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1. Occurrence of Mobile Colistin Resistance Genes mcr-1–mcr-10 including Novel mcr Gene Variants in Different Pathotypes of Porcine Escherichia coli Isolates Collected in Germany from 2000 to 2021

Author

Lisa Göpel, Ellen Prenger-Berninghoff, Silver A. Wolf, Torsten Semmler, Rolf Bauerfeind, and Christa Ewers

Subjects
Escherichia coli, pathotype, mobile colistin resistance, mcr-1, mcr-4, mcr-5, Microbiology, QR1-502
Abstract

In the European Union, gastrointestinal disease in pigs is the main indication for the use of colistin, but large-scale epidemiologic data concerning the frequency of mobile colistin resistance (mcr) genes in pig-associated pathotypes of Escherichia coli (E. coli) are lacking. Multiplex polymerase chain reactions were used to detect virulence-associated genes (VAGs) and mcr-1–mcr-10 genes in 10,573 porcine E. coli isolates collected in Germany from July 2000 to December 2021. Whole genome sequencing was performed on 220 representative mcr-positive E. coli strains. The total frequency of mcr genes was 10.2%, the most frequent being mcr-1 (8.4%) and mcr-4 (1.6%). All other mcr genes were rarely identified (mcr-2, mcr-3, mcr-5) or absent (mcr-6 to mcr-10). The highest frequencies of mcr genes were found in enterotoxigenic and shiga toxin-encoding E. coli (ETEC/STEC hybrid) and in edema disease E. coli (EDEC) strains (21.9% and 17.7%, respectively). We report three novel mcr variants, mcr-1.36, mcr-4.8, and mcr-5.5. In 39 attaching and effacing E. coli (AEEC) isolates analyzed in our study, the eae subtype β1 was the most prevalent (71.8%). Constant surveillance for the presence of mcr genes in various sectors should consider the different frequency of mcr-positive isolates in pathogenic E. coli.

Published
2023
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2. Antibiotic prophylaxis and hospitalization of horses subjected to median laparotomy: gut microbiota trajectories and abundance increase of Escherichia

Author

Anne Kauter, Julian Brombach, Antina Lübke-Becker, Dania Kannapin, Corinna Bang, Sören Franzenburg, Sabita D. Stoeckle, Alexander Mellmann, Natalie Scherff, Robin Köck, Sebastian Guenther, Lothar H. Wieler, Heidrun Gehlen, Torsten Semmler, Silver A. Wolf, and Birgit Walther

Subjects
horse, microbiome, gastrointestinal tract, microbiota, 16S rRNA gene sequencing, hospitalization, Microbiology, QR1-502
Abstract

IntroductionHorse clinics are hotspots for the accumulation and spread of clinically relevant and zoonotic multidrug-resistant bacteria, including extended-spectrum β-lactamase producing (ESBL) Enterobacterales. Although median laparotomy in cases of acute equine colic is a frequently performed surgical intervention, knowledge about the effects of peri-operative antibiotic prophylaxis (PAP) based on a combination of penicillin and gentamicin on the gut microbiota is limited.MethodsWe collected fecal samples of horses from a non-hospitalized control group (CG) and from horses receiving either a pre-surgical single-shot (SSG) or a peri-operative 5-day (5DG) course of PAP. To assess differences between the two PAP regimens and the CG, all samples obtained at hospital admission (t0), on days three (t1) and 10 (t2) after surgery, were screened for ESBL-producing Enterobacterales and subjected to 16S rRNA V1–V2 gene sequencing.ResultsWe included 48 samples in the SSG (n = 16 horses), 45 in the 5DG (n = 15), and 20 in the CG (for t0 and t1, n = 10). Two samples of equine patients receiving antibiotic prophylaxis (6.5%) were positive for ESBL-producing Enterobacterales at t0, while this rate increased to 67% at t1 and decreased only slightly at t2 (61%). Shannon diversity index (SDI) was used to evaluate alpha-diversity changes, revealing there was no significant difference between horses suffering from acute colic (5DG, SDImean of 5.90, SSG, SDImean of 6.17) when compared to the CG (SDImean of 6.53) at t0. Alpha-diversity decreased significantly in both PAP groups at t1, while at t2 the onset of microbiome recovery was noticed. Although we did not identify a significant SDImean difference with respect to PAP duration, the community structure (beta-diversity) was considerably restricted in samples of the 5DG at t1, most likely due to the ongoing administration of antibiotics. An increased abundance of Enterobacteriaceae, especially Escherichia, was noted for both study groups at t1.ConclusionColic surgery and PAP drive the equine gut microbiome towards dysbiosis and reduced biodiversity that is accompanied by an increase of samples positive for ESBL-producing Enterobacterales. Further studies are needed to reveal important factors promoting the increase and residency of ESBL-producing Enterobacterales among hospitalized horses.

Published
2023
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3. Repeated Occurrence of Mobile Colistin Resistance Gene-Carrying Plasmids in Pathogenic Escherichia coli from German Pig Farms

Author

Lisa Göpel, Ellen Prenger-Berninghoff, Silver A. Wolf, Torsten Semmler, Rolf Bauerfeind, and Christa Ewers

Subjects
Escherichia coli, ETEC, EDEC, mobile colistin resistance, mcr-1, plasmid, Biology (General), QH301-705.5
Abstract

The global spread of plasmid-mediated mobile colistin resistance (mcr) genes threatens the vital role of colistin as a drug of last resort. We investigated whether the recurrent occurrence of specific E. coli pathotypes and plasmids in individual pig farms resulted from the continued presence or repeated reintroduction of distinct E. coli strains. E. coli isolates (n = 154) obtained from three pig farms with at least four consecutive years of mcr detection positive for virulence-associated genes (VAGs) predicting an intestinal pathogenic pathotype via polymerase chain reaction were analyzed. Detailed investigation of VAGs, antimicrobial resistance genes and plasmid Inc types was conducted using whole genome sequencing for 87 selected isolates. Sixty-one E. coli isolates harbored mcr-1, and one isolate carried mcr-4. On Farm 1, mcr-positive isolates were either edema disease E. coli (EDEC; 77.3%) or enterotoxigenic E. coli (ETEC; 22.7%). On Farm 2, all mcr-positive strains were ETEC, while mcr-positive isolates from Farm 3 showed a wider range of pathotypes. The mcr-1.1 gene was located on IncHI2 (Farm 1), IncX4 (Farm 2) or IncX4 and IncI2 plasmids (Farm 3). These findings suggest that various pathogenic E. coli strains play an important role in maintaining plasmid-encoded colistin resistance genes in the pig environment over time.

Published
2024
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4. ESBL-Type and AmpC-Type Beta-Lactamases in Third Generation Cephalosporin-Resistant Enterobacterales Isolated from Animal Feces in Madagascar

Author

Ulrich Schotte, Julian Ehlers, Johanna Nieter, Raphaël Rakotozandrindrainy, Silver A. Wolf, Torsten Semmler, Hagen Frickmann, Sven Poppert, and Christa Ewers

Subjects
cephalosporin resistance, fosfomycin, epidemiology, feces, animals, Madagascar, Veterinary medicine, SF600-1100, Zoology, QL1-991
Abstract

Third generation cephalosporin-resistant (3GCR) Enterobacterales are known to be prevalent in Madagascar, with high colonization or infection rates in particular in Madagascan patients. Extended spectrum beta-lactamases (ESBLs) have been reported to be the predominant underlying resistance mechanism in human isolates. So far, little is known on antimicrobial resistance and its molecular determinants in Enterobacterales and other bacteria causing enteric colonization of Madagascan wild animals. To address this topic, swabs from 49 animal stool droppings were collected in the Madagascan Tsimanapesotsa National Park and assessed by cultural growth of bacterial microorganisms on elective media. In addition to 7 Acinetobacter spp., a total of 31 Enterobacterales growing on elective agar for Enterobacterales could be isolated and subjected to whole genome sequencing. Enterobacter spp. was the most frequently isolated genus, and AmpC-type beta-lactamases were the quantitatively dominating molecular resistance mechanism. In contrast, the blaCTX-M-15 gene, which has repeatedly been associated with 3GC-resistance in Madagascan Enterobacterales from humans, was detected in a single Escherichia coli isolate only. The identification of the fosfomycin-resistance gene fosA in a high proportion of isolates is concerning, as fosfomycin is increasingly used to treat infections caused by multidrug-resistant bacteria. In conclusion, the proof-of-principle assessment indicated a high colonization rate of resistant bacteria in stool droppings of Madagascan wild animals with a particular focus on 3GCR Enterobacterales. Future studies should confirm these preliminary results in a more systematic way and assess the molecular relationship of animal and human isolates to identify potential routes of transmission.

