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An integrated model system to gain mechanistic insights into biofilm formation and antimicrobial resistance development in Pseudomonas aeruginosa MPAO1

View ORCID ProfileAdithi R. Varadarajan, Raymond N. Allan, Jules D. P. Valentin, Olga E. Castañeda Ocampo, Vincent Somerville, Franziska Pietsch, Matthias T. Buhmann, Jonathan West, Paul J. Skipp, Henny C. van der Mei, Qun Ren, Frank Schreiber, Jeremy S. Webb, View ORCID ProfileChristian H. Ahrens
doi: https://doi.org/10.1101/2020.02.06.936690
Adithi R. Varadarajan
1Agroscope, Research Group Molecular Diagnostics, Genomics & Bioinformatics and SIB Swiss Institute of Bioinformatics, CH-8820 Wädenswil, Switzerland
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  • ORCID record for Adithi R. Varadarajan
  • For correspondence: adithi.varadarajan@agroscope.admin.ch christian.ahrens@agroscope.admin.ch
Raymond N. Allan
2School of Biological Sciences, Faculty of Environmental & Life Sciences, University of Southampton, Southampton, SO17 1BJ, UK
3National Biofilms Innovation Centre, University of Southampton, Southampton, SO17 1BJ, UK
4School of Pharmacy, Faculty of Health and Life Sciences, De Montfort University, Leicester, LE1 9BH, UK
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Jules D. P. Valentin
5Laboratory for Biointerfaces, Empa, Swiss Federal Laboratories for Materials Science and Technology, St. Gallen, Switzerland
6University of Groningen and University Medical Center Groningen, Department of BioMedical Engineering, Groningen, Netherlands
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Olga E. Castañeda Ocampo
6University of Groningen and University Medical Center Groningen, Department of BioMedical Engineering, Groningen, Netherlands
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Vincent Somerville
1Agroscope, Research Group Molecular Diagnostics, Genomics & Bioinformatics and SIB Swiss Institute of Bioinformatics, CH-8820 Wädenswil, Switzerland
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Franziska Pietsch
7Federal Institute for Materials Research and Testing (BAM), Division of Biodeterioration and Reference Organisms, Berlin, Germany
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Matthias T. Buhmann
5Laboratory for Biointerfaces, Empa, Swiss Federal Laboratories for Materials Science and Technology, St. Gallen, Switzerland
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Jonathan West
8Faculty of Medicine, University of Southampton, Southampton, SO17 1BJ, UK
9Centre for Hybrid Biodevices, University of Southampton, Southampton, SO17 1BJ, UK
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Paul J. Skipp
10Centre for Proteomics Research, University of Southampton, Southampton, SO17 1BJ, UK
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Henny C. van der Mei
6University of Groningen and University Medical Center Groningen, Department of BioMedical Engineering, Groningen, Netherlands
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Qun Ren
5Laboratory for Biointerfaces, Empa, Swiss Federal Laboratories for Materials Science and Technology, St. Gallen, Switzerland
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Frank Schreiber
7Federal Institute for Materials Research and Testing (BAM), Division of Biodeterioration and Reference Organisms, Berlin, Germany
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Jeremy S. Webb
2School of Biological Sciences, Faculty of Environmental & Life Sciences, University of Southampton, Southampton, SO17 1BJ, UK
3National Biofilms Innovation Centre, University of Southampton, Southampton, SO17 1BJ, UK
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Christian H. Ahrens
1Agroscope, Research Group Molecular Diagnostics, Genomics & Bioinformatics and SIB Swiss Institute of Bioinformatics, CH-8820 Wädenswil, Switzerland
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  • ORCID record for Christian H. Ahrens
  • For correspondence: adithi.varadarajan@agroscope.admin.ch christian.ahrens@agroscope.admin.ch
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Abstract

Pseudomonas aeruginosa MPAO1 is the parental strain of the widely utilized transposon mutant collection for this important clinical pathogen. Here, we validate a model system to identify genes involved in biofilm growth and antibiotic resistance.

Our model employs a genomics-driven workflow to assemble the complete MPAO1 genome, identify unique and conserved genes by comparative genomics with the PAO1 reference strain and missed genes by proteogenomics. Among over 200 unique MPAO1 genes, we identified six general essential genes that were overlooked when mapping public Tn-seq datasets against PAO1, including an antitoxin. Genomic data were integrated with phenotypic data from an experimental workflow using a user-friendly, soft lithography-based microfluidic flow chamber for biofilm growth. Experiments conducted across three laboratories delivered reproducible data on P. aeruginosa biofilms and validated both known and novel genes involved in biofilm growth and antibiotic resistance identified in screens of the mutant collection. Differential protein expression data from planktonic cells versus biofilm confirmed upregulation of candidates known to affect biofilm formation, of structural and secreted proteins of type six secretion systems, and provided proteogenomic evidence for some missed MPAO1 genes. This integrated, broadly applicable model promises to improve the mechanistic understanding of biofilm formation, antimicrobial tolerance and resistance evolution.

Footnotes

  • ↵* shared first authorship

  • https://iptgxdb.expasy.org/database/

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An integrated model system to gain mechanistic insights into biofilm formation and antimicrobial resistance development in Pseudomonas aeruginosa MPAO1
Adithi R. Varadarajan, Raymond N. Allan, Jules D. P. Valentin, Olga E. Castañeda Ocampo, Vincent Somerville, Franziska Pietsch, Matthias T. Buhmann, Jonathan West, Paul J. Skipp, Henny C. van der Mei, Qun Ren, Frank Schreiber, Jeremy S. Webb, Christian H. Ahrens
bioRxiv 2020.02.06.936690; doi: https://doi.org/10.1101/2020.02.06.936690
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An integrated model system to gain mechanistic insights into biofilm formation and antimicrobial resistance development in Pseudomonas aeruginosa MPAO1
Adithi R. Varadarajan, Raymond N. Allan, Jules D. P. Valentin, Olga E. Castañeda Ocampo, Vincent Somerville, Franziska Pietsch, Matthias T. Buhmann, Jonathan West, Paul J. Skipp, Henny C. van der Mei, Qun Ren, Frank Schreiber, Jeremy S. Webb, Christian H. Ahrens
bioRxiv 2020.02.06.936690; doi: https://doi.org/10.1101/2020.02.06.936690

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