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1. High throughput sequencing provides exact genomic locations of inducible prophages and accurate phage-to-host ratios in gut microbial strains

Author

Mirjam Zünd, Hans-Joachim Ruscheweyh, Christopher M. Field, Natalie Meyer, Miguelangel Cuenca, Daniel Hoces, Wolf-Dietrich Hardt, and Shinichi Sunagawa

Subjects
Prophage localisation, Prophage induction, Phage activity, Phage replication, High-throughput sequencing, Phage-to-host ratio, Microbial ecology, QR100-130
Abstract

Abstract Background Temperate phages influence the density, diversity and function of bacterial populations. Historically, they have been described as carriers of toxins. More recently, they have also been recognised as direct modulators of the gut microbiome, and indirectly of host health and disease. Despite recent advances in studying prophages using non-targeted sequencing approaches, methodological challenges in identifying inducible prophages in bacterial genomes and quantifying their activity have limited our understanding of prophage-host interactions. Results We present methods for using high-throughput sequencing data to locate inducible prophages, including those previously undiscovered, to quantify prophage activity and to investigate their replication. We first used the well-established Salmonella enterica serovar Typhimurium/p22 system to validate our methods for (i) quantifying phage-to-host ratios and (ii) accurately locating inducible prophages in the reference genome based on phage-to-host ratio differences and read alignment alterations between induced and non-induced prophages. Investigating prophages in bacterial strains from a murine gut model microbiota known as Oligo-MM12 or sDMDMm2, we located five novel inducible prophages in three strains, quantified their activity and showed signatures of lateral transduction potential for two of them. Furthermore, we show that the methods were also applicable to metagenomes of induced faecal samples from Oligo-MM12 mice, including for strains with a relative abundance below 1%, illustrating its potential for the discovery of inducible prophages also in more complex metagenomes. Finally, we show that predictions of prophage locations in reference genomes of the strains we studied were variable and inconsistent for four bioinformatic tools we tested, which highlights the importance of their experimental validation. Conclusions This study demonstrates that the integration of experimental induction and bioinformatic analysis presented here is a powerful approach to accurately locate inducible prophages using high-throughput sequencing data and to quantify their activity. The ability to generate such quantitative information will be critical in helping us to gain better insights into the factors that determine phage activity and how prophage-bacteria interactions influence our microbiome and impact human health. Video abstract.

Published
2021
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2. Uncoupling of invasive bacterial mucosal immunogenicity from pathogenicity

Author

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, and Siegfried Hapfelmeier

Subjects
Science
Abstract

Virulent pathogens generally induce a stronger mucosal immunity than avirulent strains, but whether the associated inflammation is necessary for this is unclear. Here, using auxotrophic Salmonella enterica, the authors show that virulence factor function determines induction of protective IgA.

Published
2020
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3. Microbial abundance, activity and population genomic profiling with mOTUs2

Author

Alessio Milanese, Daniel R Mende, Lucas Paoli, Guillem Salazar, Hans-Joachim Ruscheweyh, Miguelangel Cuenca, Pascal Hingamp, Renato Alves, Paul I Costea, Luis Pedro Coelho, Thomas S. B. Schmidt, Alexandre Almeida, Alex L Mitchell, Robert D. Finn, Jaime Huerta-Cepas, Peer Bork, Georg Zeller, and Shinichi Sunagawa

Subjects
Science
Abstract

Metagenomic analysis based on universal phylogenetic marker gene (MG)-based operational taxonomic units (mOTUs) is a useful strategy, especially for microbial species without reference genomes. Here, the authors develop mOTUs2, an updated and functionally extended profiling tool for microbial abundance, activity and population profiling.

Published
2019
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4. Author Correction: Uncoupling of invasive bacterial mucosal immunogenicity from pathogenicity

Author

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, and Siegfried Hapfelmeier

Subjects
Science
Abstract

A Correction to this paper has been published: https://doi.org/10.1038/s41467-021-21096-5.

Published
2021
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5. Innate immunity restricts Citrobacter rodentium A/E pathogenesis initiation to an early window of opportunity.