Published
2024
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5. How to survive pig farming: Mechanism of SCCmec element deletion and metabolic stress adaptation in livestock-associated MRSA

Author

Charlotte Huber, Silver A. Wolf, Wilma Ziebuhr, Mark A. Holmes, Julia Assmann, Antina Lübke-Becker, Andrea Thürmer, Torsten Semmler, Julian Brombach, Astrid Bethe, Markus Bischoff, Lothar H. Wieler, Lennard Epping, and Birgit Walther

Subjects
methicillin resistant Staphylococcus aureus, livestock associated, SCCmec, transcriptome analysis, recombination, deletion, Microbiology, QR1-502
Abstract

Previous research on methicillin susceptible Staphylococcus aureus (MSSA) belonging to livestock-associated (LA-) sequence type (ST) 398, isolated from pigs and their local surroundings, indicated that differences between these MSSA and their methicillin resistant predecessors (MRSA) are often limited to the absence of the staphylococcal cassette chromosome mec (SCCmec) and few single nucleotide polymorphisms. So far, our understanding on how LA-MRSA endure the environmental conditions associated with pig-farming as well as the putative impact of this particular environment on the mobilisation of SCCmec elements is limited. Thus, we performed in-depth genomic and transcriptomic analyses using the LA-MRSA ST398 strain IMT38951 and its methicillin susceptible descendant. We identified a mosaic-structured SCCmec region including a putative replicative SCCmecVc which is absent from the MSSA chromosome through homologous recombination. Based on our data, such events occur between short repetitive sequences identified within and adjacent to two distinct alleles of the large cassette recombinase genes C (ccrC). We further evaluated the global transcriptomic response of MRSA ST398 to particular pig-farm associated conditions, i.e., contact with host proteins (porcine serum) and a high ammonia concentration. Differential expression of global regulators involved in stress response control were identified, i.e., ammonia-induced alternative sigma factor B-depending activation of genes for the alkaline shock protein 23, the heat shock response and the accessory gene regulator (agr)-controlled transcription of virulence factors. Exposure to serum transiently induced the transcription of distinct virulence factor encoding genes. Transcription of genes reported for mediating the loss of methicillin resistance, especially ccrC, was not significantly different compared to the unchallenged controls. We concluded that, from an evolutionary perspective, bacteria may save energy by incidentally dismissing a fully replicative SCCmec element in contrast to the induction of ccr genes on a population scale. Since the genomic SCCmec integration site is a hot-spot of recombination, occasional losses of elements of 16 kb size may restore capacities for the uptake of foreign genetic material. Subsequent spread of resistance, on the other hand, might depend on the autonomous replication machinery of the deleted SCCmec elements that probably enhance chances for reintegration of SCCmec into susceptible genomes by mere multiplication.

Published
2022
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6. Farming Practice Influences Antimicrobial Resistance Burden of Non-Aureus Staphylococci in Pig Husbandries

Author

Manonmani Soundararajan, Gabriella Marincola, Olivia Liong, Tessa Marciniak, Freya D. R. Wencker, Franka Hofmann, Hannah Schollenbruch, Iris Kobusch, Sabrina Linnemann, Silver A. Wolf, Mustafa Helal, Torsten Semmler, Birgit Walther, Christoph Schoen, Justin Nyasinga, Gunturu Revathi, Marc Boelhauve, and Wilma Ziebuhr

Subjects
non-aureus staphylococci, NAS, alternative pig farming, antimicrobial resistance, one-health approach, intervention strategies, Biology (General), QH301-705.5
Abstract

Non-aureus staphylococci (NAS) are ubiquitous bacteria in livestock-associated environments where they may act as reservoirs of antimicrobial resistance (AMR) genes for pathogens such as Staphylococcus aureus. Here, we tested whether housing conditions in pig farms could influence the overall AMR-NAS burden. Two hundred and forty porcine commensal and environmental NAS isolates from three different farm types (conventional, alternative, and organic) were tested for phenotypic antimicrobial susceptibility and subjected to whole genome sequencing. Genomic data were analysed regarding species identity and AMR gene carriage. Seventeen different NAS species were identified across all farm types. In contrast to conventional farms, no AMR genes were detectable towards methicillin, aminoglycosides, and phenicols in organic farms. Additionally, AMR genes to macrolides and tetracycline were rare among NAS in organic farms, while such genes were common in conventional husbandries. No differences in AMR detection existed between farm types regarding fosfomycin, lincosamides, fusidic acid, and heavy metal resistance gene presence. The combined data show that husbandry conditions influence the occurrence of resistant and multidrug-resistant bacteria in livestock, suggesting that changing husbandry practices may be an appropriate means of limiting the spread of AMR bacteria on farms.

Published
2022
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7. Frequency, Local Dynamics, and Genomic Characteristics of ESBL-Producing Escherichia coli Isolated From Specimens of Hospitalized Horses

Author

Anne Kauter, Lennard Epping, Fereshteh Ghazisaeedi, Antina Lübke-Becker, Silver A. Wolf, Dania Kannapin, Sabita D. Stoeckle, Torsten Semmler, Sebastian Günther, Heidrun Gehlen, and Birgit Walther

Subjects
horse, ESBL, Escherichia coli, antibiotic resistance, multidrug resistant, spread, Microbiology, QR1-502
Abstract

Previous research identified veterinary clinics as hotspots with respect to accumulation and spread of multidrug resistant extended-spectrum β-lactamase (ESBL)-producing Escherichia coli (EC). Therefore, promoting the prudent use of antibiotics to decrease selective pressure in that particular clinical environment is preferable to enhance biosecurity for animal patients and hospital staff. Accordingly, this study comparatively investigated the impact of two distinct perioperative antibiotic prophylaxis (PAP) regimens (short-term versus prolonged) on ESBL-EC carriage of horses subjected to colic surgery. While all horses received a combination of penicillin/gentamicin (P/G) as PAP, they were assigned to either the “single-shot group” (SSG) or the conventional “5-day group” (5DG). Fecal samples collected on arrival (t0), on the 3rd (t1) and on the 10th day after surgery (t2) were screened for ESBL-EC. All isolates were further investigated using whole genome sequences. In total, 81 of 98 horses met the inclusion criteria for this study. ESBL-EC identified in samples available at t0, t1 and t2 were 4.8% (SSG) and 9.7% (5DG), 37% (SSG) and 47.2% (5DG) as well as 55.6% (SSG) and 56.8% (5DG), respectively. Regardless of the P/G PAP regimen, horses were 9.12 times (95% CI 2.79–29.7) more likely to carry ESBL-EC at t1 compared to t0 (p < 0.001) and 15.64 times (95% CI 4.57–53.55) more likely to carry ESBL-EC at t2 compared to t0 (p < 0.001). ESBL-EC belonging to sequence type (ST) 10, ST86, ST641, and ST410 were the most prevalent lineages, with blaCTX–M–1 (60%) being the dominant ESBL gene. A close spatio-temporal relationship between isolates sharing a particular ST was revealed by genome analysis, strongly indicating local spread. Consequently, hospitalization itself has a strong impact on ESBL-EC isolation rates in horses, possibly masking differences between distinct PAP regimens. The results of this study reveal accumulation and spread of multi-drug resistant ESBL-EC among horses subjected to colic surgery with different P/G PAP regimens, challenging the local hygiene management system and work-place safety of veterinary staff. Moreover, the predominance of particular ESBL-EC lineages in clinics providing health care for horses needs further investigation.

