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3. Randomly barcoded transposon mutant libraries for gut commensals I: Strategies for efficient library construction

Author

Tripathi, Surya, Voogdt, Carlos Geert Pieter, Bassler, Stefan Oliver, Anderson, Mary, Huang, Po-Hsun, Sakenova, Nazgul, Capraz, Tümay, Jain, Sunit, Koumoutsi, Alexandra, Bravo, Afonso Martins, Trotter, Valentine, Zimmerman, Michael, Sonnenburg, Justin L, Buie, Cullen, Typas, Athanasios, Deutschbauer, Adam M, Shiver, Anthony L, and Huang, Kerwyn Casey

Subjects
Biological Sciences, Genetics, DNA Transposable Elements, High-Throughput Nucleotide Sequencing, Cloning, Molecular, Gene Library, Bacteria, Mutagenesis, Insertional, CP: Microbiology, RB-Tn-seq, arrayed libraries, functional genomics, gut microbiota, in vitro screening, magic pools, protein function, transposon mutagenesis, Biochemistry and Cell Biology, Medical Physiology, Biological sciences
Abstract

Randomly barcoded transposon mutant libraries are powerful tools for studying gene function and organization, assessing gene essentiality and pathways, discovering potential therapeutic targets, and understanding the physiology of gut bacteria and their interactions with the host. However, construction of high-quality libraries with uniform representation can be challenging. In this review, we survey various strategies for barcoded library construction, including transposition systems, methods of transposon delivery, optimal library size, and transconjugant selection schemes. We discuss the advantages and limitations of each approach, as well as factors to consider when selecting a strategy. In addition, we highlight experimental and computational advances in arraying condensed libraries from mutant pools. We focus on examples of successful library construction in gut bacteria and their application to gene function studies and drug discovery. Given the need for understanding gene function and organization in gut bacteria, we provide a comprehensive guide for researchers to construct randomly barcoded transposon mutant libraries.

Published
2024

8. Systematic analysis of drug combinations against Gram-positive bacteria

Author

Cacace, Elisabetta, Kim, Vladislav, Varik, Vallo, Knopp, Michael, Tietgen, Manuela, Brauer-Nikonow, Amber, Inecik, Kemal, Mateus, André, Milanese, Alessio, Mårli, Marita Torrissen, Mitosch, Karin, Selkrig, Joel, Brochado, Ana Rita, Kuipers, Oscar P., Kjos, Morten, Zeller, Georg, Savitski, Mikhail M., Göttig, Stephan, Huber, Wolfgang, and Typas, Athanasios

Published
2023
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12. A Dual-Mechanism Antibiotic Kills Gram-Negative Bacteria and Avoids Drug Resistance

Author

Martin, James K, Sheehan, Joseph P, Bratton, Benjamin P, Moore, Gabriel M, Mateus, André, Li, Sophia Hsin-Jung, Kim, Hahn, Rabinowitz, Joshua D, Typas, Athanasios, Savitski, Mikhail M, Wilson, Maxwell Z, and Gitai, Zemer

Subjects
Biodefense, Antimicrobial Resistance, Prevention, Emerging Infectious Diseases, Infectious Diseases, Vaccine Related, 5.1 Pharmaceuticals, Development of treatments and therapeutic interventions, 2.2 Factors relating to the physical environment, Aetiology, Infection, Animals, Anti-Bacterial Agents, Cell Membrane, Drug Resistance, Bacterial, Female, Folic Acid, Gram-Negative Bacteria, Gram-Positive Bacteria, HEK293 Cells, Humans, Male, Methicillin-Resistant Staphylococcus aureus, Mice, Mice, Inbred BALB C, Microbial Sensitivity Tests, Ovariectomy, Proteomics, Pseudomonas aeruginosa, Pyrroles, Quinazolines, Acinetobacter baumannii, Gram-negative pathogens, Neisseria gonorrhoeae, antibiotics, broad spectrum, dual-target drugs, folate metabolism, membrane disrupting, Biological Sciences, Medical and Health Sciences, Developmental Biology
Abstract