Author

Stefanie Buschor, Miguelangel Cuenca, Stephanie S Uster, Olivier P Schären, Maria L Balmer, Miguel A Terrazos, Christian M Schürch, and Siegfried Hapfelmeier

Subjects
Immunologic diseases. Allergy, RC581-607, Biology (General), QH301-705.5
Abstract

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.

Published
2017
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6. D-Alanine-Controlled Transient Intestinal Mono-Colonization with Non-Laboratory-Adapted Commensal E. coli Strain HS.

Author

Miguelangel Cuenca, Simona P Pfister, Stefanie Buschor, Firuza Bayramova, Sara B Hernandez, Felipe Cava, Erkin Kuru, Michael S Van Nieuwenhze, Yves V Brun, Fernanda M Coelho, and Siegfried Hapfelmeier

Subjects
Medicine, Science
Abstract

Soon after birth the mammalian gut microbiota forms a permanent and collectively highly resilient consortium. There is currently no robust method for re-deriving an already microbially colonized individual again-germ-free. We previously developed the in vivo growth-incompetent E. coli K-12 strain HA107 that is auxotrophic for the peptidoglycan components D-alanine (D-Ala) and meso-diaminopimelic acid (Dap) and can be used to transiently associate germ-free animals with live bacteria, without permanent loss of germ-free status. Here we describe the translation of this experimental model from the laboratory-adapted E. coli K-12 prototype to the better gut-adapted commensal strain E. coli HS. In this genetic background it was necessary to complete the D-Ala auxotrophy phenotype by additional knockout of the hypothetical third alanine racemase metC. Cells of the resulting fully auxotrophic strain assembled a peptidoglycan cell wall of normal composition, as long as provided with D-Ala and Dap in the medium, but could not proliferate a single time after D-Ala/Dap removal. Yet, unsupplemented bacteria remained active and were able to complete their cell cycle with fully sustained motility until immediately before autolytic death. Also in vivo, the transiently colonizing bacteria retained their ability to stimulate a live-bacteria-specific intestinal Immunoglobulin (Ig)A response. Full D-Ala auxotrophy enabled rapid recovery to again-germ-free status. E. coli HS has emerged from human studies and genomic analyses as a paradigm of benign intestinal commensal E. coli strains. Its reversibly colonizing derivative may provide a versatile research tool for mucosal bacterial conditioning or compound delivery without permanent colonization.

Published
2016
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8. Additional file 1 of High throughput sequencing provides exact genomic locations of inducible prophages and accurate phage-to-host ratios in gut microbial strains

Author

Zünd, Mirjam, Hans-Joachim Ruscheweyh, Field, Christopher M., Meyer, Natalie, Miguelangel Cuenca, Hoces, Daniel, Wolf-Dietrich Hardt, and Sunagawa, Shinichi

Abstract

Additional file 1: Supplementary Figure S1. A correct reference genome sequence is favourable for determining accurate ΔPtoH ratios. Supplementary Figure S2: Several in vitro-induced Oligo-MM12 strains reveal genomic regions with putative prophages. Supplementary Figure S3. OPR analysis localtes a putative prophage region in cultured A. muris KB18 and F. plautii YL31. Supplementary Figure S4. Ex vivo induction of prophages in A. muciniphila YL44 and B. coccoides YL58.

Published
2021
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9. Import of Aspartate and Malate by DcuABC Drives H2/Fumarate Respiration to Promote Initial Salmonella Gut-Lumen Colonization in Mice

Author

Rebekka Bauer, Ersin Gül, Beat Christen, V Miguelangel Cuenca, Shinichi Sunagawa, Leanid Laganenka, Franziska Besser, Julia A. Vorholt, Laura Heeb, Steffen Porwollik, Philipp J. Keller, Bidong D. Nguyen, Joel Rüthi, Susanne Meile, Johannes Hartl, Lea Fuchs, Michael McClelland, Pau Pérez Escriva, Wolf-Dietrich Hardt, Matthias Christen, Uwe Sauer, Céline Margot, Céline Fetz, and Markus Furter

