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

Title: Integrated Proteomics and Lipidomics Reveal That the Swarming Motility of Paenibacillus polymyxa Is Characterized by Phospholipid Modification, Surfactant Deployment, and Flagellar Specialization Relative to Swimming Motility

Journal Article · · Frontiers in Microbiology

Paenibacillus polymyxa is a Gram-positive bacterium commonly found associated with plant roots. P. polymyxa can exhibit two forms of flagellar motility: swimming in liquid culture and swarming on a surface. Here, swimming cells were compared to swarming cells using an integrated proteomic and lipidomic approach, yielding information about how lipid modifications and protein/enzyme pathways are tailored for these specific phenotypes. Observed differences in both phospholipid composition and metabolism between the two conditions suggest membrane remodeling in response to the surrounding environment. Key enzymes involved in glycerophospholipid metabolism were abundant in swimming bacteria, while enzymes associated with glycerol-3-phosphate metabolism were more abundant in swarming bacteria. Several glycoside hydrolases were either unique to or more abundant during swarming. This likely reflects the degradation of their own exopolysaccharides to both enhance swarming and supply the necessary chemical energy to compensate for increased flagellar synthesis. The observed upregulation of biosynthetic gene clusters (polyketides, lantibiotics, and surfactin) in swarming bacteria suggest the importance of signaling, antimicrobial activity, and surfactin production during this mode of motility – the latter of which is confirmed via RT-PCR.

Sponsoring Organization:
USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23)
Grant/Contract Number:
AC05-00OR22725
OSTI ID:
1574543
Journal Information:
Frontiers in Microbiology, Journal Name: Frontiers in Microbiology Vol. 10; ISSN 1664-302X
Publisher:
Frontiers Research FoundationCopyright Statement
Country of Publication:
Switzerland
Language:
English

References (78)