Published
2021
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9. Antibiotic prophylaxis and hospitalization of horses subjected to median laparotomy: gut microbiota trajectories and abundance increase ofEscherichia

Author

Anne Kauter, Julian Brombach, Antina Lübke-Becker, Dania Kannapin, Corinna Bang, Sören Franzenburg, Sabita D. Stoeckle, Alexander Mellmann, Natalie Effelsberg, Robin Köck, Sebastian Guenther, Lothar H. Wieler, Heidrun Gehlen, Torsten Semmler, Silver A. Wolf, and Birgit Walther

Abstract

Horse clinics are hotspots for the accumulation and spread of clinically relevant and zoonotic multidrug-resistant bacteria, including extended-spectrum β-lactamase producing (ESBL) Enterobacterales. Although median laparotomy in cases of acute equine colic is a frequently performed surgical intervention, knowledge about the effects of peri-operative antibiotic prophylaxis (PAP) based on a combination of penicillin and gentamicin on the gut microbiota is limited. Therefore, we collected fecal samples of horses from a non-hospitalized control group (CG) and from horses receiving either a pre-surgical single-shot (SSG) or a peri-operative 5-day (5DG) course of PAP. To assess differences between the two PAP regimens and the CG, all samples obtained at hospital admission (t0), on days three (t1) and ten (t2) after surgery, were screened for ESBL-producing Enterobacterales and subjected to 16S rRNA V1– V2 gene sequencing.We included 48 samples in the SSG (n=16 horses), 45 in the 5DG (n=15) and 20 in the CG (n=10). Two samples (6.5%) were positive for ESBL-producing Enterobacterales at t0while this rate increased to 67% at t1and decreased only slightly at t2(61%). Shannon diversity index (SDI) was used to evaluate alpha-diversity changes, revealing that horses suffering from acute colic seemed to have a compromised fecal microbiota composition (5DG, SDImeanof 5.90; SSG, SDImeanof 6.17) when compared to the CG (SDImeanof 6.53) at t0, although the difference lacked significance. Alpha-diversity decreased significantly in both PAP groups at t1, while at t2the onset of microbiome recovery was noticed. Although we did not identify a significant SDImeandifference with respect to PAP duration, the community structure (beta-diversity) was considerably restricted in samples of the 5DG at t1, most likely due to the ongoing administration of antibiotics. An increased abundance ofEnterobacteriaceae,especiallyEscherichia, was noted for both study groups at t1. Further studies are needed to reveal important factors promoting the increase and residency of ESBL-producing Enterobacterales among hospitalized horses.

Published
2023
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10. Extended-spectrum beta-lactamase (ESBL)-producing Escherichia coli and Acinetobacter baumannii among horses entering a veterinary teaching hospital: The contemporary 'Trojan Horse'.

Author

Birgit Walther, Katja-Sophia Klein, Ann-Kristin Barton, Torsten Semmler, Charlotte Huber, Silver Anthony Wolf, Karsten Tedin, Roswitha Merle, Franziska Mitrach, Sebastian Guenther, Antina Lübke-Becker, and Heidrun Gehlen

Subjects
Medicine, Science
Abstract

Pathogens frequently associated with multi-drug resistant (MDR) phenotypes, including extended-spectrum beta-lactamase (ESBL)-producing Enterobacteriaceae (ESBL-E) and Acinetobacter baumannii isolated from horses admitted to horse clinics, pose a risk for animal patients and personnel in horse clinics. To estimate current rates of colonization, a total of 341 equine patients were screened for carriage of zoonotic indicator pathogens at hospital admission. Horses showing clinical signs associated with colic (n = 233) or open wounds (n = 108) were selected for microbiological examination of nostril swabs, faecal samples and wound swabs taken from the open wound group. The results showed alarming carriage rates of Gram-negative MDR pathogens in equine patients: 10.7% (34 of 318) of validated faecal specimens were positive for ESBL-E (94%: ESBL-producing Escherichia coli), with recorded rates of 10.5% for the colic and 11% for the open wound group. 92.7% of the ESBL-producing E. coli were phenotypically resistant to three or more classes of antimicrobials. A. baumannii was rarely detected (0.9%), and all faecal samples investigated were negative for Salmonella, both directly and after two enrichment steps. Screening results for the equine nostril swabs showed detection rates for ESBL-E of 3.4% among colic patients and 0.9% in the open wound group, with an average rate of 2.6% (9/340) for both indications. For all 41 ESBL-producing E. coli isolated, a broad heterogeneity was revealed using pulsed-field gel electrophoresis (PFGE) patterns and whole genome sequencing (WGS) -analysis. However, a predominance of sequence type complex (STC)10 and STC1250 was observed, including several novel STs. The most common genes associated with ESBL-production were identified as blaCTX-M-1 (31/41; 75.6%) and blaSHV-12 (24.4%). The results of this study reveal a disturbingly large fraction of multi-drug resistant and ESBL-producing E. coli among equine patients, posing a clear threat to established hygiene management systems and work-place safety of veterinary staff in horse clinics.

Published
2018
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11. Gene amplifications cause high-level resistance against albicidin in Gram-negative bacteria

Author

Mareike Saathoff, Simone Kosol, Torsten Semmler, Karsten Tedin, Nicole Dimos, Johannes Kupke, Maria Seidel, Fereshteh Ghazisaeedi, Silver A. Wolf, Benno Kuropka, Wojciech Czyszczoń, Dmitry Ghilarov, Stefan Grätz, Jonathan G. Heddle, Bernhard Loll, Roderich D. Süssmuth, and Marcus Fulde

Abstract

Antibiotic resistance is a continuously increasing concern for public health care. Understanding resistance mechanisms and their emergence is crucial for the development of new antibiotics and their effective use. Here, we report the discovery of a gene amplification-based mechanism that imparts an up to 1000-fold increase in resistance levels against the antibiotic albicidin. We show that this mechanism protects Salmonella Typhimurium and Escherichia coli by increasing the copy number of the GyrI-like transcription regulator STM3175 (YgiV) which binds albicidin. X-ray crystallography and molecular docking studies reveal a conserved binding motif that can interact with aromatic building blocks of albicidin. Phylogenetic studies suggest that this resistance mechanism is ubiquitous in Gram-negative bacteria and our experiments confirm that STM3175 homologs can convey resistance in pathogens such as Vibrio vulnificus and Pseudomonas aeruginosa.

Published
2022
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12. A global metagenomic map of urban microbiomes and antimicrobial resistance

