 clades and their virotypes has been published from Iran so far.

Methods: A collection of 73 consecutive ST131 isolates from extraintestinal specimens was investigated for determination of virotypes, antibiotic susceptibility patterns, resistance/virulence determinants, and clade subsets.

Results: Most of the isolates belonged to subclade C2 (33/73; 45.2%), which had the highest virulence factor (VF) scores and resistance rates, followed by C1-M27 (18; 24.6%), C1-non-M27 (14; 19.1%), and A (8; 10.9%). The distinctive profiles of subclade C2 virulence genes were revealed by principle coordinates analysis testing. The distribution of the virulence gene among subclade C2 was not uniform, so that positive strains (21; 63.6%) showed significantly higher rates of resistance ( , , , , ) and virulence (, , , , , ) markers and gentamicin/tobramycin resistance. Virotype C as the most common virotype (34; 46.5%) was predominant among the subclade C1 population, while virotypes E and F (21; 28.7%) were detected among subclade C2, which had the highest VF scores and aminoglycoside resistance rates.

Conclusions: The appearance of virotypes E and F among subclade C2 strains with higher rates of aminoglycoside resistance/virulence gene content shows the shifting dynamics of this pandemic clone in response to antibiotic selection pressure by establishing subsets with higher survival potential.
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http://dx.doi.org/10.1093/ofid/ofaa410DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7691798PMC
November 2020

A metagenomic glimpse into the gut of wild and domestic animals: Quantification of antimicrobial resistance and more.

PLoS One 2020 3;15(12):e0242987. Epub 2020 Dec 3.

Department of Microbiology, National Veterinary Research Institute, Puławy, Poland.

Antimicrobial resistance (AMR) in bacteria is a complex subject, why one need to look at this phenomenon from a wider and holistic perspective. The extensive use of the same antimicrobial classes in human and veterinary medicine as well as horticulture is one of the main drivers for the AMR selection. Here, we applied shotgun metagenomics to investigate the AMR epidemiology in several animal species including farm animals, which are often exposed to antimicrobial treatment opposed to an unique set of wild animals that seems not to be subjected to antimicrobial pressure. The comparison of the domestic and wild animals allowed to investigate the possible anthropogenic impact on AMR spread. Inclusion of animals with different feeding behaviors (carnivores, omnivores) enabled to further assess which AMR genes that thrives within the food chain. We tested fecal samples not only of intensively produced chickens, turkeys, and pigs, but also of wild animals such as wild boars, red foxes, and rodents. A multi-directional approach mapping obtained sequences to several databases provided insight into the occurrence of the different AMR genes. The method applied enabled also analysis of other factors that may influence AMR of intestinal microbiome such as diet. Our findings confirmed higher levels of AMR in farm animals than in wildlife. The results also revealed the potential of wildlife in the AMR dissemination. Particularly in red foxes, we found evidence of several AMR genes conferring resistance to critically important antimicrobials like quinolones and cephalosporins. In contrast, the lowest abundance of AMR was observed in rodents originating from natural environment with presumed limited exposure to antimicrobials. Shotgun metagenomics enabled us to demonstrate that discrepancies between AMR profiles found in the intestinal microbiome of various animals probably resulted from the different antimicrobial exposure, habitats, and behavior of the tested animal species.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0242987PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7714112PMC
February 2021

Metagenomics-Based Proficiency Test of Smoked Salmon Spiked with a Mock Community.

Microorganisms 2020 Nov 25;8(12). Epub 2020 Nov 25.

Department of Veterinary Medical Sciences, University of Bologna, Via Tolara di Sopra 50, 40064 Ozzano dell'Emilia, Italy.

An inter-laboratory proficiency test was organized to assess the ability of participants to perform shotgun metagenomic sequencing of cold smoked salmon, experimentally spiked with a mock community composed of six bacteria, one parasite, one yeast, one DNA, and two RNA viruses. Each participant applied its in-house wet-lab workflow(s) to obtain the metagenomic dataset(s), which were then collected and analyzed using MG-RAST. A total of 27 datasets were analyzed. Sample pre-processing, DNA extraction protocol, library preparation kit, and sequencing platform, influenced the abundance of specific microorganisms of the mock community. Our results highlight that despite differences in wet-lab protocols, the reads corresponding to the mock community members spiked in the cold smoked salmon, were both detected and quantified in terms of relative abundance, in the metagenomic datasets, proving the suitability of shotgun metagenomic sequencing as a genomic tool to detect microorganisms belonging to different domains in the same food matrix. The implementation of standardized wet-lab protocols would highly facilitate the comparability of shotgun metagenomic sequencing dataset across laboratories and sectors. Moreover, there is a need for clearly defining a sequencing reads threshold, to consider pathogens as detected or undetected in a food sample.
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http://dx.doi.org/10.3390/microorganisms8121861DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7760972PMC
November 2020

Long-Term Temporal Stability of the Resistome in Sewage from Copenhagen.

mSystems 2020 Oct 20;5(5). Epub 2020 Oct 20.