Subjects
Salmonella typhimurium, Male, Salmonella, Antiporter, Malates, Succinic Acid, medicine.disease_cause, Inbred C57BL, Feces, Mice, 0302 clinical medicine, Fumarates, Colonization, chemistry.chemical_classification, 0303 health sciences, Electron acceptor, Intestines, Infectious Diseases, Medical Microbiology, Administration, Female, Sequence Analysis, Oral, 16S, Anaerobic respiration, mouse model, Citric Acid Cycle, Immunology, Biology, Microbiology, 03 medical and health sciences, Metabolism, Intestine, Infection, Mouse model, Bacterial Proteins, Virology, Respiration, medicine, Escherichia coli, Animals, intestine, 030304 developmental biology, Ribosomal, Aspartic Acid, Animal, DNA, infection, Gastrointestinal Microbiome, Enzyme, Emerging Infectious Diseases, chemistry, Mutagenesis, Disease Models, RNA, Parasitology, Digestive Diseases, metabolism, 030217 neurology & neurosurgery
Abstract

Summary Initial enteropathogen growth in the microbiota-colonized gut is poorly understood. Salmonella Typhimurium is metabolically adaptable and can harvest energy by anaerobic respiration using microbiota-derived hydrogen (H2) as an electron donor and fumarate as an electron acceptor. As fumarate is scarce in the gut, the source of this electron acceptor is unclear. Here, transposon sequencing analysis along the colonization trajectory of S. Typhimurium implicates the C4-dicarboxylate antiporter DcuABC in early murine gut colonization. In competitive colonization assays, DcuABC and enzymes that convert the C4-dicarboxylates aspartate and malate into fumarate (AspA, FumABC), are required for fumarate/H2-dependent initial growth. Thus, S. Typhimurium obtains fumarate by DcuABC-mediated import and conversion of L-malate and L-aspartate. Fumarate reduction yields succinate, which is exported by DcuABC in exchange for L-aspartate and L-malate. This cycle allows S. Typhimurium to harvest energy by H2/fumarate respiration in the microbiota-colonized gut. This strategy may also be relevant for commensal E. coli diminishing the S. Typhimurium infection.

Published
2020

10. Microbial abundance, activity and population genomic profiling with mOTUs2

Author

Pascal Hingamp, Paul I. Costea, Renato J. Alves, Lucas Paoli, Alessio Milanese, Shinichi Sunagawa, Miguelangel Cuenca, Thomas Schmidt, Hans-Joachim Ruscheweyh, Daniel R. Mende, Georg Zeller, Luis Pedro Coelho, Jaime Huerta-Cepas, Alexandre Almeida, Alex L. Mitchell, Peer Bork, Robert D. Finn, Guillem Salazar, European Molecular Biology Laboratory (EMBL), University of Hawai'i [Honolulu] (UH), Institute of Microbiology and Swiss Institute of Bioinformatics, Instituto de Fisica [Mexico] (UASLP), Universidad Autonoma de San Luis Potosi [México] (UASLP), Eidgenössische Technische Hochschule - Swiss Federal Institute of Technology [Zürich] (ETH Zürich), 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)-Université de Toulon (UTLN)-Centre National de la Recherche Scientifique (CNRS), Heidelberg University, European Molecular Biology Laboratory [Heidelberg] (EMBL), Leuphana University of Lueneburg, National University of Singapore (NUS), Center for Genomic Regulation (CRG-UPF), CIBER de Epidemiología y Salud Pública (CIBERESP), European Molecular Biology Laboratory, European Molecular Biology Laboratory [Grenoble] (EMBL), and EMBL, ETH Zürich [PHRT-521], the Helmut Horten Foundation, and the Novartis Foundation for Medical-Biological Research [#17B077], the BMBF through the German Network for Bioinformatics Infrastructure (de.NBI) [#031A537B], and the European Molecular Biology Organization [ALTF 721-2015], LTFCOFUND2013 [PCOFUND-GA-2013-609409].