Author

Nadine Farhat, Tomoki Takeda, Astred Castro, Ken McGrath, Khaliun Sanchir, Iman Hajirasouliha, Eunice So, Laraib Zafar, Diana N. Nunes, Harun Mustafa, Amy Zhang, Priscilla Lisboa, Christian Schori, Marisano James, Jasna Chalangal, Sebastien Halary, Shahryar Rana, Yunmi Lee, Oli Schacher, Liliana Godoy, David A. Coil, Phanthira Pugdeethosal, Michelle D. Williams, German Marchandon, Angela Cantillo, Naoya Takahashi, Christopher Mozsary, Juana Gonzalez, Patrick K. H. Lee, Gerardo de Lamotte, Alessandro Robertiello, Steven Du, Fabienne Velter, Stefan G. Stark, Miguel Carbajo, Vincent Matthys, David A. Westfall, Julia Boeri, Irène Mauricette Mendy, Jonathan Cedillo, Francesco Oteri, Robert W. Crawford, Takayuki Ito, Tina Wunderlin, Maureen Muscat, David Paez-Espino, Carmen Urgiles, Aida Nesimi, Steffen Schaaf, Adan Ramirez-Rojas, Kunihiko Miyake, Christopher E. Mason, Anais Cardenas, Sharah Islam, Diego Benítez, Melissa Pool Pizzi, Kianna Ciaramella, Ciro Borrelli, Riham Islam, Dorottya Nagy-Szakal, Abd-Manaaf Bakere, Ait-hamlat Adel, Olha Lakhneko, Badamnyambuu Iderzorig, Ana Valeria Castro, Adam Phillips, Robert A. Petit, Flavia Corsi, Romain Conte, Krista Ryon, Soojin Jang, Joseph Benson, Fernanda de Souza Gomes Kehdy, Cindy Wang, Nicole Mathews, Jenn-Wei Chen, Rachel Paras, Paulina Pastuszek, Abigail Lyons, Paul Roldán, Muntaha Munia, Pierre Nicolas, Cassie L. Ettinger, Kyrylo Pyrshev, Katterinne N. Mendez, Eduardo Castro-Nallar, Valeriia Dotsenko, Michelle Tuz, Krizzy Mallari, Eileen Png, Yuya Sonohara, Tanja Miketic, Stéphane Delmas, Shu Zhang, Masaki Sato, Yuanting Zheng, Jifeng Zhu, Roland Häusler, Lucie Bittner, Savlatjon Rahmatulloev, Jonathan Foox, Bruno D'Alessandro, Alketa Plaku, Faisal Alquaddoomi, Yang Zhang, Kern Rei Chng, Juliana Lago, Allaeddine Chettouh, Tamera Henry, Houtan Noushmehr, Tranette Gregory, Sara Abdul Majid, Frank J. Kelly, Benjamin Pulatov, Laurie Casalot, Takema Kajita, Lennard Epping, Thais Fernanda Bartelli, Eftar Moniruzzaman, Renee Vivancos-Koopman, Thirumalaisamy P. Velavan, Tracy W. Liu, Yelyzaveta Tymoshenko, Alma Plaku, Nika Gurianova, Ambar Mendez, Anna Tomaselli, Sonia Dorado, Donato Giovannelli, Hira Choudhry, Synti Ng, Sheelta S. Kumar, Jennifer Q. Lu, Weijun Liang, Ellen Koag, Dennis Gankin, Maria João Amorim, Gwenola Simon, Kiyoshi Suganuma, Mikhail Karasikov, Christos A. Ouzounis, Madelyn May, Eran Elhaik, Stephan Ossowski, Kevin Bolzli, Matthew Arthur, Yuya Oto, Jananan Pathmanathan, Salah Mahmoud, Kou Takahashi, Brunna Marques, Kelly French, Felipe Sepúlveda, Shusei Yoshikawa, Paulo Thiago de Souza Santos, Andrew N. Gray, Juliana S Bernardes, Felipe Segato, Björn Brindefalk, George C. Yeh, Jhovana L. Velasco Flores, Jill Sullivan, Silva Baburyan, Denisse Flores, Russell Y. Neches, Sabrina Persaud, Rasheena Wright, Takumi Togashi, Verónica Antelo, Nao Kato, Skye Felice, Tatjana Mustac, Daisy Donnellan, Katerine Carrillo, Anna Litskevitch, Catalina García, Sota Ito, Naya Eady, Andrew Wan, Irene Meng, Sophie Guasco, Danilo Ercolini, Francesca De Filippis, Vincent Lemaire, Luice Fan, Lothar H. Wieler, Mariia Rybak, Jorge Sanchez, Jonathan S. Gootenberg, Itsuki Tomita, Maritza S Mosella, Laura Garcia, Natalka Makogon, Daisy Cheung, Hitler Francois Vasquez Arevalo, Freddy Asenjo, Gabriela P. Branco, Erika Cifuentes, Chloé Dequeker, Aspassia D. Chatziefthimiou, Alexis Terrero, Roy Meoded, Isabelle de Oliveira Moraes, Shaleni K. Singh, Orgil-Erdene Molomjamts, Karishma Miah, Laurent David, Wolfgang Haehr, Dao Phuong Giang, Romain Lannes, Prashanthi Ratnanandan, Ryota Yamanaka, Riccardo Vicedomini, Sadaf Ayaz, Oluwatosin M. Osuolale, Laura E. Vann, Gregory Chem, Andrea Gonzalez, Aszia Burrell, Ariel Chernomoretz, Sakura Ishizuka, Michelle Rivera, Avigdor Nosrati, Michelle B. Chen, Juliette Auvinet, Nils Ordioni, Tomoro Warashina, Guillaume Blanc, Tomislav Ivankovic, Christina Black, Lauren E. Hittle, David Hess-Homeier, Michael Kozhar, Hamood Suliman, Karobi Moitra, Saher Rahiel, Spyridon Gkotzis, Jenny Arevalo, Shaikh B. Iqbal, Beth Mutai, Mohammed Mohsin, Scott Tighe, Sylvie Collin, Yoshitaka Saito, Wayne Menary, Youping Deng, Lucy Lee, Esmeralda Jiminez, Ayuki Watanabe, Nikos C. Kyrpides, Natasha Mohan, Angelika Pupiec, Dedan Githae, Simone Cawthorne, Jonathan A. Eisen, Tomoki Iwashiro, Chiaki Homma, Thomas Saw Aung, Laura Molina, Marcus H. Y. Leung, Ophélie Da Silva, Yan Ling Wong, Hosna Noorzi, Mario Moreno, Alina Butova, Leming Shi, Brian W. Wong, Sarah S. Jackson, Moses Lin, Annabelle Meagher, Pujita Das, Catherine Burke, Mitsuki Ota, Maria Domenica Moccia, Nicolas Sprinsky, Catherine E. Pugh, David C. Green, Fazlina Fauzi, Erdenetsetseg Batdelger, Annie Geiger, Valeria Ventorino, Tolulope Oluwadare, Delisia Cuebas, Catalina Truong, Leonardo Posada, Michael Angelov, Tathiane M. Malta, Amanda Ng, Francesca Nadalin, Arya Hawkins-Zafarnia, Yuh Shiwa, Athena Mitsios, Milton Ozório Moraes, Manolo Laiola, Kalyn Ali, Jaden J.A. Hastings, Ikuto Saito, Maheen Shakil, Chisato Suzuki, Elena M. Vayndorf, Hubert Rehrauer, Ajay Menon, Kaitlan Russell, Aliyah Shari, Rebecca Smith, Gregorio Iraola, Max Priestman, Alan Briones, Silver A. Wolf, Camila Gonzalez-Poblete, Eleonora De Lazzari, Shirley Chiu, Michelle Ki, Irene Hoxie, Marianne Jaubert, Ayantu Jinfessa, Ryan J. King, Nghiem Xuan Hoan, Jalia Bynoe, Jacob Friedman, Aneisa Ramcharan, Pablo Fresia, Cristina Muñoz, Muhammad Afaq, Anyi Tang, Médine Benchouaia, Isabella Kuniko T. Takenaka, Anastasia Chasapi, Areeg Naeem, Hannah Benisty, Cecilia N. Cossio, Nathalie Hüsser, Mahfuza Sabina, Thais S. Sabedot, JoAnn Jacobs, Camila P. E. de Souza, Manuela Oliveira, Jean-Pierre Bouly, Mariko Usui, Wilson Miranda, Natalia Marciniak, Hiram Caballero, Samuel Weekes, Alexandra B. Graf, Emily Leong, Tatyana Nikolayeva, Dominique Thomas, Charlotte Greselle, Cecilia Salazar, Sreya Ray Chaudhuri, Kevin Becher, Sandra Roth, Ryusei Miura, Kari Oline Bøifot, Dimitri Manoir, Oliver Toth, Chandrima Bhattacharya, Manuel Perez, Isha Lamba, Takafumi Tsurumaki, Timothy D. Read, Anna-Lena M. Schinke, Ryan Sankar, Le Huu Song, Narasimha Rao Nedunuri, Emmanuel Dias-Neto, Ana Flávia Costa, Adiell Melamed, Christelle Desnues, Natalie R. Davidson, Aaron E. Darling, Hyung Jun Kim, Josephine Galipon, Jacqueline Orrego, Dimitar Vassilev, Michael Huber, Nur Hazlin Hazrin-Chong, Gaston H. Gonnet, Kaymisha Knights, Osman U. Sezerman, Dmitry Meleshko, Eunice Thambiraja, Jingcheng Yang, Aubin Fleiss, Gloria Nguyen, Katelyn Jackson, Nuria Aventin, Stephanie L. Hyland, Andrea Hässig, Catharine Aquino, Simona Lysakova, Israel O. Osuolale, Kasia Sluzek, Rania Siam, Alina Frolova, Samuel Hernandez, Yui Him Lo, Bazartseren Boldgiv, Ben Young, Maryna Korshevniuk, Majelia Ampadu, Yuk Man Tang, Amanda L. Muehlbauer, Sade Thomas, Gabriel Figueroa, Alexis Rivera, Lisbeth Pineda, Alexandra Dutan, Jennifer M. Tran, Chris K. Deng, Vedbar S. Khadka, Paola Florez de Sessions, Elizabeth Humphries, Hugues Richard, Hiba Naveed, Nora C. Toussaint, Mahshid Khavari, Maria del Mar Vivanco