Research Group for Genomic Epidemiology, National Food Institute, Technical University of Denmark, Kongens Lyngby, Denmark.

Antimicrobial resistance (AMR) is a major threat to global health, and it is crucial to understand the epidemiological aspects in order to predict the emergence and propagation of AMR genes. The aim of this study was to assess the variability and medium-term AMR trends within the mostly healthy human population of a single city. We monitored over 36 months (November 2015 to November 2018) the AMR level in the city of Copenhagen, Denmark, by taking bi-weekly sewage samples from the inlets of the three main water treatment plants, extracting the DNA, performing metagenomic sequencing, and read-mapping against a database of known AMR genes. We found that the AMR level was surprisingly stable with no periodic variability and no signs of drift over the measured period. We found, however, that the seemingly random variations at each site correlate in time with each other, suggesting that the variations we see are due to real environmental changes in the occurrence of AMR. The Copenhagen sewage resistome is surprisingly stable in time. The implication is that, at least for cities that are comparable to Copenhagen in terms of sewer infrastructure, few or even single samples provide a robust picture of the resistome within a city.
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http://dx.doi.org/10.1128/mSystems.00841-20DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7577296PMC
October 2020

Detection of mobile genetic elements associated with antibiotic resistance in Salmonella enterica using a newly developed web tool: MobileElementFinder.

J Antimicrob Chemother 2021 01;76(1):101-109

National Food Institute, Technical University of Denmark, 2800 Kgs. Lyngby, Denmark.

Objectives: Antimicrobial resistance (AMR) in clinically relevant bacteria is a growing threat to public health globally. In these bacteria, antimicrobial resistance genes are often associated with mobile genetic elements (MGEs), which promote their mobility, enabling them to rapidly spread throughout a bacterial community.

Methods: The tool MobileElementFinder was developed to enable rapid detection of MGEs and their genetic context in assembled sequence data. MGEs are detected based on sequence similarity to a database of 4452 known elements augmented with annotation of resistance genes, virulence factors and detection of plasmids.

Results: MobileElementFinder was applied to analyse the mobilome of 1725 sequenced Salmonella enterica isolates of animal origin from Denmark, Germany and the USA. We found that the MGEs were seemingly conserved according to multilocus ST and not restricted to either the host or the country of origin. Moreover, we identified putative translocatable units for specific aminoglycoside, sulphonamide and tetracycline genes. Several putative composite transposons were predicted that could mobilize, among others, AMR, metal resistance and phosphodiesterase genes associated with macrophage survivability. This is, to our knowledge, the first time the phosphodiesterase-like pdeL has been found to be potentially mobilized into S. enterica.

Conclusions: MobileElementFinder is a powerful tool to study the epidemiology of MGEs in a large number of genome sequences and to determine the potential for genomic plasticity of bacteria. This web service provides a convenient method of detecting MGEs in assembled sequence data. MobileElementFinder can be accessed at https://cge.cbs.dtu.dk/services/MobileElementFinder/.
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http://dx.doi.org/10.1093/jac/dkaa390DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7729385PMC
January 2021

Setting a baseline for global urban virome surveillance in sewage.

Sci Rep 2020 08 13;10(1):13748. Epub 2020 Aug 13.

Viroscience Department, Erasmus Medical Center, Rotterdam, The Netherlands.

The rapid development of megacities, and their growing connectedness across the world is becoming a distinct driver for emerging disease outbreaks. Early detection of unusual disease emergence and spread should therefore include such cities as part of risk-based surveillance. A catch-all metagenomic sequencing approach of urban sewage could potentially provide an unbiased insight into the dynamics of viral pathogens circulating in a community irrespective of access to care, a potential which already has been proven for the surveillance of poliovirus. Here, we present a detailed characterization of sewage viromes from a snapshot of 81 high density urban areas across the globe, including in-depth assessment of potential biases, as a proof of concept for catch-all viral pathogen surveillance. We show the ability to detect a wide range of viruses and geographical and seasonal differences for specific viral groups. Our findings offer a cross-sectional baseline for further research in viral surveillance from urban sewage samples and place previous studies in a global perspective.
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http://dx.doi.org/10.1038/s41598-020-69869-0DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7426863PMC
August 2020

ResFinder 4.0 for predictions of phenotypes from genotypes.

