Oxidative stress protection by polyphosphate—new roles for an old player

Gray, Michael J.; Jakob, Ursula

doi:10.1016/j.mib.2014.12.004

Cited by 146 publications

(142 citation statements)

References 43 publications

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“…Inorganic polyphosphate was also reported to play a key role in stress tolerance by acting as a protein-protecting chaperone and by regulating sigma factors involved in stress response in bacteria (52). Polyphosphate accumulation in the form of volutin granules has been evidenced in various Lactobacillus species (29), in Corynebacterium glutamicum (53), and in P. freudenreichii (54).…”

Section: Resultsmentioning

confidence: 99%

Hyperconcentrated Sweet Whey, a New Culture Medium That Enhances Propionibacterium freudenreichii Stress Tolerance

Song

Rabah

Jardin

et al. 2016

Appl Environ Microbiol

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Propionibacterium freudenreichii is used as a cheese-ripening starter and as a probiotic. Its reported physiological effects at the gut level, including modulation of bifidobacteria, colon epithelial cell proliferation and apoptosis, and intestinal inflammation, rely on active metabolism in situ. Survival and activity are thus key factors determining its efficacy, creating stress adaptation and tolerance bottlenecks for probiotic applications. Growth media and growth conditions determine tolerance acquisition. We investigated the possibility of using sweet whey, a dairy by-product, to sustain P. freudenreichii growth. It was used at different concentrations (dry matter) as a culture medium. Using hyperconcentrated sweet whey led to enhanced multistress tolerance acquisition, overexpression of key stress proteins, and accumulation of intracellular storage molecules and compatible solutes, as well as enhanced survival upon spray drying. A simplified process from growth to spray drying of propionibacteria was developed using sweet whey as a 2-in-1 medium to both culture P. freudenreichii and protect it from heat and osmotic injury without harvesting and washing steps. As spray drying is far cheaper and more energy efficient than freeze-drying, this work opens new perspectives for the sustainable development of new starter and probiotic preparations with enhanced robustness. IMPORTANCEIn this study, we demonstrate that sweet whey, a dairy industry by-product, not only allows the growth of probiotic dairy propionibacteria, but also triggers a multitolerance response through osmoadaptation and general stress response. We also show that propionibacteria accumulate compatible solutes under these culture conditions, which might account for the limited loss of viability after spray drying. This work opens new perspectives for more energy-efficient production of dairy starters and probiotics.

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Section: Resultsmentioning

confidence: 99%

Hyperconcentrated Sweet Whey, a New Culture Medium That Enhances Propionibacterium freudenreichii Stress Tolerance

Song

Rabah

Jardin

et al. 2016

Appl Environ Microbiol

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“…Besides the function as a reservoir for phosphorus, several other functions of polyP have been discussed in the literature. In bacteria, multiple pieces of evidence that polyP is not essential for survival but enhances survival under several stress conditions have been published (14,(50)(51)(52). Recently, some evidence for a connection of polyP metabolism with PHA metabolism in Pseudomonas putida was shown (53).…”

Section: Discussionmentioning

confidence: 99%

Formation of Polyphosphate by Polyphosphate Kinases and Its Relationship to Poly(3-Hydroxybutyrate) Accumulation in Ralstonia eutropha Strain H16

Tumlirsch

Sznajder

Jendrossek

2015

Appl Environ Microbiol

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A protein (PhaX) that interacted with poly(3-hydroxybutyrate) (PHB) depolymerase PhaZa1 and with PHB granule-associated phasin protein PhaP2 was identified by two-hybrid analysis. Deletion of phaX resulted in an increase in the level of polyphosphate (polyP) granule formation and in impairment of PHB utilization in nutrient broth-gluconate cultures. A procedure for enrichment of polyP granules from cell extracts was developed. Twenty-seven proteins that were absent in other cell fractions were identified in the polyP granule fraction by proteome analysis. One protein (A2437) harbored motifs characteristic of type 1 polyphosphate kinases (PPK1s), and two proteins (A1212, A1271) had PPK2 motifs. In vivo colocalization with polyP granules was confirmed by expression of C-and N-terminal fusions of enhanced yellow fluorescent protein (eYFP) with the three polyphosphate kinases (PPKs). Screening of the genome DNA sequence for additional proteins with PPK motifs revealed one protein with PPK1 motifs and three proteins with PPK2 motifs. Construction and subsequent expression of C-and N-terminal fusions of the four new PPK candidates with eYFP showed that only A1979 (PPK2 motif) colocalized with polyP granules. The other three proteins formed fluorescent foci near the cell pole (apart from polyP) (A0997, B1019) or were soluble (A0226). Expression of the Ralstonia eutropha ppk (ppk Reu ) genes in an Escherichia coli ⌬ppk background and construction of a set of single and multiple chromosomal deletions revealed that both A2437 (PPK1a) and A1212 (PPK2c) contributed to polyP granule formation. Mutants with deletion of both genes were unable to produce polyP granules. The formation and utilization of PHB and polyP granules were investigated in different chromosomal backgrounds. R alstonia eutropha H16 is a facultative chemolithoautotrophic bacterium and has become famous because of its ability to grow autotrophically with hydrogen as the electron donor (the organism is referred to as Knallgasbakterium in German) and to accumulate large amounts of poly(3-hydroxybutyrate) (PHB). The PHB produced by R. eutropha or related species is, meanwhile, a commercially available biopolymer (1, 2). The formation of polyhydroxyalkanoates (PHAs) was studied in the past by many groups (for reviews, see references 3 to 9). Meanwhile, it is generally accepted that PHB granules are supramolecular complexes, and the designation as carbonosomes has been suggested for PHA granules (10). Carbonosomes are composed of a polymer core and have a surface layer of up to 16 proteins with different functions.Inspection of the R. eutropha genome sequence (11) reveals the presence of the key enzymes for biosynthesis of biopolymers other than PHB, such as cyanophycin synthase (12) and polyphosphate kinase (PPK). While the synthesis of cyanophycin has not yet been demonstrated in R. eutropha, the formation of polyphosphate (polyP) is thought to be ubiquitous in all organisms (13-15). Indeed, the formation of polyP granules in R. eutropha is evident from early i...