Mutations in genes encoding antibiotic substances increase the synthesis of poly-γ-glutamic acid in Bacillus amyloliquefaciens LL3 journal August 2016
The lipopeptides mycosubtilin and surfactin enhance spreading of Bacillus subtilis strains by their surface-active properties journal September 2006
Biofilm Formation by Paenibacillus polymyxa Strains Differing in the Production and Rheological Properties of Their Exopolysaccharides journal February 2011
Paenibacillus polymyxa Rhizobacteria and Their Synthesized Exoglycans in Interaction with Wheat Roots: Colonization and Root Hair Deformation journal January 2013
A locus coding for putative non-ribosomal peptide/polyketide synthase functions is mutated in a swarming-defective Proteus mirabilis strain journal January 1997
Ecology and biotechnological potential of Paenibacillus polymyxa: a minireview journal March 2009
Surfactin, a crystalline peptidelipid surfactant produced by Bacillussubtilis: Isolation, characterization and its inhibition of fibrin clot formation journal May 1968
Periplasmic glycerophosphodiester phosphodiesterase of Escherichia coli, a new enzyme of the glp regulon. journal May 1983
Comparison of three directly coupled HPLC MS/MS strategies for identification of proteins from complex mixtures: single-dimension LC-MS/MS, 2-phase MudPIT, and 3-phase MudPIT journal August 2002
Surfactin production enhances the level of cardiolipin in the cytoplasmic membrane of Bacillus subtilis journal November 2013
Molecular mechanisms of membrane targeting antibiotics journal May 2016
Identification and functional analysis of the fusaricidin biosynthetic gene of Paenibacillus polymyxa E681 journal January 2008
Swarming motility plays the major role in migration during tomato root colonization by Bacillus subtilis SWR01 journal July 2016
Production, characterization and antioxidant activities in vitro of exopolysaccharides from endophytic bacterium Paenibacillus polymyxa EJS-3 journal September 2009
In vitro and in vivo antioxidant activity of exopolysaccharides from endophytic bacterium Paenibacillus polymyxa EJS-3 journal November 2010
Nonribosomal Biosynthesis of Fusaricidins by Paenibacillus polymyxa PKB1 Involves Direct Activation of a d-Amino Acid journal February 2008
Genome sequence of type strain Paenibacillus polymyxa DSM 365, a highly efficient producer of optically active (R,R)-2,3-butanediol journal February 2015
BlastKOALA and GhostKOALA: KEGG Tools for Functional Characterization of Genome and Metagenome Sequences journal February 2016
Living on a surface: swarming and biofilm formation journal October 2008
Lipidomics: An analysis of cellular lipids by ESI-MS journal June 2006
Metabolomic Analysis and Visualization Engine for LC−MS Data journal December 2010
Spontaneous Curvature of Phosphatidic Acid and Lysophosphatidic Acid journal February 2005
Faster SEQUEST Searching for Peptide Identification from Tandem Mass Spectra journal September 2011
Modulation of Membrane Curvature by Phosphatidic Acid and Lysophosphatidic Acid: Biophysical Properties of Phosphatidic Acid and Lysophosphatidic Acid journal March 2003
Large-scale analysis of the yeast proteome by multidimensional protein identification technology journal March 2001
moFF: a robust and automated approach to extract peptide ion intensities journal November 2016
Semi-supervised learning for peptide identification from shotgun proteomics datasets journal October 2007
Membrane lipid homeostasis in bacteria journal March 2008
A field guide to bacterial swarming motility journal August 2010
Bacterial swarming: a model system for studying dynamic self-assembly journal January 2009
A phosphatidic acid-binding protein is important for lipid homeostasis and adaptation to anaerobic biofilm conditions in Pseudomonas aeruginosa journal June 2018
Swarming motility in undomesticated Bacillus subtilis: B. subtilis swarming motility journal August 2003
A four-tiered transcriptional regulatory circuit controls flagellar biogenesis in Pseudomonas aeruginosa: Transcriptional regulation of flagellar biogenesis journal September 2003
Adaptor-mediated Lon proteolysis restricts Bacillus subtilis hyperflagellation journal December 2014
Microbial glycoside hydrolases as antibiofilm agents with cross-kingdom activity journal June 2017
ClueGO: a Cytoscape plug-in to decipher functionally grouped gene ontology and pathway annotation networks journal February 2009
Prokka: rapid prokaryotic genome annotation journal March 2014
CAZymes Analysis Toolkit (CAT): Web service for searching and analyzing carbohydrate-active enzymes in a newly sequenced organism using CAZy database journal August 2010
Fast Genome-Wide Functional Annotation through Orthology Assignment by eggNOG-Mapper journal April 2017
KEGG: Kyoto Encyclopedia of Genes and Genomes journal January 2000
KEGG for integration and interpretation of large-scale molecular data sets journal November 2011
Paenibacillus chartarius sp. nov., isolated from a paper mill journal August 2011
