A Central Role for Carbon-Overflow Pathways in the Modulation of Bacterial Cell Death

English version České info

Many bacterial species including the pathogen Staphylococcus aureus are capable of adhering to surfaces and forming complex communities called biofilms. This mode of growth can be particularly challenging from an infection control standpoint, as they are often refractory to antibiotics and host immune system. Although developmental processes underlying biofilm formation are not entirely clear, recent evidence suggests that cell death of a subpopulation is crucial for its maturation. In this study we provide insight regarding the metabolic pathways that control cell death and demonstrate that acetate, a by-product of glucose catabolism, potentiates a form of cell death that exhibits physiological and biochemical hallmarks of apoptosis in eukaryotic organisms. Finally, we demonstrate that altering the ability of metabolic pathways that regulate acetate mediated cell death in S. aureus affects the outcome of biofilm-related diseases, such as infective endocarditis.

Vyšlo v časopise: A Central Role for Carbon-Overflow Pathways in the Modulation of Bacterial Cell Death. PLoS Pathog 10(6): e32767. doi:10.1371/journal.ppat.1004205
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1004205

Souhrn

Zdroje

1. Ameisen JC (2001) The origin and evolution of programmed cell death. eLS: Wiley.

2. BaylesKW (2007) The biological role of death and lysis in biofilm development. Nat Rev Microbiol 5: 721–726.

3. RiceKC, BaylesKW (2008) Molecular control of bacterial death and lysis. Microbiol Mol Biol Rev 72: 85–109 table of contents

4. DwyerDJ, CamachoDM, KohanskiMA, CalluraJM, CollinsJJ (2012) Antibiotic-induced bacterial cell death exhibits physiological and biochemical hallmarks of apoptosis. Mol Cell 46: 561–572.

5. BosJ, YakhninaAA, GitaiZ (2012) BapE DNA endonuclease induces an apoptotic-like response to DNA damage in Caulobacter. Proc Natl Acad Sci U S A 109: 18096–18101.

6. ErentalA, SharonI, Engelberg-KulkaH (2012) Two programmed cell death systems in Escherichia coli: an apoptotic-like death is inhibited by the mazEF-mediated death pathway. PLoS Biol 10: e1001281.

7. YangSJ, DunmanPM, ProjanSJ, BaylesKW (2006) Characterization of the Staphylococcus aureus CidR regulon: elucidation of a novel role for acetoin metabolism in cell death and lysis. Mol Microbiol 60: 458–468.

8. SonensheinAL (2007) Control of key metabolic intersections in Bacillus subtilis. Nat Rev Microbiol 5: 917–927.

9. NahkuR, ValgepeaK, LahtveePJ, ErmS, AbnerK, et al. (2010) Specific growth rate dependent transcriptome profiling of Escherichia coli K12 MG1655 in accelerostat cultures. J Biotechnol 145: 60–65.

10. SadykovMR, BaylesKW (2012) The control of death and lysis in staphylococcal biofilms: a coordination of physiological signals. Curr Opin Microbiol 15: 211–215.

11. AndersenJL, KornbluthS (2013) The tangled circuitry of metabolism and apoptosis. Mol Cell 49: 399–410.

12. SmithJJ, McFetersGA (1997) Mechanisms of INT (2-(4-iodophenyl)-3-(4-nitrophenyl)-5-phenyl tetrazolium chloride), and CTC (5-cyano-2,3-ditolyl tetrazolium chloride) reduction in Escherichia coli K-12. Journal of Microbiological Methods 29: 161–175.

13. SetsukinaiK, UranoY, KakinumaK, MajimaHJ, NaganoT (2003) Development of novel fluorescence probes that can reliably detect reactive oxygen species and distinguish specific species. J Biol Chem 278: 3170–3175.

14. RezaikiL, CesselinB, YamamotoY, VidoK, van WestE, et al. (2004) Respiration metabolism reduces oxidative and acid stress to improve long-term survival of Lactococcus lactis. Mol Microbiol 53: 1331–1342.

15. HiguchiY (2003) Chromosomal DNA fragmentation in apoptosis and necrosis induced by oxidative stress. Biochem Pharmacol 66: 1527–1535.

16. SomervilleGA, ProctorRA (2009) At the crossroads of bacterial metabolism and virulence factor synthesis in staphylococci. Microbiol Mol Biol Rev 73: 233–248.

17. PattonTG, RiceKC, FosterMK, BaylesKW (2005) The Staphylococcus aureus cidC gene encodes a pyruvate oxidase that affects acetate metabolism and cell death in stationary phase. Mol Microbiol 56: 1664–1674.

18. Booth IR, Stratford M (2003) Acidulants and low pH. In: Russell NJ, Gould GW, editors. Food preservatives. 2nd ed. New York: Kluwer Academic/Plenum Publishers. 25–42 p.

19. SadykovMR, ThomasVC, MarshallDD, WenstromCJ, MoormeierDE, et al. (2013) Inactivation of the Pta-AckA pathway causes cell death in Staphylococcus aureus. J Bacteriol 195: 3035–3044.

20. TsangLH, CassatJE, ShawLN, BeenkenKE, SmeltzerMS (2008) Factors contributing to the biofilm-deficient phenotype of Staphylococcus aureus sarA mutants. PLoS One 3: e3361.

21. TsauJL, GuffantiAA, MontvilleTJ (1992) Conversion of Pyruvate to Acetoin Helps To Maintain pH Homeostasis in Lactobacillus plantarum. Appl Environ Microbiol 58: 891–894.

