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Miguel A. Terrazos
Institute for Infectious Diseases, University of Bern, Bern, Switzerland

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Author correction
Published: 29 January 2021 in Nature Communications
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A Correction to this paper has been published: https://doi.org/10.1038/s41467-021-21096-5.

ACS Style

Simona P. Pfister; Olivier P. Schären; Luca Beldi; Andrea Printz; Matheus D. Notter; Mohana Mukherjee; Hai Li; Julien P. Limenitakis; Joel P. Werren; Disha Tandon; Miguelangel Cuenca; Stefanie Hagemann; Stephanie S. Uster; Miguel A. Terrazos; Mercedes Gomez de Agüero; Christian M. Schürch; Fernanda M. Coelho; Roy Curtiss; Emma Slack; Maria L. Balmer; Siegfried Hapfelmeier. Author Correction: Uncoupling of invasive bacterial mucosal immunogenicity from pathogenicity. Nature Communications 2021, 12, 1 -1.

AMA Style

Simona P. Pfister, Olivier P. Schären, Luca Beldi, Andrea Printz, Matheus D. Notter, Mohana Mukherjee, Hai Li, Julien P. Limenitakis, Joel P. Werren, Disha Tandon, Miguelangel Cuenca, Stefanie Hagemann, Stephanie S. Uster, Miguel A. Terrazos, Mercedes Gomez de Agüero, Christian M. Schürch, Fernanda M. Coelho, Roy Curtiss, Emma Slack, Maria L. Balmer, Siegfried Hapfelmeier. Author Correction: Uncoupling of invasive bacterial mucosal immunogenicity from pathogenicity. Nature Communications. 2021; 12 (1):1-1.

Chicago/Turabian Style

Simona P. Pfister; Olivier P. Schären; Luca Beldi; Andrea Printz; Matheus D. Notter; Mohana Mukherjee; Hai Li; Julien P. Limenitakis; Joel P. Werren; Disha Tandon; Miguelangel Cuenca; Stefanie Hagemann; Stephanie S. Uster; Miguel A. Terrazos; Mercedes Gomez de Agüero; Christian M. Schürch; Fernanda M. Coelho; Roy Curtiss; Emma Slack; Maria L. Balmer; Siegfried Hapfelmeier. 2021. "Author Correction: Uncoupling of invasive bacterial mucosal immunogenicity from pathogenicity." Nature Communications 12, no. 1: 1-1.

Journal article
Published: 31 July 2020 in Viruses
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Enteroviruses are small RNA viruses that affect millions of people each year by causing an important burden of disease with a broad spectrum of symptoms. In routine diagnostic laboratories, enteroviruses are identified by PCR-based methods, often combined with partial sequencing for genotyping. In this proof-of-principle study, we assessed direct RNA sequencing (DRS) using nanopore sequencing technology for fast whole-genome sequencing of viruses directly from clinical samples. The approach was complemented by sequencing the corresponding viral cDNA via Illumina MiSeq sequencing. DRS of total RNA extracted from three different enterovirus-positive stool samples produced long RNA fragments, covering between 59% and 99.6% of the most similar reference genome sequences. The identification of the enterovirus sequences in the samples was confirmed by short-read cDNA sequencing. Sequence identity between DRS and Illumina MiSeq enterovirus consensus sequences ranged between 94% and 97%. Here, we show that nanopore DRS can be used to correctly identify enterovirus genotypes from patient stool samples with high viral load and that the approach also provides rich metatranscriptomic information on sample composition for all life domains.

ACS Style

Carole Grädel; Miguel A. Terrazos Miani; Christian Baumann; Maria Teresa Barbani; Stefan Neuenschwander; Stephen L. Leib; Franziska Suter-Riniker; Alban Ramette. Whole-Genome Sequencing of Human Enteroviruses from Clinical Samples by Nanopore Direct RNA Sequencing. Viruses 2020, 12, 841 .

AMA Style

Carole Grädel, Miguel A. Terrazos Miani, Christian Baumann, Maria Teresa Barbani, Stefan Neuenschwander, Stephen L. Leib, Franziska Suter-Riniker, Alban Ramette. Whole-Genome Sequencing of Human Enteroviruses from Clinical Samples by Nanopore Direct RNA Sequencing. Viruses. 2020; 12 (8):841.

Chicago/Turabian Style

Carole Grädel; Miguel A. Terrazos Miani; Christian Baumann; Maria Teresa Barbani; Stefan Neuenschwander; Stephen L. Leib; Franziska Suter-Riniker; Alban Ramette. 2020. "Whole-Genome Sequencing of Human Enteroviruses from Clinical Samples by Nanopore Direct RNA Sequencing." Viruses 12, no. 8: 841.

