DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: Transport capabilities of environmental Pseudomonads for sulfur compounds

Abstract

Sulfur is an essential element in plant rhizospheres and microbial activity plays a key role in increasing the biological availability of sulfur in soil environments. To better understand the mechanisms facilitating the exchange of sulfur-containing molecules in soil, we profiled the binding specificities of eight previously uncharacterized ABC transporter solute-binding proteins from plant-associated Pseudomonads. A high-throughput screening procedure indicated eighteen significant organosulfur binding ligands, with at least one high-quality screening hit for each protein target. Calorimetric and spectroscopic methods were used to validate the best ligand assignments and catalog the thermodynamic properties of the protein-ligand interactions. Two novel high-affinity ligand binding activities were identified and quantified in this set of solute binding proteins. Bacteria were cultured in minimal media with screening library components supplied as the sole sulfur sources, demonstrating that these organosulfur compounds can be metabolized and confirming the relevance of ligand assignments. These results expand the set of experimentally validated ligands amenable to transport by this ABC transporter family and demonstrate the complex range of protein-ligand interactions that can be accomplished by solute-binding proteins. As a result, characterizing new nutrient import pathways provides insight into Pseudomonad metabolic capabilities which can be used to further interrogate bacterial survival andmore » participation in soil and rhizosphere communities.« less

Authors:
 [1];  [1];  [1];  [1]
  1. Argonne National Lab. (ANL), Lemont, IL (United States)
Publication Date:
Research Org.:
Argonne National Lab. (ANL), Argonne, IL (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER)
OSTI Identifier:
1371913
Alternate Identifier(s):
OSTI ID: 1401894
Grant/Contract Number:  
AC02-06CH11357
Resource Type:
Accepted Manuscript
Journal Name:
Protein Science
Additional Journal Information:
Journal Volume: 26; Journal Issue: 4; Journal ID: ISSN 0961-8368
Publisher:
The Protein Society
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; 60 APPLIED LIFE SCIENCES; ABC transporter; Pseudomonas fluorescens; Pseudomonas protegens; organosulfur compounds; rhizosphere

Citation Formats

Zerbs, Sarah, Korajczyk, Peter J., Noirot, Philippe H., and Collart, Frank R. Transport capabilities of environmental Pseudomonads for sulfur compounds. United States: N. p., 2017. Web. doi:10.1002/pro.3124.
Zerbs, Sarah, Korajczyk, Peter J., Noirot, Philippe H., & Collart, Frank R. Transport capabilities of environmental Pseudomonads for sulfur compounds. United States. https://doi.org/10.1002/pro.3124
Zerbs, Sarah, Korajczyk, Peter J., Noirot, Philippe H., and Collart, Frank R. Fri . "Transport capabilities of environmental Pseudomonads for sulfur compounds". United States. https://doi.org/10.1002/pro.3124. https://www.osti.gov/servlets/purl/1371913.
@article{osti_1371913,
title = {Transport capabilities of environmental Pseudomonads for sulfur compounds},
author = {Zerbs, Sarah and Korajczyk, Peter J. and Noirot, Philippe H. and Collart, Frank R.},
abstractNote = {Sulfur is an essential element in plant rhizospheres and microbial activity plays a key role in increasing the biological availability of sulfur in soil environments. To better understand the mechanisms facilitating the exchange of sulfur-containing molecules in soil, we profiled the binding specificities of eight previously uncharacterized ABC transporter solute-binding proteins from plant-associated Pseudomonads. A high-throughput screening procedure indicated eighteen significant organosulfur binding ligands, with at least one high-quality screening hit for each protein target. Calorimetric and spectroscopic methods were used to validate the best ligand assignments and catalog the thermodynamic properties of the protein-ligand interactions. Two novel high-affinity ligand binding activities were identified and quantified in this set of solute binding proteins. Bacteria were cultured in minimal media with screening library components supplied as the sole sulfur sources, demonstrating that these organosulfur compounds can be metabolized and confirming the relevance of ligand assignments. These results expand the set of experimentally validated ligands amenable to transport by this ABC transporter family and demonstrate the complex range of protein-ligand interactions that can be accomplished by solute-binding proteins. As a result, characterizing new nutrient import pathways provides insight into Pseudomonad metabolic capabilities which can be used to further interrogate bacterial survival and participation in soil and rhizosphere communities.},
doi = {10.1002/pro.3124},
journal = {Protein Science},
number = 4,
volume = 26,
place = {United States},
year = {2017},
month = {1}
}