Ruiz, Antonin Thiébaut, Nicolás Rascovan, Marius Dybwad, Orhan Özcan, Lawrence Kwong, David Danko, Shaira Khan, Andrea Tassinari, Silvia Beurmann, Tsoi Ying Lai, Nanami Kubota, Tieliu Shi, Diana Chicas, Evan E. Afshin, Hirokazu Yano, Jonas Krebs, Mayuko Nakagawa, Hyun Jung Lee, Irene González Navarrete, Rachid Ounit, Lucia E. Alvarado-Arnez, Masaki Nasu, Allison Chan, Harilanto Andrianjakarivony, Jennifer Amachee, Mahdi Taye, Wan Chiew Ng, Kathryn O’Brien, Shino Ishikawa, Tristan Bitard-Feildel, Sora Takagi, Felix Hartkopf, Niamh B. O’Hara, Marcos A. S. Fonseca, Subhamitra Pakrashi, Amrit Kaur, Eva Hell, Patricia Vera-Wolf, Naimah Munim, Luiza Ferreira de Araújo, Mizuki Igarashi, Brianna Pompa-Hogan, Alessandra Carbone, Anne-Sophie Benoiston, Eric Helfrich, Michael A. Suarez-Villamil, Omar O. Abudayyeh, Natasha Abdullah, Jaime J. Fuentes, Juan Carlos Forero, Tetiana Yeskova, Denis Bertrand, Sambhawa Priya, Denisse Maldonado, Agier Nicolas, Ana Valeria B Castro, Starr Chatziefthimiou, André Kahles, Aaishah Francis, Fernanda Arredondo, Emilio Tarcitano, Irvind Buttar, Alex Alexiev, Jennifer Molinet, Sarah Shalaby, Itunu A. Oluwadare, Jason Sperry, Katrin Bakhl, Ana M. Cañas, Sofia Ahsanuddin, Miar Elaskandrany, Elodie Laine, Sven Bönigk, Johannes Werner, Stephen Eduard Boja Ruiz, Gargi Dayama, Paulina Buczansla, Brandon Valentine, Bharath Prithiviraj, Toni Bode, Stas Zubenko, Jake Cohen, Guilllaume Jospin, Zulena Saravi, Per O. Ljungdahl, Inderjit Kaur, Mauricio Moldes, Giuseppe KoLoMonaco, Denise Syndercombe Court, Sonia Bouchard, Sonia Losim, Sookwon Moon, Heba Shaaban, Suraj Patel, Sibo Zhu, Sarh Aly, Arif Asyraf Md Supie, LaShonda Dorsey, Juan Guerra, François Baudon, Rantimi A. Olawoyin, Alexia Bordigoni, Iqra Faiz, Mathilde Garcia, Gabriella Mason-Buck, María Gabriela Portilla, Niranjan Nagarajan, Fumie Takahara, Nancy Merino, Watson Andrew, Gina Kim, Yuma Sato, Hyenah Shim, Marie-Laure Jerier, Affifah Saadah Ahmad Kassim, Katerina Kuchin, Daniel Butler, Paweł P. Łabaj, Nadezhda Kobko-Litskevitch, Emmanuel F. Mongodin, Yuto Togashi, Paula Rodríguez, Pilar Lopez Hernandez, Xiaoqing Chen, Maria A. Sierra, Olga Nikolayeva, Manon Loubens, Colleen Conger, Hikaru Shirahata, Chenhao Li, Timothy Donahoe, Youngja Park, Lucia Elena Alvarado Arnez, Salama Chaker, Francisco Chavez, Alessandra Breschi, Jorge L. Sanchez, Kaung Myat San, Nayra Aguilar Rojas, Marcos Abraao, Kai Sasaki, Bryan Nazario, Olena Yemets, Klas I. Udekwu, Lynn M. Schriml, Anisia Peters, Aliaksei Holik, Mark Hernandez, Emile Faure, Malay Bhattacharyya, Josef W. Moser, Núria Andreu Somavilla, María Mercedes Zambrano, Kannan Rajendran, Gabriela E. Albuquerque, Tao Qing, Kazutoshi Tsuda, Ymke De Jong, Princess Osma, Mayra Arauco Livia, Javier Quilez Oliete, Carl Chrispin, Hyun Woo Joo, Ingrid Lafontaine, Nala An, Seisuke Sato, Felipe Segato Dezem, Andrew Maltez Thomas, Alexandre Desert, Xiao Wen Cai, O. Osuolale, Jun Wu, Coral Pardo-Esté, Courtney Robinson, Yuri Matsuzaki, Marina Nieto-Caballero, Cem Meydan, Ralph Schlapbach, Mark Menor, Sofia Castro, Rachel Kwong, Brittany Blyther, Olexandr Lykhenko, Jason R. Schriml, Christian Brion, Jenessa Orpilla, Juan A. Ugalde, Elsy Mankah Ngwa, Álvaro Aranguren, Lauren Mak, Matías Giménez, Ashanti Narce, Torsten Semmler, Stefan I. Tsonev, Abdollahi Nika, Katherine E. Dahlhausen, Monika Devi, Gunnar Rätsch, Oasima Muner, Carla Bello, Muhammad Al-Fath Amran, Anyelic Rosario, Melissa Ortega, Andrea Patrignani, Ante Peros, Elias McComb, Ryo Sato, Ireen Alam, Clara N. Dias, Soma Tanaka, Dayana Calderon, Ran Blekhman, Mathilde Mignotte, Alicia Boyd, Jochen Hecht, Thomas Neff, Xinzhao Tong, Josue Alicea, Kiara Olmeda, Sonia Marinovic, Carme Arnan, Kohei Ito, Samantha L. Goldman, Marianna S. Serpa, Renee Richer, Kaisei Sato, Jordana M. Silva, Akash Keluth Chavan, Sangwan Kim, Laís Pereira Ferreira, Sophie Vacant, Nowshin Sayara, Haruo Suzuki, Madeline Leahy, Juan C. Severyn, Sierra Vincent, Masaru Tomita, Maliha Mamun, Lucinda B. Davenport, Gabriella Oken, Dagmara Lewandowska, Gustavo Adolfo Malca Salas, Andrii Kuklin, Tyler Wong, Charlie Feigin, Eric Minwei Liu, Sonia L. Ghose, Daniela Bezdan, Antonietta La Storia, Juan P. Escalera-Antezana, Nuno Rufino de Sousa, Samuel M. Gerner, Weill Cornell Medicine [New York], Icahn School of Medicine at Mount Sinai [New York] (MSSM), Genome Institute of Singapore (GIS), Centre for Genomic Regulation [Barcelona] (CRG), Universitat Pompeu Fabra [Barcelona] (UPF)-Centro Nacional de Analisis Genomico [Barcelona] (CNAG), Eidgenössische Technische Hochschule - Swiss Federal Institute of Technology [Zürich] (ETH Zürich), Lawrence Berkeley National Laboratory [Berkeley] (LBNL), AUTRES, Massachusetts Institute of Technology (MIT), Indian Statistical Institute [Kolkata], University of Minnesota System, Universidad Andrés Bello [Santiago] (UNAB), California State University [Sacramento], University of Naples Federico II, University of Hawaii, Institut méditerranéen d'océanologie (MIO), Institut de Recherche pour le Développement (IRD)-Aix Marseille Université (AMU)-Institut national des sciences de l'Univers (INSU - CNRS)-Centre National de la Recherche Scientifique (CNRS)-Université de Toulon (UTLN), Medical Genomics Group, University College of London [London] (UCL)-UCL Cancer Institute, Norwegian Defence Research Establishment (FFI), Lund University [Lund], Institute of Molecular Biology and Genetics of National Academy of Sciences of Ukraine, University of Vienna [Vienna], King‘s College London, University of Colorado [Boulder], Institut Pasteur de Montevideo, Réseau International des Instituts Pasteur (RIIP), Institut Pasteur Korea - Institut Pasteur de Corée, Fudan University [Shanghai], City University of Hong Kong [Hong Kong] (CUHK), Stockholm University, University of Maryland School of Medicine, University of Maryland System, Fundação Oswaldo Cruz (FIOCRUZ), University of São Paulo (USP), Instituto de Patologia e Imunologia Molecular da Universidade do Porto (IPATIMUP), Barcelona Institute of Science and Technology (BIST), Elizade University, Acibadem Mehmet Ali Aydınlar University, Paléogénomique microbienne - Microbial paleogenomics, Institut Pasteur [Paris]-Centre National de la Recherche Scientifique (CNRS), Sorbonne Université (SU), Robert Koch Institute [Berlin] (RKI), East China Normal University [Shangaï] (ECNU), Cairo University, Vietnamese-German Center for Medical Research, Keio University, Université du Vermont, Universidad del Desarrollo, University of Sofia, University of Alaska [Fairbanks] (UAF), Universitätsklinikum Tübingen - University Hospital of Tübingen, Eberhard Karls Universität Tübingen = Eberhard Karls University of Tuebingen, Corporación Corpogen-Research Center, Biologie Computationnelle et Quantitative = Laboratory of Computational and Quantitative Biology (LCQB), Sorbonne Université (SU)-Centre National de la Recherche Scientifique (CNRS)-Institut de Biologie Paris Seine (IBPS), Sorbonne Université (SU)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS), Weill Cornell Medicine [Cornell University], Cornell University [New York], University of Naples Federico II = Università degli studi di Napoli Federico II, Institut de Recherche pour le Développement (IRD)-Aix Marseille Université (AMU)-Institut national des sciences de l'Univers (INSU - CNRS)-Université de Toulon (UTLN)-Centre National de la Recherche Scientifique (CNRS), Fundação Oswaldo Cruz / Oswaldo Cruz Foundation (FIOCRUZ), Universidade de São Paulo = University of São Paulo (USP), Institut Pasteur [Paris] (IP)-Centre National de la Recherche Scientifique (CNRS), Софийски университет = Sofia University, Institut National de la Santé et de la Recherche Médicale (INSERM)-Sorbonne Université (SU)-Centre National de la Recherche Scientifique (CNRS)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS), Universidad Andrés Bello - UNAB (CHILE), Acibadem University Dspace, Danko, D., Bezdan, D., Afshin, E. 