Other
Published: 09 June 2020
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Enteroviruses are small RNA viruses that affect millions of people each year by causing an important burden of disease with a broad spectrum of symptoms. In routine diagnostic laboratories, those viruses are identified by PCR based methods, often combined with partial sequencing for genotyping. In this proof-of-principle study, we assessed direct RNA sequencing (DRS) using nanopore sequencing technology for fast whole-genome sequencing of viruses directly from clinical samples. Results of the approach were complemented with those obtained by sequencing the corresponding viral cDNA via Illumina MiSeq sequencing. DRS of total RNA extracted from three different enterovirus-positive stool samples produced long RNA fragments, covering between 59% to 99.6 % of the best reference genomes. The identification of the enterovirus sequences in the sample was confirmed by the short-read cDNA sequencing. Sequence identity between DRS and Illumina MiSeq enterovirus consensus sequences ranged between 94-97%. Here we show that nanopore DRS can be used to correctly identify the genotypes of enteroviruses from patient stool samples with high viral load.

ACS Style

Carole Grädel; Miguel A Terrazos Miani; Christian Baumann; Maria Teresa Barbani; Stefan Neuenschwander; Stephen L Leib; Franziska Suter-Riniker; Alban Ramette. Whole genome sequencing of human enteroviruses from clinical samples by nanopore direct RNA sequencing. 2020, 1 .

AMA Style

Carole Grädel, Miguel A Terrazos Miani, Christian Baumann, Maria Teresa Barbani, Stefan Neuenschwander, Stephen L Leib, Franziska Suter-Riniker, Alban Ramette. Whole genome sequencing of human enteroviruses from clinical samples by nanopore direct RNA sequencing. . 2020; ():1.

Chicago/Turabian Style

Carole Grädel; Miguel A Terrazos Miani; Christian Baumann; Maria Teresa Barbani; Stefan Neuenschwander; Stephen L Leib; Franziska Suter-Riniker; Alban Ramette. 2020. "Whole genome sequencing of human enteroviruses from clinical samples by nanopore direct RNA sequencing." , no. : 1.

Journal article
Published: 24 April 2020 in Nature Communications
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There is the notion that infection with a virulent intestinal pathogen induces generally stronger mucosal adaptive immunity than the exposure to an avirulent strain. Whether the associated mucosal inflammation is important or redundant for effective induction of immunity is, however, still unclear. Here we use a model of auxotrophic Salmonella infection in germ-free mice to show that live bacterial virulence factor-driven immunogenicity can be uncoupled from inflammatory pathogenicity. Although live auxotrophic Salmonella no longer causes inflammation, its mucosal virulence factors remain the main drivers of protective mucosal immunity; virulence factor-deficient, like killed, bacteria show reduced efficacy. Assessing the involvement of innate pathogen sensing mechanisms, we show MYD88/TRIF, Caspase-1/Caspase-11 inflammasome, and NOD1/NOD2 nodosome signaling to be individually redundant. In colonized animals we show that microbiota metabolite cross-feeding may recover intestinal luminal colonization but not pathogenicity. Consequent immunoglobulin A immunity and microbial niche competition synergistically protect against Salmonella wild-type infection.

ACS Style

Simona P. Pfister; Olivier P. Schären; Luca Beldi; Andrea Printz; Matheus D. Notter; Mohana Mukherjee; Hai Li; Julien P. Limenitakis; Joel P. Werren; Disha Tandon; Miguelangel Cuenca; Stefanie Hagemann; Stephanie S. Uster; Miguel A. Terrazos; Mercedes Gomez De Agüero; Christian M. Schürch; Fernanda M. Coelho; Roy Curtiss; Emma Slack; Maria L. Balmer; Siegfried Hapfelmeier. Uncoupling of invasive bacterial mucosal immunogenicity from pathogenicity. Nature Communications 2020, 11, 1 -18.

AMA Style

Simona P. Pfister, Olivier P. Schären, Luca Beldi, Andrea Printz, Matheus D. Notter, Mohana Mukherjee, Hai Li, Julien P. Limenitakis, Joel P. Werren, Disha Tandon, Miguelangel Cuenca, Stefanie Hagemann, Stephanie S. Uster, Miguel A. Terrazos, Mercedes Gomez De Agüero, Christian M. Schürch, Fernanda M. Coelho, Roy Curtiss, Emma Slack, Maria L. Balmer, Siegfried Hapfelmeier. Uncoupling of invasive bacterial mucosal immunogenicity from pathogenicity. Nature Communications. 2020; 11 (1):1-18.