The rise of antibiotic resistance and declining discovery of new antibiotics has created a global health crisis. Of particular concern, no new antibiotic classes have been approved for treating Gram-negative pathogens in decades. Here, we characterize a compound, SCH-79797, that kills both Gram-negative and Gram-positive bacteria through a unique dual-targeting mechanism of action (MoA) with undetectably low resistance frequencies. To characterize its MoA, we combined quantitative imaging, proteomic, genetic, metabolomic, and cell-based assays. This pipeline demonstrates that SCH-79797 has two independent cellular targets, folate metabolism and bacterial membrane integrity, and outperforms combination treatments in killing methicillin-resistant Staphylococcus aureus (MRSA) persisters. Building on the molecular core of SCH-79797, we developed a derivative, Irresistin-16, with increased potency and showed its efficacy against Neisseria gonorrhoeae in a mouse vaginal infection model. This promising antibiotic lead suggests that combining multiple MoAs onto a single chemical scaffold may be an underappreciated approach to targeting challenging bacterial pathogens.

Published
2020

14. Bacterial retrons encode phage-defending tripartite toxin–antitoxin systems

Author

Bobonis, Jacob, Mitosch, Karin, Mateus, André, Karcher, Nicolai, Kritikos, George, Selkrig, Joel, Zietek, Matylda, Monzon, Vivian, Pfalz, Birgit, Garcia-Santamarina, Sarela, Galardini, Marco, Sueki, Anna, Kobayashi, Callie, Stein, Frank, Bateman, Alex, Zeller, Georg, Savitski, Mikhail M., Elfenbein, Johanna R., Andrews-Polymenis, Helene L., and Typas, Athanasios

Published
2022
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15. LD-transpeptidation is crucial for fitness and polar growth in Agrobacterium tumefaciens.

Author

Aliashkevich, Alena, Guest, Thomas, Alvarez, Laura, Gilmore, Michael C., Rea, Daniel, Amstutz, Jennifer, Mateus, André, Schiffthaler, Bastian, Ruiz, Iñigo, Typas, Athanasios, Savitski, Mikhail M., Brown, Pamela J. B., and Cava, Felipe

Subjects
PHYTOPATHOGENIC microorganisms, CELL morphology, CARRIER proteins, MICROBIAL cells, MEMBRANE proteins, AGROBACTERIUM tumefaciens, BACTERIAL cell walls
Abstract

Peptidoglycan (PG), a mesh-like structure which is the primary component of the bacterial cell wall, is crucial to maintain cell integrity and shape. While most bacteria rely on penicillin binding proteins (PBPs) for crosslinking, some species also employ LD-transpeptidases (LDTs). Unlike PBPs, the essentiality and biological functions of LDTs remain largely unclear. The Hyphomicrobiales order of the Alphaproteobacteria, known for their polar growth, have PG which is unusually rich in LD-crosslinks, suggesting that LDTs may play a more significant role in PG synthesis in these bacteria. Here, we investigated LDTs in the plant pathogen Agrobacterium tumefaciens and found that LD-transpeptidation, resulting from at least one of 14 putative LDTs present in this bacterium, is essential for its survival. Notably, a mutant lacking a distinctive group of 7 LDTs which are broadly conserved among the Hyphomicrobiales exhibited reduced LD-crosslinking and tethering of PG to outer membrane β-barrel proteins. Consequently, this mutant suffered severe fitness loss and cell shape rounding, underscoring the critical role played by these Hyphomicrobiales-specific LDTs in maintaining cell wall integrity and promoting elongation. Tn-sequencing screens further revealed non-redundant functions for A. tumefaciens LDTs. Specifically, Hyphomicrobiales-specific LDTs exhibited synthetic genetic interactions with division and cell cycle proteins, and a single LDT from another group. Additionally, our findings demonstrate that strains lacking all LDTs except one displayed distinctive phenotypic profiles and genetic interactions. Collectively, our work emphasizes the critical role of LD-crosslinking in A. tumefaciens cell wall integrity and growth and provides insights into the functional specialization of these crosslinking activities. Author summary: Peptidoglycan (PG) is essential for bacterial cell wall integrity. While most bacteria use penicillin binding proteins (PBPs) for crosslinking, some also employ LD-transpeptidases (LDTs); however, the essentiality and functions of LDTs remain poorly understood. Interestingly, Hyphomicrobiales bacteria have PG rich in LD-crosslinks, suggesting that LDTs play a vital role in maintaining cell wall integrity in these organisms. Our study of Agrobacterium tumefaciens revealed that LD-transpeptidation, mediated by at least one of 14 putative LDTs, is essential for maintaining both viability and morphogenesis. A mutant lacking 7 Hyphomicrobiales-specific LDTs suffered fitness and shape loss due to reduced LD-crosslinking and PG tethering to the outer membrane. Our results provide new insights into LD-transpeptidase specialized functions and conditional essentiality. The conservation of these enzymes across diverse polar-growing species suggests broader implications for understanding microbial cell wall growth and adaptation to environmental stresses. [ABSTRACT FROM AUTHOR]