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F., Batdelger, E., Baudon, F., Becher, K., Bello, C., Benchouaia, M., Benisty, H., Benoiston, A. -S., Benson, J., Benitez, D., Bernardes, J., Bertrand, D., Beurmann, S., Bitard-Feildel, T., Bittner, L., Black, C., Blanc, G., Blyther, B., Bode, T., Boeri, J., Boldgiv, B., Bolzli, K., Bordigoni, A., Borrelli, C., Bouchard, S., Bouly, J. -P., Boyd, A., Branco, G. P., Breschi, A., Brindefalk, B., Brion, C., Briones, A., Buczansla, P., Burke, C. M., Burrell, A., Butova, A., Buttar, I., Bynoe, J., Bonigk, S., Boifot, K. O., Caballero, H., Cai, X. W., Calderon, D., Cantillo, A., Carbajo, M., Carbone, A., Cardenas, A., Carrillo, K., Casalot, L., Castro, S., Castro, A. V., Castro, A., Castro, A. V. B., Cawthorne, S., Cedillo, J., Chaker, S., Chalangal, J., Chan, A., Chasapi, A. I., Chatziefthimiou, S., Chaudhuri, S. R., Chavan, A. K., Chavez, F., Chem, G., Chen, X., Chen, M., Chen, J. -W., Chernomoretz, A., Chettouh, A., Cheung, D., Chicas, D., Chiu, S., Choudhry, H., Chrispin, C., Ciaramella, K., Cifuentes, E., Cohen, J., Coil, D. A., Collin, S., Conger, C., Conte, R., Corsi, F., Cossio, C. N., Costa, A. F., Cuebas, D., D'Alessandro, B., Dahlhausen, K. E., Darling, A. E., Das, P., Davenport, L. B., David, L., Davidson, N. R., Dayama, G., Delmas, S., Deng, C. K., Dequeker, C., Desert, A., Devi, M., Dezem, F. S., Dias, C. N., Donahoe, T. R., Dorado, S., Dorsey, L., Dotsenko, V., Du, S., Dutan, A., Eady, N., Eisen, J. A., Elaskandrany, M., Epping, L., Escalera-Antezana, J. P., Ettinger, C. L., Faiz, I., Fan, L., Farhat, N., Faure, E., Fauzi, F., Feigin, C., Felice, S., Ferreira, L. P., Figueroa, G., Fleiss, A., Flores, D., Velasco Flores, J. L., Fonseca, M. A. S., Foox, J., Forero, J. C., Francis, A., French, K., Fresia, P., Friedman, J., Fuentes, J. J., Galipon, J., Garcia, M., Garcia, L., Garcia, C., Geiger, A., Gerner, S. M., Ghose, S. L., Giang, D. P., Gimenez, M., Giovannelli, D., Githae, D., Gkotzis, S., Godoy, L., Goldman, S., Gonnet, G. H., Gonzalez, J., Gonzalez, A., Gonzalez-Poblete, C., Gray, A., Gregory, T., Greselle, C., Guasco, S., Guerra, J., Gurianova, N., Haehr, W., Halary, S., Hartkopf, F., Hawkins-Zafarnia, A., Hazrin-Chong, N. H., Helfrich, E., Hell, E., Henry, T., Hernandez, S., Hernandez, P. L., Hess-Homeier, D., Hittle, L. E., Hoan, N. X., Holik, A., Homma, C., Hoxie, I., Huber, M., Humphries, E., Hyland, S., Hassig, A., Hausler, R., Husser, N., Petit, R. A., Iderzorig, B., Igarashi, M., Iqbal, S. B., Ishikawa, S., Ishizuka, S., Islam, S., Islam, R., Ito, K., Ito, S., Ito, T., Ivankovic, T., Iwashiro, T., Jackson, S., Jacobs, J., James, M., Jaubert, M., Jerier, M. -L., Jiminez, E., Jinfessa, A., De Jong, Y., Joo, H. W., Jospin, G., Kajita, T., Ahmad Kassim, A. S., Kato, N., Kaur, A., Kaur, I., de Souza Gomes Kehdy, F., Khadka, V. S., Khan, S., Khavari, M., Ki, M., Kim, G., Kim, H. J., Kim, S., King, R. J., Kolomonaco, G., Koag, E., Kobko-Litskevitch, N., Korshevniuk, M., Kozhar, M., Krebs, J., Kubota, N., Kuklin, A., Kumar, S. S., Kwong, R., Kwong, L., Lafontaine, I., Lago, J., Lai, T. Y., Laine, E., Laiola, M., Lakhneko, O., Lamba, I., de Lamotte, G., Lannes, R., De Lazzari, E., Leahy, M., Lee, H., Lee, Y., Lee, L., Lemaire, V., Leong, E., Lewandowska, D., Li, C., Liang, W., Lin, M., Lisboa, P., Litskevitch, A., Liu, E. M., Liu, T., Livia, M. A., Lo, Y. H., Losim, S., Loubens, M., Lu, J., Lykhenko, O., Lysakova, S., Mahmoud, S., Majid, S. A., Makogon, N., Maldonado, D., Mallari, K., Malta, T. M., Mamun, M., Manoir, D., Marchandon, G., Marciniak, N., Marinovic, S., Marques, B., Mathews, N., Matsuzaki, Y., Matthys, V., May, M., Mccomb, E., Meagher, A., Melamed, A., Menary, W., Mendez, K. N., Mendez, A., Mendy, I. M., Meng, I., Menon, A., Menor, M., Meoded, R., Merino, N., Miah, K., Mignotte, M., Miketic, T., Miranda, W., Mitsios, A., Miura, R., Miyake, K., Moccia, M. D., Mohan, N., Mohsin, M., Moitra, K., Moldes, M., Molina, L., Molinet, J., Molomjamts, O. -E., Moniruzzaman, E., Moon, S., de Oliveira Moraes, I., Moreno, M., Mosella, M. S., Moser, J. W., Mozsary, C., Muehlbauer, A. L., Muner, O., Munia, M., Munim, N., Muscat, M., Mustac, T., Munoz, C., Nadalin, F., Naeem, A., Nagy-Szakal, D., Nakagawa, M., Narce, A., Nasu, M., Navarrete, I. G., Naveed, H., Nazario, B., Nedunuri, N. R., Neff, T., Nesimi, A., Ng, W. C., Ng, S., Nguyen, G., Ngwa, E., Nicolas, A., Nicolas, P., Nika, A., Noorzi, H., Nosrati, A., Nunes, D. N., O'Brien, K., O'Hara, N. B., Oken, G., Olawoyin, R. A., Oliete, J. Q., Olmeda, K., Oluwadare, T., Oluwadare, I. A., Ordioni, N., Orpilla, J., Orrego, J., Ortega, M., Osma, P., Osuolale, I. O., Osuolale, O. M., Ota, M., Oteri, F., Oto, Y., Ounit, R., Ouzounis, C. 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Subjects
Urban Population, Drug Resistance, Sequence assembly, Microbiologia, microbiome, global health, computer.software_genre, Medical and Health Sciences, shotgun sequencing, BGC, 0302 clinical medicine, Databases, Genetic, 11. Sustainability, Global health, AMR, 11 Medical and Health Sciences, ComputingMilieux_MISCELLANEOUS, 0303 health sciences, built environment, metagenome, antimicrobial resistance, NGS, de novo assembly, biology, Shotgun sequencing, Microbiota, built Environment, Bacterial, Biodiversity, Biological Sciences, 3. Good health, [SDV.MP]Life Sciences [q-bio]/Microbiology and Parasitology, Infection, Biotechnology, Geospatial analysis, [SDV.BID]Life Sciences [q-bio]/Biodiversity, Article, General Biochemistry, Genetics and Molecular Biology, Databases, 03 medical and health sciences, Antibiotic resistance, Genetic, Drug Resistance, Bacterial, International MetaSUB Consortium, Genetics, Humans, Microbiome, 030304 developmental biology, Human Genome, 06 Biological Sciences, 15. Life on land, biology.organism_classification, Resistènica als medicaments antiinfecciosos, SAÚDE PÚBLICA, Genòmica, 13. Climate action, Evolutionary biology, Metagenomics, Antimicrobial Resistance, [SDE.BE]Environmental Sciences/Biodiversity and Ecology, computer, 030217 neurology & neurosurgery, Archaea, Developmental Biology
Abstract

