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Title: A High-Throughput Method for Identifying Novel Genes That Influence Metabolic Pathways Reveals New Iron and Heme Regulation in Pseudomonas aeruginosa

Abstract

Heme is an essential metabolite for most life on earth. Bacterial pathogens almost universally require iron to infect a host, often acquiring this nutrient in the form of heme. The Gram-negative pathogen Pseudomonas aeruginosa is no exception, where heme acquisition and metabolism are known to be crucial for both chronic and acute infections. To unveil unknown genes and pathways that could play a role with heme metabolic flux in this pathogen, we devised an omic-based approach we dubbed “Met-Seq,” for metabolite-coupled transposon sequencing. Met-Seq couples a biosensor with fluorescence-activated cell sorting (FACS) and massively parallel sequencing, allowing for direct identification of genes associated with metabolic changes. In this work, we first construct and validate a heme biosensor for use with P. aeruginosa and exploit Met-Seq to identify 188 genes that potentially influence intracellular heme levels. Identified genes largely consisted of metabolic pathways not previously associated with heme, including many secreted virulence effectors, as well as 11 predicted small RNAs (sRNAs) and riboswitches whose functions are not currently understood. We verify that five Met-Seq hits affect intracellular heme levels; a predicted extracytoplasmic function (ECF) factor, a phospholipid acquisition system, heme biosynthesis regulator Dnr, and two predicted antibiotic monooxygenase (ABM) domains ofmore » unknown function (PA0709 and PA3390). Finally, we demonstrate that PA0709 and PA3390 are novel heme-binding proteins. Our data suggest that Met-Seq could be extrapolated to other biological systems and metabolites for which there is an available biosensor, and provides a new template for further exploration of iron/heme regulation and metabolism in P. aeruginosa and other pathogens.« less

Authors:
 [1];  [2];  [1];  [3];  [3]; ORCiD logo [4]; ORCiD logo [1];
+ Show Author Affiliations
  1. Department of Microbiology and Immunology, Loyola University Chicago, Maywood, Illinois, USA
  2. MRC Centre for Molecular Bacteriology and Infection, Department of Medicine, Imperial College, London, United Kingdom
  3. Great Lakes Bioenergy Research Center, Wisconsin Energy Institute, University of Wisconsin, Madison, Wisconsin, USA
  4. Great Lakes Bioenergy Research Center, Wisconsin Energy Institute, University of Wisconsin, Madison, Wisconsin, USA, Department of Bacteriology, University of Wisconsin, Madison, Wisconsin, USA
Publication Date:
Research Org.:
Great Lakes Bioenergy Research Center (GLBRC), Madison, WI (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER); National Institutes of Health (NIH)
OSTI Identifier:
1784789
Alternate Identifier(s):
OSTI ID: 1776824
Grant/Contract Number:  
BER DE-SC0018409; SC0018409; R01AI135060
Resource Type:
Published Article
Journal Name:
mSystems
Additional Journal Information:
Journal Name: mSystems Journal Volume: 6 Journal Issue: 1; Journal ID: ISSN 2379-5077
Publisher:
American Society for Microbiology
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; Pseudomonas aeruginosa; Tn-seq; biosensor; heme; heme biosynthesis; heme transport; infection; iron; metabolism; transposon sequencing; FlowSeq; Met-Seq