Chicago/Turabian Style

Simona P. Pfister; Olivier P. Schären; Luca Beldi; Andrea Printz; Matheus D. Notter; Mohana Mukherjee; Hai Li; Julien P. Limenitakis; Joel P. Werren; Disha Tandon; Miguelangel Cuenca; Stefanie Hagemann; Stephanie S. Uster; Miguel A. Terrazos; Mercedes Gomez De Agüero; Christian M. Schürch; Fernanda M. Coelho; Roy Curtiss; Emma Slack; Maria L. Balmer; Siegfried Hapfelmeier. 2020. "Uncoupling of invasive bacterial mucosal immunogenicity from pathogenicity." Nature Communications 11, no. 1: 1-18.

Preprint content
Published: 31 August 2019
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Amplicon sequencing of 16S rRNA gene is commonly used for the identification of bacterial isolates in diagnostic laboratories, and mostly relies on the Sanger sequencing method. The latter, however, suffers from a number of limitations with the most significant being the inability to resolve mixed amplicons when closely related species are co-amplified from a mixed culture. This often leads to either increased turnover time or absence of usable sequence data. Short-read NGS technologies could address the mixed amplicon issue, but would lack both cost efficiency at low throughput and fast turnaround times. Nanopore sequencing developed by Oxford Nanopore Technologies (ONT) could solve those issues by enabling flexible number of samples per run and adjustable sequencing time. Here we report on the development of a standardized laboratory workflow combined with a fully automated analysis pipelineLORCAN(Long Read Consensus ANalysis), which together provide a sample-to-report solution for amplicon sequencing and taxonomic identification of the resulting consensus sequences. Validation of the approach was conducted on a panel of reference strains and on clinical samples consisting of single or mixed rRNA amplicons associated with various bacterial genera by direct comparison to the corresponding Sanger sequences. Additionally, artificial read mixtures of closely related species were used to assessLORCAN’s behaviour when dealing with samples with known cross-contamination level. We demonstrate that by combining ONT amplicon sequencing results withLORCAN, the accuracy of Sanger sequencing can be closely matched (>99.6% sequence identity) and that mixed samples can be resolved at the single base resolution level. The presented approach has the potential to significantly improve the flexibility, reliability and availability of amplicon sequencing in diagnostic settings.

ACS Style

Stefan Moritz Neuenschwander; Miguel Angel Terrazos Miani; Heiko Amlang; Carmen Perroulaz; Pascal Bittel; Carlo Casanova; Sara Droz; Jean-Pierre Flandrois; Stephen L. Leib; Franziska Suter-Riniker; Alban Ramette. A sample-to-report solution for taxonomic identification of cultured bacteria in the clinical setting based on nanopore sequencing. 2019, 752774 .

AMA Style

Stefan Moritz Neuenschwander, Miguel Angel Terrazos Miani, Heiko Amlang, Carmen Perroulaz, Pascal Bittel, Carlo Casanova, Sara Droz, Jean-Pierre Flandrois, Stephen L. Leib, Franziska Suter-Riniker, Alban Ramette. A sample-to-report solution for taxonomic identification of cultured bacteria in the clinical setting based on nanopore sequencing. . 2019; ():752774.

Chicago/Turabian Style

Stefan Moritz Neuenschwander; Miguel Angel Terrazos Miani; Heiko Amlang; Carmen Perroulaz; Pascal Bittel; Carlo Casanova; Sara Droz; Jean-Pierre Flandrois; Stephen L. Leib; Franziska Suter-Riniker; Alban Ramette. 2019. "A sample-to-report solution for taxonomic identification of cultured bacteria in the clinical setting based on nanopore sequencing." , no. : 752774.

Journal article
Published: 29 August 2019 in Genes
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Enteroviruses affect millions of people worldwide and are of significant clinical importance. The standard method for enterovirus identification and genotyping still relies on Sanger sequencing of short diagnostic amplicons. In this study, we assessed the feasibility of nanopore sequencing using the new flow cell “Flongle” for fast, cost-effective, and accurate genotyping of human enteroviruses from clinical samples. PCR amplification of partial VP1 gene was performed from multiple patient samples, which were multiplexed together after barcoding PCR and sequenced multiple times on Flongle flow cells. The nanopore consensus sequences obtained from mapping reads to a reference database were compared to their Sanger sequence counterparts. Using clinical specimens sampled over different years, we were able to correctly identify enterovirus species and genotypes for all tested samples, even when doubling the number of barcoded samples on one flow cell. Average sequence identity across sequencing runs was >99.7%. Phylogenetic analysis showed that the consensus sequences achieved with Flongle delivered accurate genotyping. We conclude that the new Flongle-based assay with its fast turnover time, low cost investment, and low cost per sample represents an accurate, reproducible, and cost-effective platform for enterovirus identification and genotyping.