Works referenced in this record:

Complete genome sequence of the plant commensal Pseudomonas fluorescens Pf-5
journal, June 2005

  • Paulsen, Ian T.; Press, Caroline M.; Ravel, Jacques
  • Nature Biotechnology, Vol. 23, Issue 7
  • DOI: 10.1038/nbt1110

Characterization of Transport Proteins for Aromatic Compounds Derived from Lignin: Benzoate Derivative Binding Proteins
journal, November 2012

  • Michalska, Karolina; Chang, Changsoo; Mack, Jamey C.
  • Journal of Molecular Biology, Vol. 423, Issue 4
  • DOI: 10.1016/j.jmb.2012.08.017

The biosynthetic pathway of new polyamines in Caldariella acidophila
journal, October 1978

  • De Rosa, Mario; De Rosa, Salvatore; Gambacorta, Agata
  • Biochemical Journal, Vol. 176, Issue 1
  • DOI: 10.1042/bj1760001

Seasonal fluctuation of organic and inorganic components in xylem sap of Populus nigra
journal, January 2011


TcyR regulates l-cystine uptake via the TcyABC transporter in Streptococcus mutans
journal, January 2012


High-Density Miniaturized Thermal Shift Assays as a General Strategy for Drug Discovery
journal, December 2001

  • Pantoliano, M. W.; Petrella, E. C.; Kwasnoski, J. D.
  • Journal of Biomolecular Screening, Vol. 6, Issue 6
  • DOI: 10.1177/108705710100600609

Locating proteins in the cell using TargetP, SignalP and related tools
journal, April 2007

  • Emanuelsson, Olof; Brunak, Søren; von Heijne, Gunnar
  • Nature Protocols, Vol. 2, Issue 4
  • DOI: 10.1038/nprot.2007.131

Impact of protein and ligand impurities on ITC-derived protein–ligand thermodynamics
journal, September 2014

  • Grüner, Stefan; Neeb, Manuel; Barandun, Luzi Jakob
  • Biochimica et Biophysica Acta (BBA) - General Subjects, Vol. 1840, Issue 9
  • DOI: 10.1016/j.bbagen.2014.04.018

The High-Affinity E. coli Methionine ABC Transporter: Structure and Allosteric Regulation
journal, July 2008


Functional Assignment of Solute-Binding Proteins of ABC Transporters Using a Fluorescence-Based Thermal Shift Assay
journal, December 2008

  • Giuliani, Sarah E.; Frank, Ashley M.; Collart, Frank R.
  • Biochemistry, Vol. 47, Issue 52
  • DOI: 10.1021/bi801648r

The Phyre2 web portal for protein modeling, prediction and analysis
journal, May 2015

  • Kelley, Lawrence A.; Mezulis, Stefans; Yates, Christopher M.
  • Nature Protocols, Vol. 10, Issue 6
  • DOI: 10.1038/nprot.2015.053

SignalP 4.0: discriminating signal peptides from transmembrane regions
journal, September 2011

  • Petersen, Thomas Nordahl; Brunak, Søren; von Heijne, Gunnar
  • Nature Methods, Vol. 8, Issue 10
  • DOI: 10.1038/nmeth.1701

TransportDB: a comprehensive database resource for cytoplasmic membrane transport systems and outer membrane channels
journal, January 2007

  • Ren, Q.; Chen, K.; Paulsen, I. T.
  • Nucleic Acids Research, Vol. 35, Issue Database
  • DOI: 10.1093/nar/gkl925

The Escherichia coli ssuEADCB Gene Cluster Is Required for the Utilization of Sulfur from Aliphatic Sulfonates and Is Regulated by the Transcriptional Activator Cbl
journal, October 1999

  • van der Ploeg, Jan R.; Iwanicka-Nowicka, Roksana; Bykowski, Tomasz
  • Journal of Biological Chemistry, Vol. 274, Issue 41
  • DOI: 10.1074/jbc.274.41.29358