22. SimonHU, Haj-YehiaA, Levi-SchafferF (2000) Role of reactive oxygen species (ROS) in apoptosis induction. Apoptosis 5: 415–418.

23. GranotD, LevineA, Dor-HefetzE (2003) Sugar-induced apoptosis in yeast cells. FEMS Yeast Res 4: 7–13.

24. MoormeierDE, EndresJL, MannEE, SadykovMR, HorswillAR, et al. (2013) Use of microfluidic technology to analyze gene expression during Staphylococcus aureus biofilm formation reveals distinct physiological niches. Appl Environ Microbiol 79: 3413–3424.

25. RodeTM, MoretroT, LangsrudS, LangsrudO, VogtG, et al. (2010) Responses of Staphylococcus aureus exposed to HCl and organic acid stress. Can J Microbiol 56: 777–792.

26. HidalgoG, BurnsA, HerzE, HayAG, HoustonPL, et al. (2009) Functional tomographic fluorescence imaging of pH microenvironments in microbial biofilms by use of silica nanoparticle sensors. Appl Environ Microbiol 75: 7426–7435.

27. HunterRC, BeveridgeTJ (2005) Application of a pH-sensitive fluoroprobe (C-SNARF-4) for pH microenvironment analysis in Pseudomonas aeruginosa biofilms. Appl Environ Microbiol 71: 2501–2510.

28. StewartPS (2003) Diffusion in biofilms. J Bacteriol 185: 1485–1491.

29. RiceKC, NelsonJB, PattonTG, YangSJ, BaylesKW (2005) Acetic acid induces expression of the Staphylococcus aureus cidABC and lrgAB murein hydrolase regulator operons. J Bacteriol 187: 813–821.

30. RepizoGD, MorteraP, MagniC (2011) Disruption of the alsSD operon of Enterococcus faecalis impairs growth on pyruvate at low pH. Microbiology 157: 2708–2719.

31. WellenKE, ThompsonCB (2012) A two-way street: reciprocal regulation of metabolism and signalling. Nat Rev Mol Cell Biol 13: 270–276.

32. WolfeAJ (2005) The acetate switch. Microbiol Mol Biol Rev 69: 12–50.

33. LudovicoP, SousaMJ, SilvaMT, LeaoC, Corte-RealM (2001) Saccharomyces cerevisiae commits to a programmed cell death process in response to acetic acid. Microbiology 147: 2409–2415.

34. MarquesC, OliveiraCS, AlvesS, ChavesSR, CoutinhoOP, et al. (2013) Acetate-induced apoptosis in colorectal carcinoma cells involves lysosomal membrane permeabilization and cathepsin D release. Cell Death Dis 4: e507.

35. TittmannK, GolbikR, GhislaS, HubnerG (2000) Mechanism of elementary catalytic steps of pyruvate oxidase from Lactobacillus plantarum. Biochemistry 39: 10747–10754.

36. RussellP, HagerLP, GennisRB (1977) Characterization of the proteolytic activation of pyruvate oxidase. Control by specific ligands and by the flavin oxidation-reduction state. J Biol Chem 252: 7877–7882.

37. Regev-YochayG, TrzcinskiK, ThompsonCM, LipsitchM, MalleyR (2007) SpxB is a suicide gene of Streptococcus pneumoniae and confers a selective advantage in an in vivo competitive colonization model. J Bacteriol 189: 6532–6539.

38. DhawanVK, YeamanMR, CheungAL, KimE, SullamPM, et al. (1997) Phenotypic resistance to thrombin-induced platelet microbicidal protein in vitro is correlated with enhanced virulence in experimental endocarditis due to Staphylococcus aureus. Infect Immun 65: 3293–3299.

39. Herzberg MC (2000) Persistence of infective endocarditis. In: Nataro JP, Blaser, M. J., Cunningham-Rundles, S., editor. Persistent bacterial infections Washington, DC: ASM Press. pp. 470.

40. ZhuangK, VemuriGN, MahadevanR (2011) Economics of membrane occupancy and respiro-fermentation. Mol Syst Biol 7: 500.

41. XieZ, SchendelS, MatsuyamaS, ReedJC (1998) Acidic pH promotes dimerization of Bcl-2 family proteins. Biochemistry 37: 6410–6418.

42. FurlongIJ, AscasoR, Lopez RivasA, CollinsMK (1997) Intracellular acidification induces apoptosis by stimulating ICE-like protease activity. J Cell Sci 110(Pt 5): 653–661.

43. LeeCY, BuranenSL, YeZH (1991) Construction of single-copy integration vectors for Staphylococcus aureus. Gene 103: 101–105.

44. NicholsonWL (2008) The Bacillus subtilis ydjL (bdhA) gene encodes acetoin reductase/2,3-butanediol dehydrogenase. Appl Environ Microbiol 74: 6832–6838.

45. MannEE, RiceKC, BolesBR, EndresJL, RanjitD, et al. (2009) Modulation of eDNA release and degradation affects Staphylococcus aureus biofilm maturation. PLoS One 4: e5822.

46. HeydornA, NielsenAT, HentzerM, SternbergC, GivskovM, et al. (2000) Quantification of biofilm structures by the novel computer program COMSTAT. Microbiology 146: 2395–2407.

47. ThurlowLR, ThomasVC, NarayananS, OlsonS, FlemingSD, et al. (2010) Gelatinase contributes to the pathogenesis of endocarditis caused by Enterococcus faecalis. Infect Immun 78: 4936–4943.