ACS Style

Carole Grädel; Miguel Angel Terrazos Miani; Maria Teresa Barbani; Stephen L Leib; Franziska Suter-Riniker; Alban Ramette. Rapid and Cost-Efficient Enterovirus Genotyping from Clinical Samples Using Flongle Flow Cells. Genes 2019, 10, 659 .

AMA Style

Carole Grädel, Miguel Angel Terrazos Miani, Maria Teresa Barbani, Stephen L Leib, Franziska Suter-Riniker, Alban Ramette. Rapid and Cost-Efficient Enterovirus Genotyping from Clinical Samples Using Flongle Flow Cells. Genes. 2019; 10 (9):659.

Chicago/Turabian Style

Carole Grädel; Miguel Angel Terrazos Miani; Maria Teresa Barbani; Stephen L Leib; Franziska Suter-Riniker; Alban Ramette. 2019. "Rapid and Cost-Efficient Enterovirus Genotyping from Clinical Samples Using Flongle Flow Cells." Genes 10, no. 9: 659.

Research article
Published: 29 June 2017 in PLOS Pathogens
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Citrobacter rodentium infection is a mouse model for the important human diarrheal infection caused by enteropathogenic E. coli (EPEC). The pathogenesis of both species is very similar and depends on their unique ability to form intimately epithelium-adherent microcolonies, also known as “attachment/effacement” (A/E) lesions. These microcolonies must be dynamic and able to self-renew by continuous re-infection of the rapidly regenerating epithelium. It is unknown whether sustained epithelial A/E lesion pathogenesis is achieved through re-infection by planktonic bacteria from the luminal compartment or local spread of sessile bacteria without a planktonic phase. Focusing on the earliest events as C. rodentium becomes established, we show here that all colonic epithelial A/E microcolonies are clonal bacterial populations, and thus depend on local clonal growth to persist. In wild-type mice, microcolonies are established exclusively within the first 18 hours of infection. These early events shape the ongoing intestinal geography and severity of infection despite the continuous presence of phenotypically virulent luminal bacteria. Mechanistically, induced resistance to A/E lesion de-novo formation is mediated by TLR-MyD88/Trif-dependent signaling and is induced specifically by virulent C. rodentium in a virulence gene-dependent manner. Our data demonstrate that the establishment phase of C. rodentium pathogenesis in vivo is restricted to a very short window of opportunity that determines both disease geography and severity. The so-called “attaching and effacing” (A/E) pathogens enteropathogenic E. coli (EPEC) and enterohemorrhagic E. coli (EHEC) cause serious human diarrheal infections by adhering to and damaging the intestinal epithelium. Previous work on the mouse A/E pathogen Citrobacter rodentium has established that host adaptive immune response and intestinal microbiota cooperate to control the epithelial infection and colonization with this pathogen. We found that this is complemented by a rapid pathogen-induced mucosal innate immune response that is essential to prevent excessive pathogenesis before adaptive immunity takes effect. Its effectiveness is demonstrated by the fact that it normally limits the duration during which the bacteria can induce epithelial lesions to the first 18 hours of infection. Later, luminal virulent bacteria can no longer induce new A/E lesions, but those induced already in the first 18 hours of infection persist through localized epithelial re-infection. Severity of the disease at the peak of infection is consequently shaped by the early events of the first 18 hours. This information may be important for the development of effective therapies and vaccines.

ACS Style

Stefanie Buschor; Miguelangel Cuenca; Stephanie S. Uster; Olivier P. Schären; Maria Luisa Balmer; Miguel A. Terrazos; Christian M. Schürch; Siegfried Hapfelmeier. Innate immunity restricts Citrobacter rodentium A/E pathogenesis initiation to an early window of opportunity. PLOS Pathogens 2017, 13, e1006476 -e1006476.

AMA Style

Stefanie Buschor, Miguelangel Cuenca, Stephanie S. Uster, Olivier P. Schären, Maria Luisa Balmer, Miguel A. Terrazos, Christian M. Schürch, Siegfried Hapfelmeier. Innate immunity restricts Citrobacter rodentium A/E pathogenesis initiation to an early window of opportunity. PLOS Pathogens. 2017; 13 (6):e1006476-e1006476.

Chicago/Turabian Style

Stefanie Buschor; Miguelangel Cuenca; Stephanie S. Uster; Olivier P. Schären; Maria Luisa Balmer; Miguel A. Terrazos; Christian M. Schürch; Siegfried Hapfelmeier. 2017. "Innate immunity restricts Citrobacter rodentium A/E pathogenesis initiation to an early window of opportunity." PLOS Pathogens 13, no. 6: e1006476-e1006476.