J Antimicrob Chemother 2020 12;75(12):3491-3500

National Institute of Agrarian and Veterinary Research (INIAV), National Reference Laboratory for Animal Health, Oeiras, Portugal.

Objectives: WGS-based antimicrobial susceptibility testing (AST) is as reliable as phenotypic AST for several antimicrobial/bacterial species combinations. However, routine use of WGS-based AST is hindered by the need for bioinformatics skills and knowledge of antimicrobial resistance (AMR) determinants to operate the vast majority of tools developed to date. By leveraging on ResFinder and PointFinder, two freely accessible tools that can also assist users without bioinformatics skills, we aimed at increasing their speed and providing an easily interpretable antibiogram as output.

Methods: The ResFinder code was re-written to process raw reads and use Kmer-based alignment. The existing ResFinder and PointFinder databases were revised and expanded. Additional databases were developed including a genotype-to-phenotype key associating each AMR determinant with a phenotype at the antimicrobial compound level, and species-specific panels for in silico antibiograms. ResFinder 4.0 was validated using Escherichia coli (n = 584), Salmonella spp. (n = 1081), Campylobacter jejuni (n = 239), Enterococcus faecium (n = 106), Enterococcus faecalis (n = 50) and Staphylococcus aureus (n = 163) exhibiting different AST profiles, and from different human and animal sources and geographical origins.

Results: Genotype-phenotype concordance was ≥95% for 46/51 and 25/32 of the antimicrobial/species combinations evaluated for Gram-negative and Gram-positive bacteria, respectively. When genotype-phenotype concordance was <95%, discrepancies were mainly linked to criteria for interpretation of phenotypic tests and suboptimal sequence quality, and not to ResFinder 4.0 performance.

Conclusions: WGS-based AST using ResFinder 4.0 provides in silico antibiograms as reliable as those obtained by phenotypic AST at least for the bacterial species/antimicrobial agents of major public health relevance considered.
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http://dx.doi.org/10.1093/jac/dkaa345DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7662176PMC
December 2020

Farm dust resistomes and bacterial microbiomes in European poultry and pig farms.

Environ Int 2020 10 29;143:105971. Epub 2020 Jul 29.

Institute for Risk Assessment Sciences, Utrecht University, Yalelaan 2, 3584 CM Utrecht, the Netherlands; Centre for Infectious Disease Control, National Institute for Public Health and the Environment, Antonie van Leeuwenhoeklaan 9, 3721MA Bilthoven, the Netherlands.

Background: Livestock farms are a reservoir of antimicrobial resistant bacteria from feces. Airborne dust-bound bacteria can spread across the barn and to the outdoor environment. Therefore, exposure to farm dust may be of concern for animals, farmers and neighboring residents. Although dust is a potential route of transmission, little is known about the resistome and bacterial microbiome of farm dust.

Objectives: We describe the resistome and bacterial microbiome of pig and poultry farm dust and their relation with animal feces resistomes and bacterial microbiomes, and on-farm antimicrobial usage (AMU). In addition, the relation between dust and farmers' stool resistomes was explored.

Methods: In the EFFORT-study, resistomes and bacterial microbiomes of indoor farm dust collected on Electrostatic Dust fall Collectors (EDCs), and animal feces of 35 conventional broiler and 44 farrow-to-finish pig farms from nine European countries were determined by shotgun metagenomic analysis. The analysis also included 79 stool samples from farmers working or living at 12 broiler and 19 pig farms and 46 human controls. Relative abundance of and variation in resistome and bacterial composition of farm dust was described and compared to animal feces and farmers' stool.

Results: The farm dust resistome contained a large variety of antimicrobial resistance genes (ARGs); more than the animal fecal resistome. For both poultry and pigs, composition of dust resistomes finds (partly) its origin in animal feces as dust resistomes correlated significantly with fecal resistomes. The dust bacterial microbiome also correlated significantly with the dust resistome composition. A positive association between AMU in animals on the farm and the total abundance of the dust resistome was found. Occupational exposure to pig farm dust or animal feces may contribute to farmers' resistomes, however no major shifts in farmers resistome towards feces or dust resistomes were found in this study.