Subjects
0301 basic medicine, Genetic Markers, Science, Population, General Physics and Astronomy, 02 engineering and technology, Biology, Genome, General Biochemistry, Genetics and Molecular Biology, Article, 03 medical and health sciences, Phylogenetics, Cluster Analysis, Humans, lcsh:Science, education, Relative species abundance, Phylogeny, education.field_of_study, Multidisciplinary, Genes, Essential, Phylogenetic tree, Host Microbial Interactions, Gene Expression Profiling, Microbiota, Computational Biology, Molecular Sequence Annotation, General Chemistry, Sequence Analysis, DNA, 021001 nanoscience & nanotechnology, [SDV.BIBS]Life Sciences [q-bio]/Quantitative Methods [q-bio.QM], Housekeeping gene, Gene expression profiling, 030104 developmental biology, Evolutionary biology, Metagenomics, Cardiovascular and Metabolic Diseases, lcsh:Q, Microbiome, 0210 nano-technology, Sequence Alignment, Algorithms, Software
Abstract

Metagenomic sequencing has greatly improved our ability to profile the composition of environmental and host-associated microbial communities. However, the dependency of most methods on reference genomes, which are currently unavailable for a substantial fraction of microbial species, introduces estimation biases. We present an updated and functionally extended tool based on universal (i.e., reference-independent), phylogenetic marker gene (MG)-based operational taxonomic units (mOTUs) enabling the profiling of >7700 microbial species. As more than 30% of them could not previously be quantified at this taxonomic resolution, relative abundance estimates based on mOTUs are more accurate compared to other methods. As a new feature, we show that mOTUs, which are based on essential housekeeping genes, are demonstrably well-suited for quantification of basal transcriptional activity of community members. Furthermore, single nucleotide variation profiles estimated using mOTUs reflect those from whole genomes, which allows for comparing microbial strain populations (e.g., across different human body sites)., Nature Communications, 10 (1), ISSN:2041-1723

Published
2019
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11. Import of Aspartate and Malate by DcuABC Drives H

Author

Bidong D, Nguyen, Miguelangel, Cuenca V, Johannes, Hartl, Ersin, Gül, Rebekka, Bauer, Susanne, Meile, Joel, Rüthi, Céline, Margot, Laura, Heeb, Franziska, Besser, Pau Pérez, Escriva, Céline, Fetz, Markus, Furter, Leanid, Laganenka, Philipp, Keller, Lea, Fuchs, Matthias, Christen, Steffen, Porwollik, Michael, McClelland, Julia A, Vorholt, Uwe, Sauer, Shinichi, Sunagawa, Beat, Christen, and Wolf-Dietrich, Hardt

Subjects
Male, Salmonella typhimurium, Aspartic Acid, Citric Acid Cycle, Malates, Succinic Acid, Administration, Oral, Sequence Analysis, DNA, Gastrointestinal Microbiome, Intestines, Mice, Inbred C57BL, Disease Models, Animal, Feces, Mice, Bacterial Proteins, Fumarates, Mutagenesis, Salmonella, RNA, Ribosomal, 16S, Escherichia coli, Animals, Female
Abstract

Initial enteropathogen growth in the microbiota-colonized gut is poorly understood. Salmonella Typhimurium is metabolically adaptable and can harvest energy by anaerobic respiration using microbiota-derived hydrogen (H