Published
2024
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16. High-throughput functional characterization of protein phosphorylation sites in yeast

Author

Viéitez, Cristina, Busby, Bede P., Ochoa, David, Mateus, André, Memon, Danish, Galardini, Marco, Yildiz, Umut, Trovato, Matteo, Jawed, Areeb, Geiger, Alexander G., Oborská-Oplová, Michaela, Potel, Clement M., Vonesch, Sibylle C., Szu Tu, Chelsea, Shahraz, Mohammed, Stein, Frank, Steinmetz, Lars M., Panse, Vikram G., Noh, Kyung-Min, Savitski, Mikhail M., Typas, Athanasios, and Beltrao, Pedro

Published
2022
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17. Uncovering nitroxoline activity spectrum, mode of action and resistance across Gram-negative bacteria

Author

Cacace, Elisabetta, primary, Tietgen, Manuela, additional, Steinhauer, Meike, additional, Mateus, André, additional, Schultze, Tilman G., additional, Eckermann, Marina, additional, Galardini, Marco, additional, Varik, Vallo, additional, Koumoutsi, Alexandra, additional, Parzeller, Jordan J., additional, Corona, Federico, additional, Orakov, Askarbek, additional, Knopp, Michael, additional, Brauer-Nikonow, Amber, additional, Bork, Peer, additional, Romao, Celia V., additional, Zimmermann, Michael, additional, Cloetens, Peter, additional, Savitski, Mikhail M., additional, Typas, Athanasios, additional, and Göttig, Stephan, additional

Published
2024
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18. Emergent survival and extinction of species within gut bacterial communities

Author

van den Berg, Naomi Iris, primary, Tramontano, Melanie, additional, Guan, Rui, additional, Andrejev, Sergej, additional, Blasche, Sonja, additional, Kim, Yongkyu, additional, Klunemann, Martina, additional, Gontao Brochado, Ana Rita, additional, Kalmar, Lajos, additional, Telzerow, Anja, additional, Bork, Peer, additional, Sevin, Daniel, additional, Typas, Athanasios, additional, and Patil, Kiran Raosaheb, additional

Published
2024
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19. Unravelling the collateral damage of antibiotics on gut bacteria

Author

Maier, Lisa, Goemans, Camille V., Wirbel, Jakob, Kuhn, Michael, Eberl, Claudia, Pruteanu, Mihaela, Müller, Patrick, Garcia-Santamarina, Sarela, Cacace, Elisabetta, Zhang, Boyao, Gekeler, Cordula, Banerjee, Tisya, Anderson, Exene Erin, Milanese, Alessio, Löber, Ulrike, Forslund, Sofia K., Patil, Kiran Raosaheb, Zimmermann, Michael, Stecher, Bärbel, Zeller, Georg, Bork, Peer, and Typas, Athanasios

Published
2021
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21. Bioaccumulation of therapeutic drugs by human gut bacteria

Author

Klünemann, Martina, Andrejev, Sergej, Blasche, Sonja, Mateus, Andre, Phapale, Prasad, Devendran, Saravanan, Vappiani, Johanna, Simon, Bernd, Scott, Timothy A., Kafkia, Eleni, Konstantinidis, Dimitrios, Zirngibl, Katharina, Mastrorilli, Eleonora, Banzhaf, Manuel, Mackmull, Marie-Therese, Hövelmann, Felix, Nesme, Leo, Brochado, Ana Rita, Maier, Lisa, Bock, Thomas, Periwal, Vinita, Kumar, Manjeet, Kim, Yongkyu, Tramontano, Melanie, Schultz, Carsten, Beck, Martin, Hennig, Janosch, Zimmermann, Michael, Sévin, Daniel C., Cabreiro, Filipe, Savitski, Mikhail M., Bork, Peer, Typas, Athanasios, and Patil, Kiran R.