Summary We present a global atlas of 4,728 metagenomic samples from mass-transit systems in 60 cities over 3 years, representing the first systematic, worldwide catalog of the urban microbial ecosystem. This atlas provides an annotated, geospatial profile of microbial strains, functional characteristics, antimicrobial resistance (AMR) markers, and genetic elements, including 10,928 viruses, 1,302 bacteria, 2 archaea, and 838,532 CRISPR arrays not found in reference databases. We identified 4,246 known species of urban microorganisms and a consistent set of 31 species found in 97% of samples that were distinct from human commensal organisms. Profiles of AMR genes varied widely in type and density across cities. Cities showed distinct microbial taxonomic signatures that were driven by climate and geographic differences. These results constitute a high-resolution global metagenomic atlas that enables discovery of organisms and genes, highlights potential public health and forensic applications, and provides a culture-independent view of AMR burden in cities., Graphical abstract, Highlights • Cities possess a consistent “core” set of non-human microbes • Urban microbiomes echo important features of cities and city-life • Antimicrobial resistance genes are widespread in cities • Cities contain many novel bacterial and viral species, This systematic, worldwide catalog of urban microbiomes represents a metagenomic atlas important for understanding the ecology, virulence, and antibiotic resistance of city-specific microbial communities.

Published
2021
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13. Frequency, Local Dynamics, and Genomic Characteristics of ESBL-Producing Escherichia coli Isolated From Specimens of Hospitalized Horses

Author

Antina Lübke-Becker, Fereshteh Ghazisaeedi, Sebastian Günther, Heidrun Gehlen, Birgit Walther, Anne Kauter, Torsten Semmler, Lennard Epping, Sabita D. Stoeckle, Dania Kannapin, and Silver A. Wolf

Subjects
Microbiology (medical), medicine.medical_specialty, antibiotic resistance, medicine.drug_class, Antibiotics, spread, Microbiology, 03 medical and health sciences, Antibiotic resistance, Internal medicine, medicine, Escherichia coli, ddc:610, Feces, Original Research, 030304 developmental biology, 0303 health sciences, 030306 microbiology, business.industry, multidrug resistant, Horse, 500 Naturwissenschaften und Mathematik::570 Biowissenschaften, Biologie::570 Biowissenschaften, Biologie, QR1-502, horse, Penicillin, Regimen, Carriage, ESBL, Gentamicin, 610 Medizin und Gesundheit, business, medicine.drug
Abstract

Previous research identified veterinary clinics as hotspots with respect to accumulation and spread of multidrug resistant extended-spectrum β-lactamase (ESBL)-producing Escherichia coli (EC). Therefore, promoting the prudent use of antibiotics to decrease selective pressure in that particular clinical environment is preferable to enhance biosecurity for animal patients and hospital staff. Accordingly, this study comparatively investigated the impact of two distinct perioperative antibiotic prophylaxis (PAP) regimens (short-term versus prolonged) on ESBL-EC carriage of horses subjected to colic surgery. While all horses received a combination of penicillin/gentamicin (P/G) as PAP, they were assigned to either the “single-shot group” (SSG) or the conventional “5-day group” (5DG). Fecal samples collected on arrival (t0), on the 3rd (t1) and on the 10th day after surgery (t2) were screened for ESBL-EC. All isolates were further investigated using whole genome sequences. In total, 81 of 98 horses met the inclusion criteria for this study. ESBL-EC identified in samples available at t0, t1 and t2 were 4.8% (SSG) and 9.7% (5DG), 37% (SSG) and 47.2% (5DG) as well as 55.6% (SSG) and 56.8% (5DG), respectively. Regardless of the P/G PAP regimen, horses were 9.12 times (95% CI 2.79–29.7) more likely to carry ESBL-EC at t1 compared to t0 (p < 0.001) and 15.64 times (95% CI 4.57–53.55) more likely to carry ESBL-EC at t2 compared to t0 (p < 0.001). ESBL-EC belonging to sequence type (ST) 10, ST86, ST641, and ST410 were the most prevalent lineages, with blaCTX–M–1 (60%) being the dominant ESBL gene. A close spatio-temporal relationship between isolates sharing a particular ST was revealed by genome analysis, strongly indicating local spread. Consequently, hospitalization itself has a strong impact on ESBL-EC isolation rates in horses, possibly masking differences between distinct PAP regimens. The results of this study reveal accumulation and spread of multi-drug resistant ESBL-EC among horses subjected to colic surgery with different P/G PAP regimens, challenging the local hygiene management system and work-place safety of veterinary staff. Moreover, the predominance of particular ESBL-EC lineages in clinics providing health care for horses needs further investigation.

Published
2021

14. Bringing together what belongs together: Optimizing murine infection models by using mouse-adapted Staphylococcus aureus strains

Author

Barbara M. Bröker, Knut Ohlsen, Tobias Hertlein, Bettina Krause, Daniel M. Mrochen, Ilka Jorde, Julia Zeun, Rainer G. Ulrich, Daniel Schulz, Patricia Trübe, Birgit Walther, Silver A. Wolf, Stefan Fischer, Torsten Semmler, and Silva Holtfreter

Subjects
Microbiology (medical), Staphylococcus aureus, Chemokine, Mouse, Virulence, Bacteremia, medicine.disease_cause, Microbiology, Mice, 03 medical and health sciences, Infection model, Bacterial Proteins, Leukocidins, Genotype, medicine, Animals, Humans, ddc:610, CC49, 030304 developmental biology, Mice, Inbred BALB C, Vole, 0303 health sciences, Whole Genome Sequencing, biology, Arvicolinae, 030306 microbiology, Toxin, Pneumonia, General Medicine, Staphylococcal Infections, medicine.disease, Disease Models, Animal, Host-adapted, Infectious Diseases, biology.protein, Cytokines, Female, Host adaptation, 610 Medizin und Gesundheit, Staphylococcus, Pneumonia (non-human)
Abstract

Staphylococcus (S.) aureus is a leading cause of bacterial infection world-wide, and currently no vaccine is available for humans. Vaccine development relies heavily on clinically relevant infection models. However, the suitability of mice for S. aureus infection models has often been questioned, because experimental infection of mice with human-adapted S. aureus requires very high infection doses. Moreover, mice were not considered to be natural hosts of S. aureus. The latter has been disproven by our recent findings, showing that both laboratory mice, as well as wild small mammals including mice, voles, and shrews, are naturally colonized with S. aureus. Here, we investigated whether mouse-and vole-derived S. aureus strains show an enhanced virulence in mice as compared to the human-adapted strain Newman. Using a step-wise approach based on the bacterial genotype and in vitro assays for host adaptation, we selected the most promising candidates for murine infection models out of a total of 254 S. aureus isolates from laboratory mice as well as wild rodents and shrews. Four strains representing the clonal complexes (CC) 8, 49, and 88 (n = 2) were selected and compared to the human-adapted S. aureus strain Newman (CC8) in murine pneumonia and bacteremia models. Notably, a bank vole-derived CC49 strain, named DIP, was highly virulent in BALB/c mice in pneumonia and bacteremia models, whereas the other murine and vole strains showed virulence similar to or lower than that of Newman. At one tenth of the standard infection dose DIP induced disease severity, bacterial load and host cytokine and chemokine responses in the murine bacteremia model similar to that of Newman. In the pneumonia model, DIP was also more virulent than Newman but the effect was less pronounced. Whole genome sequencing data analysis identified a pore-forming toxin gene, lukF-PV(P83)/lukM, in DIP but not in the other tested S. aureus isolates. To conclude, the mouse-adapted S. aureus strain DIP allows a significant reduction of the inoculation dose in mice and is hence a promising tool to develop clinically more relevant infection models.