Conclusion: Poultry and pig farm dust resistomes are rich and abundant and associated with the fecal resistome of the animals and the dust bacterial microbiome.
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http://dx.doi.org/10.1016/j.envint.2020.105971DOI Listing
October 2020

Description and determinants of the faecal resistome and microbiome of farmers and slaughterhouse workers: A metagenome-wide cross-sectional study.

Environ Int 2020 10 14;143:105939. Epub 2020 Jul 14.

Institute for Risk Assessment Sciences, Faculty of Veterinary Medicine, Utrecht University, Yalelaan 2, 3584 CM Utrecht, the Netherlands.

Background: By studying the entire human faecal resistome and associated microbiome, the diversity and abundance of faecal antimicrobial resistance genes (ARGs) can be comprehensively characterized. Prior culture-based studies have shown associations between occupational exposure to livestock and carriage of specific antimicrobial resistant bacteria. Using shotgun metagenomics, the present study investigated 194 faecal resistomes and bacteriomes from humans occupationally exposed to ARGs in livestock (i.e. pig and poultry farmers, employees and family members and pig slaughterhouse workers) and a control population (Lifelines cohort) in the Netherlands. In addition, we sought to identify determinants for the human resistome and bacteriome composition by applying a combination of multivariate (NMDS, PERMANOVA, SIMPER and DESeq2 analysis) and multivariable regression analysis techniques.

Results: Pig slaughterhouse workers and pig farmers carried higher total ARG abundances in their stools compared to broiler farmers and control subjects. Tetracycline, β-lactam and macrolide resistance gene clusters dominated the resistome of all studied groups. No significant resistome alpha diversity differences were found among the four populations. However, the resistome beta diversity showed a separation of the mean resistome composition of pig and pork exposed workers from broiler farmers and controls, independent of their antimicrobial use. We demonstrated differences in resistome composition between slaughter line positions, pig versus poultry exposed workers, as well as differences between farmers and employees versus family members. In addition, we found a significant correlation between the bacteriome and resistome, and significant differences in the bacteriome composition between and within the studied subpopulations. Finally, an in-depth analysis of pig and poultry farms - of which also farm livestock resistomes were analysed - showed positive associations between the number of on-farm working hours and human faecal AMR loads.

Conclusion: We found that the total normalized faecal ARG carriage was larger in persons working in the Dutch pork production chain compared to poultry farmers and controls. Additionally, we showed significant differences in resistome and bacteriome composition of pig and pork exposed workers compared to a control group, as well as within-population (farms, slaughterhouse) compositional differences. The number of on-farm working hours and the farm type (pig or broiler) that persons live or work on are determinants for the human faecal resistome. Overall, our results may suggest direct or indirect livestock contact as a determinant for human ARG carriage. Future studies should further focus on the connection between the human and livestock resistome (i.e. transmission routes) to substantiate the evidence for livestock-associated resistome acquisition.
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http://dx.doi.org/10.1016/j.envint.2020.105939DOI Listing
October 2020

Accelerating surveillance and research of antimicrobial resistance - an online repository for sharing of antimicrobial susceptibility data associated with whole-genome sequences.

Microb Genom 2020 05 30;6(5). Epub 2020 Mar 30.

See the full list of the COMPARE ML-AMR group members, in acknowledgements.

Antimicrobial resistance (AMR) is an emerging threat to modern medicine. Improved diagnostics and surveillance of resistant bacteria require the development of next-generation analysis tools and collaboration between international partners. Here, we present the 'AMR Data Hub', an online infrastructure for storage and sharing of structured phenotypic AMR data linked to bacterial whole-genome sequences. Leveraging infrastructure built by the European COMPARE Consortium and structured around the European Nucleotide Archive (ENA), the AMR Data Hub already provides an extensive data collection of more than 2500 isolates with linked genome and AMR data. Representing these data in standardized formats, we provide tools for the validation and submission of new data and services supporting search, browse and retrieval. The current collection was created through a collaboration by several partners from the European COMPARE Consortium, demonstrating the capacities and utility of the AMR Data Hub and its associated tools. We anticipate growth of content and offer the hub as a basis for future research into methods to explore and predict AMR.
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http://dx.doi.org/10.1099/mgen.0.000342DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7371118PMC
May 2020

The gut microbiome but not the resistome is associated with urogenital schistosomiasis in preschool-aged children.

Commun Biol 2020 04 2;3(1):155. Epub 2020 Apr 2.