Published
2021
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25. Spatiotemporal proteomics uncovers cathepsin-dependent macrophage cell death during Salmonella infection

Author

Selkrig, Joel, Li, Nan, Hausmann, Annika, Mangan, Matthew S. J., Zietek, Matylda, Mateus, André, Bobonis, Jacob, Sueki, Anna, Imamura, Haruna, El Debs, Bachir, Sigismondo, Gianluca, Florea, Bogdan I., Overkleeft, Herman S., Kopitar-Jerala, Nataša, Turk, Boris, Beltrao, Pedro, Savitski, Mikhail M., Latz, Eicke, Hardt, Wolf-Dietrich, Krijgsveld, Jeroen, and Typas, Athanasios

Published
2020
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27. High-throughput anaerobic screening for identifying compounds acting against gut bacteria in monocultures or communities

Author

Müller, Patrick, primary, de la Cuesta-Zuluaga, Jacobo, additional, Kuhn, Michael, additional, Baghai Arassi, Maral, additional, Treis, Tim, additional, Blasche, Sonja, additional, Zimmermann, Michael, additional, Bork, Peer, additional, Patil, Kiran Raosaheb, additional, Typas, Athanasios, additional, Garcia-Santamarina, Sarela, additional, and Maier, Lisa, additional

Published
2023
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29. A new antibiotic selectively kills Gram-negative pathogens

Author

Imai, Yu, Meyer, Kirsten J., Iinishi, Akira, Favre-Godal, Quentin, Green, Robert, Manuse, Sylvie, Caboni, Mariaelena, Mori, Miho, Niles, Samantha, Ghiglieri, Meghan, Honrao, Chandrashekhar, Ma, Xiaoyu, Guo, Jason J., Makriyannis, Alexandros, Linares-Otoya, Luis, Böhringer, Nils, Wuisan, Zerlina G., Kaur, Hundeep, Wu, Runrun, Mateus, André, Typas, Athanasios, Savitski, Mikhail M., Espinoza, Josh L., O’Rourke, Aubrie, Nelson, Karen E., Hiller, Sebastian, Noinaj, Nicholas, Schäberle, Till F., D’Onofrio, Anthony, and Lewis, Kim

Published
2019
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30. Escherichia coli limits Salmonella Typhimurium infections after diet shifts and fat-mediated microbiota perturbation in mice

Author

Wotzka, Sandra Y., Kreuzer, Markus, Maier, Lisa, Arnoldini, Markus, Nguyen, Bidong D., Brachmann, Alexander O., Berthold, Dorothée L., Zünd, Mirjam, Hausmann, Annika, Bakkeren, Erik, Hoces, Daniel, Gül, Ersin, Beutler, Markus, Dolowschiak, Tamas, Zimmermann, Michael, Fuhrer, Tobias, Moor, Kathrin, Sauer, Uwe, Typas, Athanasios, Piel, Jörn, Diard, Médéric, Macpherson, Andrew J., Stecher, Bärbel, Sunagawa, Shinichi, Slack, Emma, and Hardt, Wolf-Dietrich

Published
2019
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32. SARS‐CoV‐2 infection remodels the host protein thermal stability landscape

Author

Selkrig, Joel, Stanifer, Megan, Mateus, André, Mitosch, Karin, Barrio‐Hernandez, Inigo, Rettel, Mandy, Kim, Heeyoung, Voogdt, Carlos G P, Walch, Philipp, Kee, Carmon, Kurzawa, Nils, Stein, Frank, Potel, Clément, Jarzab, Anna, Kuster, Bernhard, Bartenschlager, Ralf, Boulant, Steeve, Beltrao, Pedro, Typas, Athanasios, and Savitski, Mikhail M

Published
2021
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33. Regulation of Peptidoglycan Synthesis by Outer-Membrane Proteins