A structural classification of substrate-binding proteins
journal, April 2010


Distribution of Free Seleno-amino Acids in Plant Tissue ofMelilotus indicaL. Grown in Selenium-Laden Soils
journal, March 1998


Analysis of the multi-copied genes and the impact of the redundant protein coding sequences on gene annotation in prokaryotic genomes
journal, July 2015


PredictProtein—an open resource for online prediction of protein structural and functional features
journal, May 2014

  • Yachdav, Guy; Kloppmann, Edda; Kajan, Laszlo
  • Nucleic Acids Research, Vol. 42, Issue W1
  • DOI: 10.1093/nar/gku366

Evaluation of fluorescence-based thermal shift assays for hit identification in drug discovery
journal, September 2004


The yliA, -B, -C, and -D Genes of Escherichia coli K-12 Encode a Novel Glutathione Importer with an ATP-Binding Cassette
journal, August 2005


Quantifying environmental adaptation of metabolic pathways in metagenomics
journal, January 2009

  • Gianoulis, T. A.; Raes, J.; Patel, P. V.
  • Proceedings of the National Academy of Sciences, Vol. 106, Issue 5
  • DOI: 10.1073/pnas.0808022106

Three Different Systems Participate in L-Cystine Uptake in Bacillus subtilis
journal, July 2004


Composition of hydrolysable amino acids in soil organic matter and soil microbial biomass
journal, March 2002


How are signals transduced across the cytoplasmic membrane? Transport proteins as transmitter of information
journal, February 2009


CDD: NCBI's conserved domain database
journal, November 2014

  • Marchler-Bauer, Aron; Derbyshire, Myra K.; Gonzales, Noreen R.
  • Nucleic Acids Research, Vol. 43, Issue D1
  • DOI: 10.1093/nar/gku1221

Characterization of a toxin produced by a rhizobacterialPseudomonas sp. that inhibits wheat growth
journal, February 1989

  • Bolton, H.; Elliott, L. F.; Gurusiddaiah, S.
  • Plant and Soil, Vol. 114, Issue 2
  • DOI: 10.1007/BF02220808

Rerouting Citrate Metabolism in Lactococcus lactis to Citrate-Driven Transamination
journal, July 2012

  • Pudlik, Agata M.; Lolkema, Juke S.
  • Applied and Environmental Microbiology, Vol. 78, Issue 18
  • DOI: 10.1128/AEM.01811-12

ATP-binding Cassette (ABC) Transport System Solute-binding Protein-guided Identification of Novel d-Altritol and Galactitol Catabolic Pathways in Agrobacterium tumefaciens C58
journal, October 2015

  • Wichelecki, Daniel J.; Vetting, Matthew W.; Chou, Liyushang
  • Journal of Biological Chemistry, Vol. 290, Issue 48
  • DOI: 10.1074/jbc.M115.686857

Polyamines: ubiquitous polycations with unique roles in growth and stress responses
journal, October 2009

  • Takahashi, Taku; Kakehi, Jun-Ichi
  • Annals of Botany, Vol. 105, Issue 1
  • DOI: 10.1093/aob/mcp259

The regulatory interplay between membrane-integrated sensors and transport proteins in bacteria
journal, September 2009


Environment sensing and response mediated by ABC transporters
journal, January 2011

  • Giuliani, Sarah E.; Frank, Ashley M.; Corgliano, Danielle M.
  • BMC Genomics, Vol. 12, Issue Suppl 1
  • DOI: 10.1186/1471-2164-12-S1-S8

Enhanced annotations and features for comparing thousands of Pseudomonas genomes in the Pseudomonas genome database
journal, November 2015

  • Winsor, Geoffrey L.; Griffiths, Emma J.; Lo, Raymond
  • Nucleic Acids Research, Vol. 44, Issue D1
  • DOI: 10.1093/nar/gkv1227

Diversity of Pseudomonas Genomes, Including Populus-Associated Isolates, as Revealed by Comparative Genome Analysis
journal, October 2015

  • Jun, Se-Ran; Wassenaar, Trudy M.; Nookaew, Intawat
  • Applied and Environmental Microbiology, Vol. 82, Issue 1
  • DOI: 10.1128/AEM.02612-15