Published
2019

12. Gene Expression Changes and Community Turnover Differentially Shape the Global Ocean Metatranscriptome

Author

Guillem Salazar, Lucas Paoli, Adriana Alberti, Jaime Huerta-Cepas, Hans-Joachim Ruscheweyh, Miguelangel Cuenca, Christopher M. Field, Luis Pedro Coelho, Corinne Cruaud, Stefan Engelen, Ann C. Gregory, Karine Labadie, Claudie Marec, Eric Pelletier, Marta Royo-Llonch, Simon Roux, Pablo Sánchez, Hideya Uehara, Ahmed A. Zayed, Georg Zeller, Margaux Carmichael, Céline Dimier, Joannie Ferland, Stefanie Kandels, Marc Picheral, Sergey Pisarev, Julie Poulain, Silvia G. Acinas, Marcel Babin, Peer Bork, Chris Bowler, Colomban de Vargas, Lionel Guidi, Pascal Hingamp, Daniele Iudicone, Lee Karp-Boss, Eric Karsenti, Hiroyuki Ogata, Stephane Pesant, Sabrina Speich, Matthew B. Sullivan, Patrick Wincker, Shinichi Sunagawa, Emmanuel Boss, Guy Cochrane, Michael Follows, Gabriel Gorsky, Nigel Grimsley, Olivier Jaillon, Stefanie Kandels-Lewis, Fabrice Not, Nicole Poulton, Jeroen Raes, Christian Sardet, Lars Stemmann, European Commission, Ministerio de Economía y Competitividad (España), Institut de Biologie François JACOB (JACOB), Direction de Recherche Fondamentale (CEA) (DRF (CEA)), Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA), Laboratoire d'océanographie de Villefranche (LOV), Institut national des sciences de l'Univers (INSU - CNRS)-Sorbonne Université (SU)-Centre National de la Recherche Scientifique (CNRS)-Institut de la Mer de Villefranche (IMEV), Sorbonne Université (SU)-Centre National de la Recherche Scientifique (CNRS)-Sorbonne Université (SU)-Centre National de la Recherche Scientifique (CNRS), Takuvik Joint International Laboratory ULAVAL-CNRS, Université Laval [Québec] (ULaval)-Centre National de la Recherche Scientifique (CNRS), Adaptation et diversité en milieu marin (AD2M), Station biologique de Roscoff (SBR), Sorbonne Université (SU)-Centre National de la Recherche Scientifique (CNRS)-Sorbonne Université (SU)-Centre National de la Recherche Scientifique (CNRS)-Centre National de la Recherche Scientifique (CNRS), Instituto de Fisica [Mexico] (UASLP), Universidad Autonoma de San Luis Potosi [México] (UASLP), Institute of Microbiology and Swiss Institute of Bioinformatics, CNS, Commissariat à l'énergie atomique et aux énergies alternatives (CEA), Center for Genomic Regulation (CRG-UPF), CIBER de Epidemiología y Salud Pública (CIBERESP), Eidgenössische Technische Hochschule - Swiss Federal Institute of Technology in Zürich [Zürich] (ETH Zürich), European Molecular Biology Laboratory [Heidelberg] (EMBL), Bayer Cropscience, Immunobiologie Cellulaire et Moléculaire des Infections Parasitaires, Université Pierre et Marie Curie - Paris 6 (UPMC)-IFR113-Institut National de la Santé et de la Recherche Médicale (INSERM), Laboratoire d'Océanographie Physique et Spatiale (LOPS), Institut de Recherche pour le Développement (IRD)-Institut Français de Recherche pour l'Exploitation de la Mer (IFREMER)-Université de Brest (UBO)-Centre National de la Recherche Scientifique (CNRS), Ohio State University [Columbus] (OSU), Institut de Chimie de Clermont-Ferrand - Clermont Auvergne (ICCF), Sigma CLERMONT (Sigma CLERMONT)-Université Clermont Auvergne (UCA)-Centre National de la Recherche Scientifique (CNRS), European Molecular Biology Laboratory [Grenoble] (EMBL), Station biologique de Roscoff [Roscoff] (SBR), Université Pierre et Marie Curie - Paris 6 (UPMC)-Centre National de la Recherche Scientifique (CNRS)-Université Pierre et Marie Curie - Paris 6 (UPMC)-Centre National de la Recherche Scientifique (CNRS)-Centre National de la Recherche Scientifique (CNRS), Takuvik Joint ULaval/CNRS Laboratory, Centre National de la Recherche Scientifique (CNRS)-Laval University [Québec], Institut de biologie de l'ENS Paris (UMR 8197/1024) (IBENS), Département de Biologie - ENS Paris, École normale supérieure - Paris (ENS Paris)-École normale supérieure - Paris (ENS Paris)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS), Institut de Génomique d'Evry (IG), Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Direction de Recherche Fondamentale (CEA) (DRF (CEA)), Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Université Paris-Saclay, Institute of Marine Sciences / Institut de Ciències del Mar [Barcelona] (ICM), Consejo Superior de Investigaciones Científicas [Spain] (CSIC), University of Maine, European Molecular Biology Laboratory European Bioinformatics Institute, Centre National de la Recherche Scientifique (CNRS)-Station biologique de Roscoff (SBR), Department of Earth, Atmospheric and Planetary Sciences [MIT, Cambridge] (EAPS), Massachusetts Institute of Technology (MIT), Observatoire océanologique de Villefranche-sur-mer (OOVM), Université Pierre et Marie Curie - Paris 6 (UPMC)-Institut national des sciences de l'Univers (INSU - CNRS)-Centre National de la Recherche Scientifique (CNRS)-Université Pierre et Marie Curie - Paris 6 (UPMC)-Institut national des sciences de l'Univers (INSU - CNRS)-Centre National de la Recherche Scientifique (CNRS)-Centre National de la Recherche Scientifique (CNRS), Biologie intégrative des organismes marins (BIOM), Sorbonne Université (SU)-Centre National de la Recherche Scientifique (CNRS)-Observatoire océanologique de Banyuls (OOB), Sorbonne Université (SU)-Centre National de la Recherche Scientifique (CNRS)-Centre National de la Recherche Scientifique (CNRS), Institut méditerranéen d'océanologie (MIO), Institut de Recherche pour le Développement (IRD)-Aix Marseille Université (AMU)-Université de Toulon (UTLN)-Centre National de la Recherche Scientifique (CNRS), Sezione Ecologia Marina Integrata, Stazione Zoologica Anton Dohrn (SZN), Sorbonne Université (SU)-Centre National de la Recherche Scientifique (CNRS), Information génomique et structurale (IGS), Aix Marseille Université (AMU)-Centre National de la Recherche Scientifique (CNRS), Center for Marine Environmental Sciences [Bremen] (MARUM), Universität Bremen, Bigelow Laboratory for Ocean Sciences, Department of Bioscience Engineering, Vrije Universiteit Brussel (VUB), Laboratoire de Biologie du Développement de Villefranche sur mer (LBDV), Institut de la Mer de Villefranche (IMEV), Sorbonne Université (SU)-Centre National de la Recherche Scientifique (CNRS)-Sorbonne Université (SU)-Centre National de la Recherche Scientifique (CNRS)-Centre National de la Recherche Scientifique (CNRS)-Sorbonne Université (SU), Laboratoire de physique des océans (LPO), Genoscope - Centre national de séquençage [Evry] (GENOSCOPE), Université Paris-Saclay-Direction de Recherche Fondamentale (CEA) (DRF (CEA)), 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), Eidgenössische Technische Hochschule - Swiss Federal Institute of Technology [Zürich] (ETH Zürich), Université Paris-Saclay, Institut de Recherche pour le Développement (IRD)-Institut Français de Recherche pour l'Exploitation de la Mer (IFREMER)-Institut national des sciences de l'Univers (INSU - CNRS)-Université de Brest (UBO)-Centre National de la Recherche Scientifique (CNRS), Centro de Investigaciones Biológicas (CSIC), Consejo Superior de Investigaciones Científicas [Madrid] (CSIC), Kyoto University, Adaptation et diversité en milieu marin (ADMM), Institut national des sciences de l'Univers (INSU - CNRS)-Station biologique de Roscoff (SBR), Kyoto University [Kyoto], Sorbonne Université (SU)-Centre National de la Recherche Scientifique (CNRS)-Institut de la Mer de Villefranche (IMEV), and Centre National de la Recherche Scientifique (CNRS)-Université Laval [Québec] (ULaval)