Identification and characterization of a highly motile and antibiotic refractory subpopulation involved in the expansion of swarming colonies of Paenibacillus vortex : Highly motile subpopulation of journal June 2013
Isolation and identification of nitrogen-fixing bacilli from plant rhizospheres in Beijing region journal November 2005
Genes governing swarming in Bacillus subtilis and evidence for a phase variation mechanism controlling surface motility: Genetic analysis of B. subtilis swarming journal March 2004
Bacillus subtilis antibiotics: structures, syntheses and specific functions: Bacillus subtilis antibiotics journal March 2005
Broad-spectrum antimicrobial peptide resistance by MprF-mediated aminoacylation and flipping of phospholipids: MprF-mediated antimicrobial peptide resistance journal March 2011
Citrinin, a mycotoxin from Penicillium citrinum, plays a role in inducing motility of Paenibacillus polymyxa: Induction of bacterial motility by citrinin journal August 2008
Two noncellulosomal cellulases of Clostridium thermocellum, Cel9I and Cel48Y, hydrolyse crystalline cellulose synergistically: Clostridium thermocellum soluble synergistic cellulases journal January 2007
A mechanical signal transmitted by the flagellum controls signalling in Bacillus subtilis : Flagella-mediated signal transduction journal August 2013
Exopolysaccharide biosynthetic glycoside hydrolases can be utilized to disrupt and prevent Pseudomonas aeruginosa biofilms journal May 2016
Exopolysaccharide production in biofilms: substratum activation of alginate gene expression by Pseudomonas aeruginosa journal April 1993
Paenibacillus polymyxa Invades Plant Roots and Forms Biofilms journal November 2005
Ultrastructure of Proteus mirabilis Swarmer Cell Rafts and Role of Swarming in Catheter-Associated Urinary Tract Infection journal June 2004
A Novel Gene Inactivation System Reveals Altered Periplasmic Flagellar Orientation in a Borrelia burgdorferi fliL Mutant journal March 2011
SwrD (YlzI) Promotes Swarming in Bacillus subtilis by Increasing Power to Flagellar Motors journal October 2017
SadC Reciprocally Influences Biofilm Formation and Swarming Motility via Modulation of Exopolysaccharide Production and Flagellar Function journal June 2007
Draft Genome Sequence of Paenibacillus polymyxa OSY-DF, Which Coproduces a Lantibiotic, Paenibacillin, and Polymyxin E1 journal August 2012
Genome Sequence of the Polymyxin-Producing Plant-Probiotic Rhizobacterium Paenibacillus polymyxa E681 journal September 2010
Complete Genome Sequence of Paenibacillus polymyxa SC2, a Strain of Plant Growth-Promoting Rhizobacterium with Broad-Spectrum Antimicrobial Activity journal October 2010
Exopolysaccharides Produced by Streptococcus mutans Glucosyltransferases Modulate the Establishment of Microcolonies within Multispecies Biofilms journal March 2010
Draft Genome Sequence of the Paenibacillus polymyxa Type Strain (ATCC 842T), a Plant Growth-Promoting Bacterium journal July 2011
The Genome of the Plant Growth-Promoting Rhizobacterium Paenibacillus polymyxa M-1 Contains Nine Sites Dedicated to Nonribosomal Synthesis of Lipopeptides and Polyketides journal September 2011
N -Acyl- l -Homoserine Lactone Autoinducers Control Production of an Extracellular Lipopeptide Biosurfactant Required for Swarming Motility of Serratia liquefaciens MG1 journal December 1998
Exopolysaccharide Production Is Required for Development of Escherichia coli K-12 Biofilm Architecture journal June 2000
Extracellular Proteolytic Activity Plays a Central Role in Swarming Motility in Bacillus subtilis journal June 2004
Comparative Analysis of the Development of Swarming Communities of Bacillus subtilis 168 and a Natural Wild Type: Critical Effects of Surfactin and the Composition of the Medium journal December 2004
Swarming Differentiation and Swimming Motility in Bacillus subtilis Are Controlled by swrA, a Newly Identified Dicistronic Operon journal July 2005
Nucleotide sequence of the hag gene encoding flagellin of Escherichia coli. journal December 1986
A novel extracellular cyclic lipopeptide which promotes flagellum-dependent and -independent spreading growth of Serratia marcescens. journal March 1992
Synthesis of sn-glycerol 3-phosphate, a key precursor of membrane lipids, in Bacillus subtilis. journal October 1995
In Vivo Behavior of the Tandem Glycine Riboswitch in Bacillus subtilis journal October 2017
Morphological Changes in Growth Phenomena of Bacterial Colony Patterns journal March 1992
Experimental Investigation on the Formation of Dense-Branching-Morphology-Like Colonies in Bacteria journal October 1998
Bacterial Motility on a Surface: Many Ways to a Common Goal journal October 2003
A Simplified Method for Gene Knockout and Direct Screening of Recombinant Clones for Application in Paenibacillus polymyxa journal June 2013
Regulation of Motility and Phenazine Pigment Production by FliA Is Cyclic-di-GMP Dependent in Pseudomonas aeruginosa PAO1 journal May 2016
LysPGS formation in Listeria monocytogenes has broad roles in maintaining membrane integrity beyond antimicrobial peptide resistance journal March 2014