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“…Inorganic polyphosphate (poly-P) is a polymer of phosphoanhydride-linked phosphate residues that can be found as chains of a few to thousands of residues in living organisms (225). In bacteria, the accumulation of poly-P is dependent on the activity of polyphosphate kinase (Ppk; EC 2.7.4.1), which catalyzes the ATP-dependent formation of a phosphoanhydride bond between a poly-P chain and orthophosphate (226).…”

Section: Metabolism Of Nitrogenmentioning

confidence: 99%

“…plantarum strains containing ppk genes also accumulate poly-P in media with low phosphate levels (228). Poly-P has a protective role against oxidative stress in bacteria, where it acts as a chaperone preventing the aggregation of damaged proteins (225). Poly-P protects some LAB, such as Lb.…”

Section: Metabolism Of Nitrogenmentioning

confidence: 99%

“…fermentum) have also been isolated from natural whey starters, and a positive role has been postulated for poly-P in acid stress resistance of LAB strains during mozzarella cheese production (230). Poly-P is also involved in the regulation of general stress resistance pathways in different bacteria (225), but more research is required to fully understand its role in LAB (228).…”

Section: Metabolism Of Nitrogenmentioning

confidence: 99%

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Stress Physiology of Lactic Acid Bacteria

Papadimitriou

Alegría

Bron

et al. 2016

Microbiol Mol Biol Rev

480

404

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SUMMARYLactic acid bacteria (LAB) are important starter, commensal, or pathogenic microorganisms. The stress physiology of LAB has been studied in depth for over 2 decades, fueled mostly by the technological implications of LAB robustness in the food industry. Survival of probiotic LAB in the host and the potential relatedness of LAB virulence to their stress resilience have intensified interest in the field. Thus, a wealth of information concerning stress responses exists today for strains as diverse as starter (e.g.,Lactococcus lactis), probiotic (e.g., severalLactobacillusspp.), and pathogenic (e.g.,EnterococcusandStreptococcusspp.) LAB. Here we present the state of the art for LAB stress behavior. We describe the multitude of stresses that LAB are confronted with, and we present the experimental context used to study the stress responses of LAB, focusing on adaptation, habituation, and cross-protection as well as on self-induced multistress resistance in stationary phase, biofilms, and dormancy. We also consider stress responses at the population and single-cell levels. Subsequently, we concentrate on the stress defense mechanisms that have been reported to date, grouping them according to their direct participation in preserving cell energy, defending macromolecules, and protecting the cell envelope. Stress-induced responses of probiotic LAB and commensal/pathogenic LAB are highlighted separately due to the complexity of the peculiar multistress conditions to which these bacteria are subjected in their hosts. Induction of prophages under environmental stresses is then discussed. Finally, we present systems-based strategies to characterize the “stressome” of LAB and to engineer new food-related and probiotic LAB with improved stress tolerance.

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Oxidative stress protection by polyphosphate—new roles for an old player

Cited by 146 publications

References 43 publications

Hyperconcentrated Sweet Whey, a New Culture Medium That Enhances Propionibacterium freudenreichii Stress Tolerance

Hyperconcentrated Sweet Whey, a New Culture Medium That Enhances Propionibacterium freudenreichii Stress Tolerance

Formation of Polyphosphate by Polyphosphate Kinases and Its Relationship to Poly(3-Hydroxybutyrate) Accumulation in Ralstonia eutropha Strain H16

Stress Physiology of Lactic Acid Bacteria

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