A transporter of Escherichia coli specific for l- and d-methionine is the prototype for a new family within the ABC superfamily
journal, August 2003

  • Zhang, Zhongge; Feige, J�r�me N.; Chang, Abraham B.
  • Archives of Microbiology, Vol. 180, Issue 2
  • DOI: 10.1007/s00203-003-0561-4

A Guide to Simple and Informative Binding Assays
journal, December 2010


Resolving the Ortholog Conjecture: Orthologs Tend to Be Weakly, but Significantly, More Similar in Function than Paralogs
journal, May 2012

  • Altenhoff, Adrian M.; Studer, Romain A.; Robinson-Rechavi, Marc
  • PLoS Computational Biology, Vol. 8, Issue 5
  • DOI: 10.1371/journal.pcbi.1002514

Paralogous metabolism: S-alkyl-cysteine degradation in Bacillus subtilis : Recovery of reduced sulphur using oxygen
journal, August 2013

  • Chan, Che-Man; Danchin, Antoine; Marlière, Philippe
  • Environmental Microbiology, Vol. 16, Issue 1
  • DOI: 10.1111/1462-2920.12210

Predicting transmembrane protein topology with a hidden markov model: application to complete genomes11Edited by F. Cohen
journal, January 2001

  • Krogh, Anders; Larsson, Björn; von Heijne, Gunnar
  • Journal of Molecular Biology, Vol. 305, Issue 3
  • DOI: 10.1006/jmbi.2000.4315

Basic local alignment search tool
journal, October 1990

  • Altschul, Stephen F.; Gish, Warren; Miller, Webb
  • Journal of Molecular Biology, Vol. 215, Issue 3, p. 403-410
  • DOI: 10.1016/S0022-2836(05)80360-2

Transport functions dominate the SAR11 metaproteome at low-nutrient extremes in the Sargasso Sea
journal, September 2008

  • Sowell, Sarah M.; Wilhelm, Larry J.; Norbeck, Angela D.
  • The ISME Journal, Vol. 3, Issue 1
  • DOI: 10.1038/ismej.2008.83

Stabilization of Proteins by Ligand Binding:  Application to Drug Screening and Determination of Unfolding Energetics
journal, May 2003

  • Waldron, Travis T.; Murphy, Kenneth P.
  • Biochemistry, Vol. 42, Issue 17
  • DOI: 10.1021/bi034212v

The Sulfur-Regulated Arylsulfatase Gene Cluster of Pseudomonas aeruginosa, a New Member of the cys Regulon
journal, April 2000


Genomic and genetic analyses of diversity and plant interactions of Pseudomonas fluorescens
journal, January 2009

  • Silby, Mark W.; Cerdeño-Tárraga, Ana M.; Vernikos, Georgios S.
  • Genome Biology, Vol. 10, Issue 5
  • DOI: 10.1186/gb-2009-10-5-r51

Amino acids in the rhizosphere: From plants to microbes
journal, September 2013


A large-scale evaluation of computational protein function prediction
journal, January 2013

  • Radivojac, Predrag; Clark, Wyatt T.; Oron, Tal Ronnen
  • Nature Methods, Vol. 10, Issue 3
  • DOI: 10.1038/nmeth.2340

Polyamines: molecules with regulatory functions in plant abiotic stress tolerance
journal, March 2010


Bacterial transporters for sulfate and organosulfur compounds
journal, April 2001


The contribution of methionine to the stability of the Escherichia coli MetNIQ ABC transporter-substrate binding protein complex
journal, September 2015

  • Nguyen, Phong T.; Li, Qi Wen; Kadaba, Neena S.
  • Biological Chemistry, Vol. 396, Issue 9-10
  • DOI: 10.1515/hsz-2015-0131

Annotation Error in Public Databases: Misannotation of Molecular Function in Enzyme Superfamilies
journal, December 2009


Streptomyces L-methionine decarboxylase: purification and properties of the enzyme and stereochemical course of substrate decarboxylation
journal, August 1990

  • Stevenson, David E.; Akhtar, Mahmoud; Gani, David
  • Biochemistry, Vol. 29, Issue 33
  • DOI: 10.1021/bi00485a015