Subjects
ASSEMBLY PROCESSES, Effects of global warming on oceans, DIVERSITY, microbial ecology, global ocean microbiome, CARBON, 0302 clinical medicine, biogeochemistry, Gene expression, ComputingMilieux_MISCELLANEOUS, 0303 health sciences, CLIMATE-CHANGE, Geography, Microbiota, Temperature, CYANOBACTERIA, [SDV.BIBS]Life Sciences [q-bio]/Quantitative Methods [q-bio.QM], GENOME, BACTERIA, community turnover, Life Sciences & Biomedicine, Biochemistry & Molecular Biology, SURFACE, Oceans and Seas, Tara Oceans, Biology, Article, metagenome, General Biochemistry, Genetics and Molecular Biology, ocean warming, 03 medical and health sciences, eco-systems biology, Microbial ecology, [SDV.BBM.GTP]Life Sciences [q-bio]/Biochemistry, Molecular Biology/Genomics [q-bio.GN], metatranscriptome, Seawater, RNA, Messenger, 14. Life underwater, Gene, [SDU.STU.OC]Sciences of the Universe [physics]/Earth Sciences/Oceanography, 030304 developmental biology, Science & Technology, Biogeochemistry, Molecular Sequence Annotation, Cell Biology, Environmental variation, Gene Expression Regulation, Cardiovascular and Metabolic Diseases, 13. Climate action, Metagenomics, Evolutionary biology, BIODIVERSITY, sense organs, [SDE.BE]Environmental Sciences/Biodiversity and Ecology, Transcriptome, 030217 neurology & neurosurgery, gene expression change, BIOGEOGRAPHY
Abstract