Institute of Immunology & Infection Research, University of Edinburgh, Ashworth Laboratories, King's Buildings, Charlotte Auerbach Road, Edinburgh, EH9 3FL, UK.

Helminth parasites have been shown to have systemic effects in the host. Using shotgun metagenomic sequencing, we characterise the gut microbiome and resistome of 113 Zimbabwean preschool-aged children (1-5 years). We test the hypothesis that infection with the human helminth parasite, Schistosoma haematobium, is associated with changes in gut microbial and antimicrobial resistance gene abundance/diversity. Here, we show that bacteria phyla Bacteroidetes, Firmicutes, Proteobacteria, and fungi phyla Ascomycota, Microsporidia, Zoopagomycota dominate the microbiome. The abundance of Proteobacteria, Ascomycota, and Basidiomycota differ between schistosome-infected versus uninfected children. Specifically, infection is associated with increases in Pseudomonas, Stenotrophomonas, Derxia, Thalassospira, Aspergillus, Tricholoma, and Periglandula, with a decrease in Azospirillum. We find 262 AMR genes, from 12 functional drug classes, but no association with individual-specific data. To our knowledge, we describe a novel metagenomic dataset of Zimbabwean preschool-aged children, indicating an association between urogenital schistosome infection and changes in the gut microbiome.
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http://dx.doi.org/10.1038/s42003-020-0859-7DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7118151PMC
April 2020

Large scale automated phylogenomic analysis of bacterial isolates and the Evergreen Online platform.

Commun Biol 2020 03 20;3(1):137. Epub 2020 Mar 20.

Research Group for Genomic Epidemiology, National Food Institute, Technical University of Denmark, Kongens Lyngby, Denmark.

Public health authorities whole-genome sequence thousands of isolates each month for microbial diagnostics and surveillance of pathogenic bacteria. The computational methods have not kept up with the deluge of data and the need for real-time results. We have therefore created a bioinformatics pipeline for rapid subtyping and continuous phylogenomic analysis of bacterial samples, suited for large-scale surveillance. The data is divided into sets by mapping to reference genomes, then consensus sequences are generated. Nucleotide based genetic distance is calculated between the sequences in each set, and isolates are clustered together at 10 single-nucleotide polymorphisms. Phylogenetic trees are inferred from the non-redundant sequences and the clustered isolates are added back. The method is accurate at grouping outbreak strains together, while discriminating them from non-outbreak strains. The pipeline is applied in Evergreen Online, which processes publicly available sequencing data from foodborne bacterial pathogens on a daily basis, updating phylogenetic trees as needed.
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http://dx.doi.org/10.1038/s42003-020-0869-5DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7083913PMC
March 2020

Metaphylogenetic analysis of global sewage reveals that bacterial strains associated with human disease show less degree of geographic clustering.

Sci Rep 2020 02 20;10(1):3033. Epub 2020 Feb 20.

DTU Food. Technical University of Denmark, Kongens Lyngby, Denmark, 2800, Danmark.

Knowledge about the difference in the global distribution of pathogens and non-pathogens is limited. Here, we investigate it using a multi-sample metagenomics phylogeny approach based on short-read metagenomic sequencing of sewage from 79 sites around the world. For each metagenomic sample, bacterial template genomes were identified in a non-redundant database of whole genome sequences. Reads were mapped to the templates identified in each sample. Phylogenetic trees were constructed for each template identified in multiple samples. The countries from which the samples were taken were grouped according to different definitions of world regions. For each tree, the tendency for regional clustering was determined. Phylogenetic trees representing 95 unique bacterial templates were created covering 4 to 71 samples. Varying degrees of regional clustering could be observed. The clustering was most pronounced for environmental bacterial species and human commensals, and less for colonizing opportunistic pathogens, opportunistic pathogens and pathogens. No pattern of significant difference in clustering between any of the organism classifications and country groupings according to income were observed. Our study suggests that while the same bacterial species might be found globally, there is a geographical regional selection or barrier to spread for individual clones of environmental and human commensal bacteria, whereas this is to a lesser degree the case for strains and clones of human pathogens and opportunistic pathogens.
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http://dx.doi.org/10.1038/s41598-020-59292-wDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7033184PMC
February 2020

Using sewage for surveillance of antimicrobial resistance.

Science 2020 Feb;367(6478):630-632

Usher Institute, University of Edinburgh, Edinburgh EH9 3FL, UK.

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http://dx.doi.org/10.1126/science.aba3432DOI Listing
February 2020
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