Published
2019
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15. SCORE: Smart Consensus Of RNA Expression-a consensus tool for detecting differentially expressed genes in bacteria

Author

Silver A. Wolf, Torsten Semmler, Knut Reinert, Sandro Andreotti, and Lennard Epping

Subjects
Statistics and Probability, Consensus, Computer science, Computational biology, Biochemistry, Transcriptome, 03 medical and health sciences, 0302 clinical medicine, Gene expression, Molecular Biology, 030304 developmental biology, 0303 health sciences, biology, Bacteria, Sequence Analysis, RNA, Gene Expression Regulation, Bacterial, biology.organism_classification, Computer Science Applications, Computational Mathematics, Differentially expressed genes, Rna expression, Computational Theory and Mathematics, 030217 neurology & neurosurgery, Software
Abstract

Summary RNA-sequencing (RNA-Seq) is the current method of choice for studying bacterial transcriptomes. To date, many computational pipelines have been developed to predict differentially expressed genes from RNA-Seq data, but no gold-standard has been widely accepted. We present the Snakemake-based tool Smart Consensus Of RNA Expression (SCORE) which uses a consensus approach founded on a selection of well-established tools for differential gene expression analysis. This allows SCORE to increase the overall prediction accuracy and to merge varying results into a single, human-readable output. SCORE performs all steps for the analysis of bacterial RNA-Seq data, from read preprocessing to the overrepresentation analysis of significantly associated ontologies. Development of consensus approaches like SCORE will help to streamline future RNA-Seq workflows and will fundamentally contribute to the creation of new gold-standards for the analysis of these types of data. Availability and implementation https://github.com/SiWolf/SCORE. Supplementary information Supplementary data are available at Bioinformatics online.

Published
2020

16. Extended-spectrum beta-lactamase (ESBL)-producing Escherichia coli and Acinetobacter baumannii among horses entering a veterinary teaching hospital: The contemporary 'Trojan Horse'

Author

Sebastian Guenther, Heidrun Gehlen, Franziska Mitrach, Silver A. Wolf, Karsten Tedin, Torsten Semmler, Roswitha Merle, Charlotte Huber, Antina Lübke-Becker, Ann-Kristin Barton, Katja-Sophia Klein, and Birgit Walther

Subjects
Acinetobacter baumannii, Bacterial Diseases, 0301 basic medicine, Salmonella, medicine.medical_treatment, lcsh:Medicine, Pathology and Laboratory Medicine, medicine.disease_cause, Medicine and Health Sciences, lcsh:Science, Mammals, Multidisciplinary, Acinetobacter, biology, Eukaryota, Genomics, Enterobacteriaceae, Hospitals, Electrophoresis, Gel, Pulsed-Field, Bacterial Pathogens, Infectious Diseases, Medical Microbiology, Vertebrates, Veterinary Hospitals, Pathogens, Research Article, Veterinary Medicine, Equines, 030106 microbiology, Microbiology, beta-Lactamases, Hospitals, Animal, 03 medical and health sciences, Escherichia coli, Genetics, medicine, Pulsed-field gel electrophoresis, Animals, Horses, Hospitals, Teaching, Microbial Pathogens, Bacteria, business.industry, lcsh:R, Organisms, Biology and Life Sciences, Computational Biology, Horse, Genome Analysis, biology.organism_classification, Health Care, Carriage, Genes, Bacterial, Health Care Facilities, Amniotes, Beta-lactamase, Veterinary Science, lcsh:Q, business
Abstract

Pathogens frequently associated with multi-drug resistant (MDR) phenotypes, including extended-spectrum beta-lactamase (ESBL)-producing Enterobacteriaceae (ESBL-E) and Acinetobacter baumannii isolated from horses admitted to horse clinics, pose a risk for animal patients and personnel in horse clinics. To estimate current rates of colonization, a total of 341 equine patients were screened for carriage of zoonotic indicator pathogens at hospital admission. Horses showing clinical signs associated with colic (n = 233) or open wounds (n = 108) were selected for microbiological examination of nostril swabs, faecal samples and wound swabs taken from the open wound group. The results showed alarming carriage rates of Gram-negative MDR pathogens in equine patients: 10.7% (34 of 318) of validated faecal specimens were positive for ESBL-E (94%: ESBL-producing Escherichia coli), with recorded rates of 10.5% for the colic and 11% for the open wound group. 92.7% of the ESBL-producing E. coli were phenotypically resistant to three or more classes of antimicrobials. A. baumannii was rarely detected (0.9%), and all faecal samples investigated were negative for Salmonella, both directly and after two enrichment steps. Screening results for the equine nostril swabs showed detection rates for ESBL-E of 3.4% among colic patients and 0.9% in the open wound group, with an average rate of 2.6% (9/340) for both indications. For all 41 ESBL-producing E. coli isolated, a broad heterogeneity was revealed using pulsed-field gel electrophoresis (PFGE) patterns and whole genome sequencing (WGS) -analysis. However, a predominance of sequence type complex (STC)10 and STC1250 was observed, including several novel STs. The most common genes associated with ESBL-production were identified as blaCTX-M-1 (31/41; 75.6%) and blaSHV-12 (24.4%). The results of this study reveal a disturbingly large fraction of multi-drug resistant and ESBL-producing E. coli among equine patients, posing a clear threat to established hygiene management systems and work-place safety of veterinary staff in horse clinics.

Published
2018
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18. Rat cytomegalovirus efficiently replicates in dendritic cells and induces changes in their transcriptional profile

Author

Julia Cecilia Madela-Mönchinger, Silver Anthony Wolf, Emanuel Wyler, Agnieszka Bauer, Marius Mischke, Lars Möller, Vanda Juranić Lisnić, Markus Landthaler, Anna Malyshkina, and Sebastian Voigt

Subjects
cytomegalovirus, dendritic cells, transcriptome, chemokines, XCL1, XCR1, Immunologic diseases. Allergy, RC581-607
Abstract

Dendritic cells (DC) play a crucial role in generating and maintaining antiviral immunity. While DC are implicated in the antiviral defense by inducing T cell responses, they can also become infected by Cytomegalovirus (CMV). CMV is not only highly species-specific but also specialized in evading immune protection, and this specialization is in part due to characteristic genes encoded by a given virus. Here, we investigated whether rat CMV can infect XCR1+ DC and if infection of DC alters expression of cell surface markers and migration behavior. We demonstrate that wild-type RCMV and a mutant virus lacking the γ-chemokine ligand xcl1 (Δvxcl1 RCMV) infect splenic rat DC ex vivo and identify viral assembly compartments. Replication-competent RCMV reduced XCR1 and MHCII surface expression. Further, gene expression of infected DC was analyzed by bulk RNA-sequencing (RNA-Seq). RCMV infection reverted a state of DC activation that was induced by DC cultivation. On the functional level, we observed impaired chemotactic activity of infected XCR1+ DC compared to mock-treated cells. We therefore speculate that as a result of RCMV infection, DC exhibit diminished XCR1 expression and are thereby blocked from the lymphocyte crosstalk.

Published
2023
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19. Genotypic Characterization of Uropathogenic Escherichia coli from Companion Animals: Predominance of ST372 in Dogs and Human-Related ST73 in Cats

Author

Sophie Aurich, Silver Anthony Wolf, Ellen Prenger-Berninghoff, Lakshmipriya Thrukonda, Torsten Semmler, and Christa Ewers

Subjects
ExPEC, UPEC, dog, cat, antimicrobial resistance genes, phylogroup B2, Therapeutics. Pharmacology, RM1-950
Abstract

Extraintestinal pathogenic Escherichia coli (ExPEC) account for over 80% and 60% of bacterial urinary tract infections (UTIs) in humans and animals, respectively. As shared uropathogenic E. coli (UPEC) strains have been previously reported among humans and pets, our study aimed to characterize E. coli lineages among UTI isolates from dogs and cats and to assess their overlaps with human UPEC lineages. We analysed 315 non-duplicate E. coli isolates from the UT of dogs (198) and cats (117) collected in central Germany in 2019 and 2020 utilizing whole genome sequencing and in silico methods. Phylogroup B2 (77.8%), dog-associated sequence type (ST) 372 (18.1%), and human-associated ST73 (16.6%), were predominant. Other STs included ST12 (8.6%), ST141 (5.1%), ST127 (4.8%), and ST131 (3.5%). Among these, 58.4% were assigned to the ExPEC group and 51.1% to the UPEC group based on their virulence associated gene (VAG) profile (ExPEC, presence of ≥VAGs: papAH and/or papC, sfa/focG, afaD/draBC, kpsMTII, and iutA; UPEC, additionally cnf1 or hlyD). Extended-spectrum cephalosporin (ESC) resistance mediated by extended-spectrum β-lactamases (ESBL) and AmpC-β-lactamase was identified in 1.9% of the isolates, along with one carbapenemase-producing isolate and one isolate carrying a mcr gene. Low occurrence of ESC-resistant or multidrug-resistant (MDR) isolates (2.9%) in the two most frequently detected STs implies that E. coli isolated from UTIs of companion animals are to a lesser extent associated with resistance, but possess virulence-associated genes enabling efficient UT colonization and carriage. Detection of human-related pandemic lineages suggests interspecies transmission and underscores the importance of monitoring companion animals.

Published
2023
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