Author

Typas, Athanasios, Banzhaf, Manuel, Saparoea, Bart van den Berg van, Verheul, Jolanda, Biboy, Jacob, Nichols, Robert J, Zietek, Matylda, Beilharz, Katrin, Kannenberg, Kai, von Rechenberg, Moritz, Breukink, Eefjan, Blaauwen, Tanneke den, Gross, Carol A, and Vollmer, Waldemar

Subjects
Biochemistry and Cell Biology, Biological Sciences, 1.1 Normal biological development and functioning, Underpinning research, Generic health relevance, Bacterial Outer Membrane Proteins, Cell Division, Cell Wall, Escherichia coli, Escherichia coli Proteins, Lipoproteins, Penicillin-Binding Proteins, Peptidoglycan, Peptidoglycan Glycosyltransferase, Protein Interaction Domains and Motifs, Medical and Health Sciences, Developmental Biology, Biological sciences, Biomedical and clinical sciences
Abstract

Growth of the mesh-like peptidoglycan (PG) sacculus located between the bacterial inner and outer membranes (OM) is tightly regulated to ensure cellular integrity, maintain cell shape, and orchestrate division. Cytoskeletal elements direct placement and activity of PG synthases from inside the cell, but precise spatiotemporal control over this process is poorly understood. We demonstrate that PG synthases are also controlled from outside of the sacculus. Two OM lipoproteins, LpoA and LpoB, are essential for the function, respectively, of PBP1A and PBP1B, the major E. coli bifunctional PG synthases. Each Lpo protein binds specifically to its cognate PBP and stimulates its transpeptidase activity, thereby facilitating attachment of new PG to the sacculus. LpoB shows partial septal localization, and our data suggest that the LpoB-PBP1B complex contributes to OM constriction during cell division. LpoA/LpoB and their PBP-docking regions are restricted to γ-proteobacteria, providing models for niche-specific regulation of sacculus growth.

Published
2010

36. Consistency across multi‐omics layers in a drug‐perturbed gut microbial community

Author

Wuyts, Sander, primary, Alves, Renato, additional, Zimmermann‐Kogadeeva, Maria, additional, Nishijima, Suguru, additional, Blasche, Sonja, additional, Driessen, Marja, additional, Geyer, Philipp E, additional, Hercog, Rajna, additional, Kartal, Ece, additional, Maier, Lisa, additional, Müller, Johannes B, additional, Garcia Santamarina, Sarela, additional, Schmidt, Thomas Sebastian B, additional, Sevin, Daniel C, additional, Telzerow, Anja, additional, Treit, Peter V, additional, Wenzel, Tobias, additional, Typas, Athanasios, additional, Patil, Kiran R, additional, Mann, Matthias, additional, Kuhn, Michael, additional, and Bork, Peer, additional

Published
2023
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40. High-throughput, quantitative analyses of genetic interactions in E. coli

Author

Typas, Athanasios, Nichols, Robert J, Siegele, Deborah A, Shales, Michael, Collins, Sean R, Lim, Bentley, Braberg, Hannes, Yamamoto, Natsuko, Takeuchi, Rikiya, Wanner, Barry L, Mori, Hirotada, Weissman, Jonathan S, Krogan, Nevan J, and Gross, Carol A

Subjects
Biological Sciences, Genetics, Human Genome, Biotechnology, 2.2 Factors relating to the physical environment, Aetiology, Infection, Conjugation, Genetic, Escherichia coli, Genome, Bacterial, Mutation, Technology, Medical and Health Sciences, Developmental Biology, Biological sciences
Abstract

Large-scale genetic interaction studies provide the basis for defining gene function and pathway architecture. Recent advances in the ability to generate double mutants en masse in Saccharomyces cerevisiae have dramatically accelerated the acquisition of genetic interaction information and the biological inferences that follow. Here we describe a method based on F factor-driven conjugation, which allows for high-throughput generation of double mutants in Escherichia coli. This method, termed genetic interaction analysis technology for E. coli (GIANT-coli), permits us to systematically generate and array double-mutant cells on solid media in high-density arrays. We show that colony size provides a robust and quantitative output of cellular fitness and that GIANT-coli can recapitulate known synthetic interactions and identify previously unidentified negative (synthetic sickness or lethality) and positive (suppressive or epistatic) relationships. Finally, we describe a complementary strategy for genome-wide suppressor-mutant identification. Together, these methods permit rapid, large-scale genetic interaction studies in E. coli.