This article is contribution number 94 of Tara Oceans.-- 37 pages, 20 figures, 1 table, supplementary information https://doi.org/10.1016/j.cell.2019.10.014.-- All raw reads are available through ENA at https://www.ebi.ac.uk/ena using the identifiers listed in https://doi.org/10.5281/zenodo.3473199. Processed data are accessible at https://www.ebi.ac.uk/biostudies/studies/S-BSST297, and additional information is provided in https://doi.org/10.5281/zenodo.3473199 and at the companion website: https://www.ocean-microbiome.org. Scripts used in this manuscript are available through a Github repository at https://github.com/SushiLab/omrgc_v2_scripts, Ocean microbial communities strongly influence the biogeochemistry, food webs, and climate of our planet. Despite recent advances in understanding their taxonomic and genomic compositions, little is known about how their transcriptomes vary globally. Here, we present a dataset of 187 metatranscriptomes and 370 metagenomes from 126 globally distributed sampling stations and establish a resource of 47 million genes to study community-level transcriptomes across depth layers from pole-to-pole. We examine gene expression changes and community turnover as the underlying mechanisms shaping community transcriptomes along these axes of environmental variation and show how their individual contributions differ for multiple biogeochemically relevant processes. Furthermore, we find the relative contribution of gene expression changes to be significantly lower in polar than in non-polar waters and hypothesize that in polar regions, alterations in community activity in response to ocean warming will be driven more strongly by changes in organismal composition than by gene regulatory mechanisms, Tara Oceans (that includes both the Tara Oceans and Tara Oceans Polar Circle expeditions) would not exist without the leadership of the Tara Expeditions Foundation and the continuous support of 23 institutes (https://oceans.taraexpeditions.org). We further thank the commitment of the following sponsors: CNRS (in particular Groupement de Recherche GDR3280 and the Research Federation for the study of Global Ocean Systems Ecology and Evolution, FR2022/Tara Oceans-GOSEE); European Molecular Biology Laboratory (EMBL); Genoscope/CEA; the French Ministry of Research; the French Government “Investissements d’Avenir” programmes OCEANOMICS (ANR-11-BTBR-0008), FRANCE GENOMIQUE (ANR-10-INBS-09-08), MEMO LIFE (ANR-10-LABX-54), and PSL∗ Research University (ANR-11-IDEX-0001-02); Gordon and Betty Moore Foundation (award 3790); the US National Science Foundation (OCE#1536989 and OCE#1829831 to M.B.S.); the European Union’s Horizon 2020 research and innovation programme (grant agreement 686070); and the Ohio Supercomputer and the EMBL and ETH Zürich HPC facilities for computational support. Funding for the collection and processing of the TARA data set was provided by NASA Ocean Biology and Biogeochemistry program under grants NNX11AQ14G, NNX09AU43G, NNX13AE58G, and NNX15AC08G to the University of Maine and Canada Excellence Research Chair on Remote sensing of Canada’s new Arctic frontier Canada Foundation for Innovation. C.B. acknowledges funding from the European Research Council (ERC) under the European Union's Horizon 2020 research and innovation program (grant agreement 835067). S.G.A. thanks the Spanish Ministry of Economy and Competitiveness (CTM2017-87736-R). S. Sunagawa. is supported by the ETH and the Helmut Horten Foundation and by funding from the Swiss National Foundation (205321_184955)

Published
2019
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13. Import of Aspartate and Malate by DcuABC Drives H 2/Fumarate Respiration to Promote Salmonella Gut-Luminal Colonization

