Increased Thermal and Osmotic Stress Resistance in Listeria monocytogenes 568 Grown in the Presence of Trehalose Due to Inactivation of the Phosphotrehalase-Encoding Gene treA

Timothy C. Ells, Lisbeth Truelstrup Hansen

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Abstract

The food-borne pathogen Listeria monocytogenes is a problem for food processors and consumers alike, as the organism is resistant to harsh environmental conditions and inimical barriers implemented to prevent the survival and/or growth of harmful bacteria. One mechanism by which listeriae mediate survival is through the accumulation of compatible solutes, such as proline, betaine and carnitine. In other bacteria, including Escherichia coli, the synthesis and accumulation of another compatible solute, trehalose, are known to aid in the survival of stressed cells. The objective of this research was to investigate trehalose metabolism in L. monocytogenes, where the sugar is thought to be transferred across the cytoplasmic membrane via a specific phosphoenolpyruvate phosphotransferase system and phosphorylation to trehalose-6-phosphate (T6P). The latter is subsequently broken down into glucose and glucose-6-phosphate by alpha,alpha-(1,1) phosphotrehalase, the putative product of the treA gene. Here we report on an isogenic treA mutant of L. monocytogenes 568 (568:Delta TreA) which, relative to the wild-type strain, displays increased tolerances to multiple stressors, including heat, high osmolarity, and desiccation. This is the first study to examine the putative trehalose operon in L. monocytogenes, and we demonstrate that lmo1254 (treA) in L. monocytogenes 568 indeed encodes a phosphotrehalase required for the hydrolysis of T6P. Disruption of the treA gene results in the accumulation of T6P which is subsequently dephosphorylated to trehalose in the cytosol, thereby contributing to the stress hardiness observed in the treA mutant. This study highlights the importance of compatible solutes for microbial survival in adverse environments.
Original languageEnglish
JournalAPPLIED AND ENVIRONMENTAL MICROBIOLOGY
Volume77
Issue number19
Pages (from-to)6841-6851
Number of pages1
ISSN0099-2240
DOIs
Publication statusPublished - 2011
Externally publishedYes

Keywords

  • Applied Microbiology and Biotechnology
  • Food Science
  • Biotechnology
  • Ecology
  • Adverse environment
  • Broken down
  • Carnitine
  • Compatible solutes
  • Cytoplasmic membrane
  • Cytosols
  • Environmental conditions
  • Food processors
  • Food-borne pathogens
  • Glucose 6 phosphates
  • Listeria monocytogenes
  • Microbial survival
  • Monocytogenes
  • Multiple stressors
  • Osmolarity
  • Osmotic stress
  • Phosphoenolpyruvates
  • Phosphotransferase system
  • Trehalose metabolism
  • Wild-type strain
  • Amino acids
  • Cell membranes
  • Encoding (symbols)
  • Escherichia coli
  • Gene encoding
  • Glucose
  • Pathogens
  • Phosphorylation
  • Listeria
  • alpha, alpha phosphotrehalase
  • alpha, alpha-phosphotrehalase
  • disaccharidase
  • drug derivative
  • sugar phosphate
  • trehalose
  • trehalose 6 phosphate
  • trehalose-6-phosphate
  • acclimation
  • bacterium
  • biotechnology
  • desiccation
  • disaccharide
  • environmental conditions
  • environmental stress
  • enzyme activity
  • gene expression
  • hydrolysis
  • metabolism
  • mutation
  • osmosis
  • pathogen
  • solute
  • survival
  • tolerance
  • article
  • drug effect
  • gene deletion
  • genetics
  • heat
  • microbial viability
  • osmotic pressure
  • physiological stress
  • physiology
  • radiation exposure
  • Desiccation
  • Disaccharidases
  • Gene Deletion
  • Hot Temperature
  • Microbial Viability
  • Osmotic Pressure
  • Stress, Physiological
  • Sugar Phosphates
  • Trehalose
  • 4484-88-2 trehalose-6-phosphate
  • B8WCK70T7I Trehalose
  • EC 3.2.1.- Disaccharidases
  • EC 3.2.1.93 alpha, alpha-phosphotrehalase
  • BIOTECHNOLOGY
  • MICROBIOLOGY
  • ESCHERICHIA-COLI
  • SACCHAROMYCES-CEREVISIAE
  • BACILLUS-SUBTILIS
  • STREPTOCOCCUS-FAECALIS
  • DESICCATION TOLERANCE
  • LOW-TEMPERATURES
  • ACCUMULATION
  • PROTEINS
  • TREHALOSE-6-PHOSPHATE
  • THERMOTOLERANCE
  • LISTERIA monocytogenes
  • adverse environment
  • environmental condition
  • osmotic stress resistance
  • stress hardiness
  • thermal stress resistance
  • Eubacteria Bacteria Microorganisms (Bacteria, Eubacteria, Microorganisms) - Regular Nonsporing Gram-Positive Rods [07830] Listeria monocytogenes species pathogen strain-568, strain-32F11
  • Facultatively Anaerobic Gram-Negative Rods Eubacteria Bacteria Microorganisms (Bacteria, Eubacteria, Microorganisms) - Enterobacteriaceae [06702] Escherichia coli species strain-DH5-alpha
  • Listeria monocytogenes treA gene [Regular Nonsporing Gram-Positive Rods]
  • betaine 107-43-7
  • carnitine 541-15-1
  • glucose 58367-01-4
  • glucose-6-phosphate 56-73-5
  • phosphoenolpyruvate phosphotransferase
  • phosphotrehalase 54576-93-1 EC 3.2.1.93
  • trehalose 99-20-7 metabolism
  • trehalose-6-phosphate 4484-88-2 phosphorylation
  • 03502, Genetics - General
  • 10060, Biochemistry studies - General
  • 10068, Biochemistry studies - Carbohydrates
  • 10802, Enzymes - General and comparative studies: coenzymes
  • 12002, Physiology - General
  • 31000, Physiology and biochemistry of bacteria
  • 31500, Genetics of bacteria and viruses
  • Biochemistry and Molecular Biophysics
  • cytoplasmic membrane
  • cytosol
  • Chemical Coordination and Homeostasis
  • Enzymology
  • Molecular Genetics
  • FOOD SAFETY
  • HEAT RESISTANCE
  • LISTERIA
  • LISTERIA MONOCYTOGENES
  • MUTANTS
  • MUTATIONS
  • OSMOTIC STRESS
  • PHYSIOLOGY
  • STRESS
  • STRESS RESISTANCE
  • THERMOPHYSICAL PROPERTIES
  • Hygiene and toxicology
  • Microbiological aspects

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