Published
2008

42. Host-Microbe Co-metabolism Dictates Cancer Drug Efficacy in C. elegans

Author

Scott, Timothy A., Quintaneiro, Leonor M., Norvaisas, Povilas, Lui, Prudence P., Wilson, Matthew P., Leung, Kit-Yi, Herrera-Dominguez, Lucia, Sudiwala, Sonia, Pessia, Alberto, Clayton, Peter T., Bryson, Kevin, Velagapudi, Vidya, Mills, Philippa B., Typas, Athanasios, Greene, Nicholas D.E., and Cabreiro, Filipe

Published
2017
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44. Outer membrane lipoprotein NlpI scaffolds peptidoglycan hydrolases within multi‐enzyme complexes in Escherichia coli

Author

Banzhaf, Manuel, Yau, Hamish CL, Verheul, Jolanda, Lodge, Adam, Kritikos, George, Mateus, André, Cordier, Baptiste, Hov, Ann Kristin, Stein, Frank, Wartel, Morgane, Pazos, Manuel, Solovyova, Alexandra S, Breukink, Eefjan, van Teeffelen, Sven, Savitski, Mikhail M, den Blaauwen, Tanneke, Typas, Athanasios, and Vollmer, Waldemar

Published
2020
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46. Recovery of gut microbiota of healthy adults following antibiotic exposure

Author

Palleja, Albert, Mikkelsen, Kristian H., Forslund, Sofia K., Kashani, Alireza, Allin, Kristine H., Nielsen, Trine, Hansen, Tue H., Liang, Suisha, Feng, Qiang, Zhang, Chenchen, Pyl, Paul Theodor, Coelho, Luis Pedro, Yang, Huanming, Wang, Jian, Typas, Athanasios, Nielsen, Morten F., Nielsen, Henrik Bjorn, Bork, Peer, Wang, Jun, Vilsbøll, Tina, Hansen, Torben, Knop, Filip K., Arumugam, Manimozhiyan, and Pedersen, Oluf

Published
2018
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47. Species-specific activity of antibacterial drug combinations

Author

Brochado, Ana Rita, Telzerow, Anja, Bobonis, Jacob, Banzhaf, Manuel, Mateus, André, Selkrig, Joel, Huth, Emily, Bassler, Stefan, Zamarreño Beas, Jordi, Zietek, Matylda, Ng, Natalie, Foerster, Sunniva, Ezraty, Benjamin, Py, Béatrice, Barras, Frédéric, Savitski, Mikhail M., Bork, Peer, Göttig, Stephan, and Typas, Athanasios

Published
2018
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50. The killing of human gut commensal E. coli ED1a by tetracycline is associated with severe ribosome dysfunction

Author

Khusainov, Iskander, Romanov, Natalie, Goemans, Camille, Turoňová, Beata, Zimmerli, Christian Eugen, Welsch, Sonja, Langer, Julian David, Typas, Athanasios, Beck, Martin, Khusainov, Iskander, Romanov, Natalie, Goemans, Camille, Turoňová, Beata, Zimmerli, Christian Eugen, Welsch, Sonja, Langer, Julian David, Typas, Athanasios, and Beck, Martin

Abstract

Ribosomes translate the genetic code into proteins. Recent technical advances have facilitated in situ structural analyses of ribosome functional states inside eukaryotic cells and the minimal bacterium Mycoplasma. However, such analyses of Gram-negative bacteria are lacking, despite their ribosomes being major antimicrobial drug targets. Here we compare two E. coli strains, a lab E. coli K-12 and human gut isolate E. coli ED1a, for which tetracycline exhibits bacteriostatic and bactericidal action, respectively. The in situ ribosome structures upon tetracycline treatment show a virtually identical drug binding-site in both strains, yet the distribution of ribosomal complexes clearly differs. While K-12 retains ribosomes in a translation competent state, tRNAs are lost in the vast majority of ED1a ribosomes. A differential response is also reflected in proteome-wide abundance and thermal stability assessment. Our study underlines the need to include molecular analyses and to consider gut bacteria when addressing antibiotic mode of action.

Published
2023

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