Author

Matthias Christen, Julia A. Vorholt, Laura Heeb, V Miguelangel Cuenca, Bidong D. Nguyen, Michael McClelland, Pau Pérez Escriva, Susanne Meile, Uwe Sauer, Céline Fetz, Steffen Porwollik, Markus Furter, Céline Margot, Rebekka Bauer, Franziska Besser, Shinichi Sunagawa, Beat Christen, Joel Rüthi, Johannes Hartl, and Wolf-Dietrich Hardt

Subjects
chemistry.chemical_classification, Salmonella, Anaerobic respiration, Chemistry, Electron donor, Metabolism, Electron acceptor, medicine.disease_cause, chemistry.chemical_compound, Enzyme, Biochemistry, Respiration, medicine, Gene
Abstract

Enteropathogen growth in the microbiota-colonized gut is poorly understood. Salmonella Typhimurium is metabolically plastic and can harvest energy by anaerobic respiration using hydrogen (H2), a product of microbiota metabolism, as an electron donor and fumarate as an electron acceptor. As fumarate is scarce in the gut, the source of this electron acceptor is unclear. Transposon sequencing analysis along the colonization-trajectory of S.Typhimurium implicated the C4-dicarboxylate exchanger DcuABC in murine gut colonization. In competitive colonization assays, DcuABC and enzymes converting the C4-dicarboxylates aspartate and malate into fumarate (AspA, FumABC), were required for fumarate/H2-dependent growth. Thus, S.Typhimurium obtains fumarate by DcuABC-mediated import and the subsequent conversion of L-malate and L-aspartate into fumarate. Fumarate reduction yields succinate, which is exported by DcuABC in exchange for L-aspartate and L-malate. This mechanism allows S.Typhimurium to harvest energy by H2/fumarate respiration in the microbiota-colonized gut. It might be relevant for other enteropathogens encoding the requisite genes.

Published
2019
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14. Microbiota-Derived Compounds Drive Steady-State Granulopoiesis via MyD88/TICAM Signaling.

Author

Balmer, Maria L., Schürch, Christian M., Yasuyuki Saito, Geuking, Markus B., Hai Li, Miguelangel Cuenca, Kovtonyuk, Larisa V., McCoy, Kathy D., Hapfelmeier, Siegfried, Ochsenbein, Adrian F., Manz, Markus G., Slack, Emma, and Macpherson, Andrew J.

Subjects
*MYELOID differentiation factor 88, *NEUTROPENIA, *NEUTROPHIL immunology, *BONE marrow cells, *IMMUNOGLOBULIN G, *LABORATORY mice, *GENETICS
Abstract

Neutropenia is probably the strongest known predisposition to infection with otherwise harmless environmental or microbiota-derived species. Because initial swarming of neutrophils at the site of infection occurs within minutes, rather than the hours required to induce "emergency granulopoiesis," the relevance of having high numbers of these cells available at any one time is obvious. We observed that germ-free (GF) animals show delayed clearance of an apathogenic bacterium after systemic challenge. In this article, we show that the size of the bone marrow myeloid cell pool correlates strongly with the complexity of the intestinal microbiota. The effect of colonization can be recapitulated by transferring sterile heat-treated serum from colonized mice into GF wild-type mice. TLR signaling was essential for microbiota-driven myelopoiesis, as microbiota colonization or transferring serum from colonized animals had no effect in GF MyD88-/-TICAM1-/- mice. Amplification of myelopoiesis occurred in the absence of microbiota-specific IgG production. Thus, very low concentrations of microbial Ags and TLR ligands, well below the threshold required for induction of adaptive immunity, sets the bone marrow myeloid cell pool size. Coevolution of mammals with their microbiota has probably led to a reliance on microbiota-derived signals to provide tonic stimulation to the systemic innate immune system and to maintain vigilance to infection. This suggests that microbiota changes observed in dysbiosis, obesity, or antibiotic therapy may affect the cross talk between hematopoiesis and the microbiota, potentially exacerbating inflammatory or infectious states in the host. [ABSTRACT FROM AUTHOR]

Published
2014
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