Citation Formats

Glanville, David G., Mullineaux-Sanders, Caroline, Corcoran, Christopher J., Burger, Brian T., Imam, Saheed, Donohue, Timothy J., Ulijasz, Andrew T., and Traxler, ed., Matthew F. A High-Throughput Method for Identifying Novel Genes That Influence Metabolic Pathways Reveals New Iron and Heme Regulation in Pseudomonas aeruginosa. United States: N. p., 2021. Web. doi:10.1128/mSystems.00933-20.
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Glanville, David G., Mullineaux-Sanders, Caroline, Corcoran, Christopher J., Burger, Brian T., Imam, Saheed, Donohue, Timothy J., Ulijasz, Andrew T., & Traxler, ed., Matthew F. A High-Throughput Method for Identifying Novel Genes That Influence Metabolic Pathways Reveals New Iron and Heme Regulation in Pseudomonas aeruginosa. United States. https://doi.org/10.1128/mSystems.00933-20
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Glanville, David G., Mullineaux-Sanders, Caroline, Corcoran, Christopher J., Burger, Brian T., Imam, Saheed, Donohue, Timothy J., Ulijasz, Andrew T., and Traxler, ed., Matthew F. Tue . "A High-Throughput Method for Identifying Novel Genes That Influence Metabolic Pathways Reveals New Iron and Heme Regulation in Pseudomonas aeruginosa". United States. https://doi.org/10.1128/mSystems.00933-20.
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@article{osti_1784789,
title = {A High-Throughput Method for Identifying Novel Genes That Influence Metabolic Pathways Reveals New Iron and Heme Regulation in Pseudomonas aeruginosa},
author = {Glanville, David G. and Mullineaux-Sanders, Caroline and Corcoran, Christopher J. and Burger, Brian T. and Imam, Saheed and Donohue, Timothy J. and Ulijasz, Andrew T. and Traxler, ed., Matthew F.},
abstractNote = {Heme is an essential metabolite for most life on earth. Bacterial pathogens almost universally require iron to infect a host, often acquiring this nutrient in the form of heme. The Gram-negative pathogen Pseudomonas aeruginosa is no exception, where heme acquisition and metabolism are known to be crucial for both chronic and acute infections. To unveil unknown genes and pathways that could play a role with heme metabolic flux in this pathogen, we devised an omic-based approach we dubbed “Met-Seq,” for metabolite-coupled transposon sequencing. Met-Seq couples a biosensor with fluorescence-activated cell sorting (FACS) and massively parallel sequencing, allowing for direct identification of genes associated with metabolic changes. In this work, we first construct and validate a heme biosensor for use with P. aeruginosa and exploit Met-Seq to identify 188 genes that potentially influence intracellular heme levels. Identified genes largely consisted of metabolic pathways not previously associated with heme, including many secreted virulence effectors, as well as 11 predicted small RNAs (sRNAs) and riboswitches whose functions are not currently understood. We verify that five Met-Seq hits affect intracellular heme levels; a predicted extracytoplasmic function (ECF) factor, a phospholipid acquisition system, heme biosynthesis regulator Dnr, and two predicted antibiotic monooxygenase (ABM) domains of unknown function (PA0709 and PA3390). Finally, we demonstrate that PA0709 and PA3390 are novel heme-binding proteins. Our data suggest that Met-Seq could be extrapolated to other biological systems and metabolites for which there is an available biosensor, and provides a new template for further exploration of iron/heme regulation and metabolism in P. aeruginosa and other pathogens.},
doi = {10.1128/mSystems.00933-20},
journal = {mSystems},
number = 1,
volume = 6,
place = {United States},
year = {Tue Feb 23 00:00:00 EST 2021},
month = {Tue Feb 23 00:00:00 EST 2021}
}
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journal, August 2010

Solution Structure of a Cyanobacterial Phytochrome GAF Domain in the Red-Light-Absorbing Ground State
journal, November 2008

  • Cornilescu, Gabriel; Ulijasz, Andrew T.; Cornilescu, Claudia C.
  • Journal of Molecular Biology, Vol. 383, Issue 2
  • DOI: 10.1016/j.jmb.2008.08.034

Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources
journal, December 2008

  • Huang, Da Wei; Sherman, Brad T.; Lempicki, Richard A.
  • Nature Protocols, Vol. 4, Issue 1
  • DOI: 10.1038/nprot.2008.211

Photosensing and quorum sensing are integrated to control Pseudomonas aeruginosa collective behaviors
journal, December 2019

Spoils of war: iron at the crux of clinical and ecological fitness of Pseudomonas aeruginosa
journal, March 2015

Transport of 5-aminolevulinic acid by the dipeptide permease in Salmonella typhimurium.
journal, January 1993

The Fourth Arginine Catabolic Pathway of Pseudomonas aeruginosa
journal, April 1988

The P. aeruginosa Heme Binding Protein PhuS Is a Heme Oxygenase Titratable Regulator of Heme Uptake
journal, June 2013

  • O’Neill, Maura J.; Wilks, Angela
  • ACS Chemical Biology, Vol. 8, Issue 8
  • DOI: 10.1021/cb400165b

Protein and Nucleotide Damage by Glyoxal and Methylglyoxal in Physiological Systems - role in Ageing and Disease
journal, January 2008

The response of Pseudomonas aeruginosa to iron: genetics, biochemistry and virulence
journal, November 1999

Bacterial Responses to Glyoxal and Methylglyoxal: Reactive Electrophilic Species
journal, January 2017

  • Lee, Changhan; Park, Chankyu
  • International Journal of Molecular Sciences, Vol. 18, Issue 1
  • DOI: 10.3390/ijms18010169

A dual component heme biosensor that integrates heme transport and synthesis in bacteria
journal, November 2015

  • Nobles, Christopher L.; Clark, Justin R.; Green, Sabrina I.
  • Journal of Microbiological Methods, Vol. 118
  • DOI: 10.1016/j.mimet.2015.07.011

The Antibiotic Activity of N -Pentylpantothenamide Results from Its Conversion to Ethyldethia-Coenzyme A, a Coenzyme A Antimetabolite
journal, October 2002

  • Strauss, Erick; Begley, Tadhg P.
  • Journal of Biological Chemistry, Vol. 277, Issue 50
  • DOI: 10.1074/jbc.M204560200

Phenazine-1-Carboxylic Acid Promotes Bacterial Biofilm Development via Ferrous Iron Acquisition
journal, May 2011

  • Wang, Y.; Wilks, J. C.; Danhorn, T.
  • Journal of Bacteriology, Vol. 193, Issue 14
  • DOI: 10.1128/JB.00396-11

Identification of Two Gene Clusters and a Transcriptional Regulator Required for Pseudomonas aeruginosa Glycine Betaine Catabolism
journal, October 2007

  • Wargo, M. J.; Szwergold, B. S.; Hogan, D. A.
  • Journal of Bacteriology, Vol. 190, Issue 8
  • DOI: 10.1128/JB.01393-07

Bacterial phytochromes: More than meets the light
journal, January 2011

  • Auldridge, Michele E.; Forest, Katrina T.
  • Critical Reviews in Biochemistry and Molecular Biology, Vol. 46, Issue 1
  • DOI: 10.3109/10409238.2010.546389

From The Cover: A truncated aminoacyl-tRNA synthetase modifies RNA
journal, April 2004

  • Salazar, J. C.; Ambrogelly, A.; Crain, P. F.
  • Proceedings of the National Academy of Sciences, Vol. 101, Issue 20
  • DOI: 10.1073/pnas.0401982101

Isochorismate Synthase (PchA), the First and Rate-limiting Enzyme in Salicylate Biosynthesis of Pseudomonas aeruginosa
journal, May 2003

  • Gaille, Catherine; Reimmann, Cornelia; Haas, Dieter
  • Journal of Biological Chemistry, Vol. 278, Issue 19
  • DOI: 10.1074/jbc.M212324200

Cytoscape: A Software Environment for Integrated Models of Biomolecular Interaction Networks
journal, November 2003

Site-Selective Modifications of Arginine Residues in Human Hemoglobin Induced by Methylglyoxal
journal, December 2006

Proteomic analysis of outer membrane vesicles derived from Pseudomonas aeruginosa
journal, July 2011

The Role of the Cytoplasmic Heme-binding Protein (PhuS) of Pseudomonas aeruginosa in Intracellular Heme Trafficking and Iron Homeostasis
journal, November 2008

  • Kaur, Ajinder P.; Lansky, Ila B.; Wilks, Angela
  • Journal of Biological Chemistry, Vol. 284, Issue 1
  • DOI: 10.1074/jbc.M806068200

Sigma factors in Pseudomonas aeruginosa
journal, January 2008

Outer Membrane Vesicles (OMVs) of Gram-negative Bacteria: A Perspective Update
journal, June 2017

Transposon insertion sequencing: a new tool for systems-level analysis of microorganisms
journal, May 2013

  • van Opijnen, Tim; Camilli, Andrew
  • Nature Reviews Microbiology, Vol. 11, Issue 7
  • DOI: 10.1038/nrmicro3033

Regulation of Pseudomonas aeruginosa hemF and hemN by the dual action of the redox response regulators Anr and Dnr
journal, August 1998

Resources for Genetic and Genomic Analysis of Emerging Pathogen Acinetobacter baumannii
journal, April 2015

  • Gallagher, Larry A.; Ramage, Elizabeth; Weiss, Eli J.
  • Journal of Bacteriology, Vol. 197, Issue 12
  • DOI: 10.1128/JB.00131-15

Improving membrane protein expression and function using genomic edits
journal, October 2017

Assessing glycolytic flux alterations resulting from genetic perturbations in E. coli using a biosensor
journal, July 2017

A vancomycin-inducible lacZ reporter system in Bacillus subtilis: induction by antibiotics that inhibit cell wall synthesis and by lysozyme.
journal, November 1996

Molecular characterization of genes of Pseudomonas sp. strain HR199 involved in bioconversion of vanillin to protocatechuate.
journal, April 1997

mini-Tn7 insertion in bacteria with single attTn7 sites: example Pseudomonas aeruginosa
journal, June 2006

Heme Synthesis and Acquisition in Bacterial Pathogens
journal, August 2016

Tryptophan catabolism in Pseudomonas aeruginosa and potential for inter-kingdom relationship
journal, July 2016

  • Bortolotti, Perrine; Hennart, Benjamin; Thieffry, Camille
  • BMC Microbiology, Vol. 16, Issue 1
  • DOI: 10.1186/s12866-016-0756-x

Anr and Its Activation by PlcH Activity in Pseudomonas aeruginosa Host Colonization and Virulence
journal, May 2013

  • Jackson, A. A.; Gross, M. J.; Daniels, E. F.
  • Journal of Bacteriology, Vol. 195, Issue 13
  • DOI: 10.1128/JB.02169-12
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