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Dispersion as an Important Step in the Biofilm Developmental Cycle


Biofilms are dynamic microbial communities in which transitions between planktonic and sessile modes of growth occur interchangeably in response to different environmental cues. In the last decade, early events associated with C. albicans biofilm formation have received considerable attention. However, very little is known about C. albicans biofilm dispersion or the mechanisms and signals that trigger it. This is important because it is precisely C. albicans cells dispersed from biofilms that are the main culprits associated with candidemia and establishment of disseminated invasive disease, two of the gravest forms of candidiasis. Using a simple flow biofilm model recently developed by our group, we have performed initial investigations into the phenomenon of C. albicans biofilm dispersion, as well as the phenotypic characteristics associated with dispersed cells. Our results indicate that C. albicans biofilm dispersion is dependent on growing conditions, including carbon source and pH of the media used for biofilm development. C. albicans dispersed cells are mostly in the yeast form and display distinct phenotypic properties compared to their planktonic counterparts, including enhanced adherence, filamentation, biofilm formation and, perhaps most importantly, increased pathogenicity in a murine model of hematogenously disseminated candidiasis, thus indicating that dispersed cells are armed with a complete arsenal of “virulence factors” important for seeding and establishing new foci of infection. In addition, utilizing genetically engineered strains of C. albicans (tetO-UME6 and tetO-PES1) we demonstrate that C. albicans biofilm dispersion can be regulated by manipulating levels of expression of these key genes, further supporting the evidence for a strong link between biofilms and morphogenetic conversions at different stages of the C. albicans biofilm developmental cycle. Overall, our results offer novel and important insight into the phenomenon of C. albicans biofilm dispersion, a key part of the biofilm developmental cycle, and provide the basis for its more detailed analysis.


Vyšlo v časopise: Dispersion as an Important Step in the Biofilm Developmental Cycle. PLoS Pathog 6(3): e32767. doi:10.1371/journal.ppat.1000828
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1000828

Souhrn

Biofilms are dynamic microbial communities in which transitions between planktonic and sessile modes of growth occur interchangeably in response to different environmental cues. In the last decade, early events associated with C. albicans biofilm formation have received considerable attention. However, very little is known about C. albicans biofilm dispersion or the mechanisms and signals that trigger it. This is important because it is precisely C. albicans cells dispersed from biofilms that are the main culprits associated with candidemia and establishment of disseminated invasive disease, two of the gravest forms of candidiasis. Using a simple flow biofilm model recently developed by our group, we have performed initial investigations into the phenomenon of C. albicans biofilm dispersion, as well as the phenotypic characteristics associated with dispersed cells. Our results indicate that C. albicans biofilm dispersion is dependent on growing conditions, including carbon source and pH of the media used for biofilm development. C. albicans dispersed cells are mostly in the yeast form and display distinct phenotypic properties compared to their planktonic counterparts, including enhanced adherence, filamentation, biofilm formation and, perhaps most importantly, increased pathogenicity in a murine model of hematogenously disseminated candidiasis, thus indicating that dispersed cells are armed with a complete arsenal of “virulence factors” important for seeding and establishing new foci of infection. In addition, utilizing genetically engineered strains of C. albicans (tetO-UME6 and tetO-PES1) we demonstrate that C. albicans biofilm dispersion can be regulated by manipulating levels of expression of these key genes, further supporting the evidence for a strong link between biofilms and morphogenetic conversions at different stages of the C. albicans biofilm developmental cycle. Overall, our results offer novel and important insight into the phenomenon of C. albicans biofilm dispersion, a key part of the biofilm developmental cycle, and provide the basis for its more detailed analysis.


Zdroje

1. BanerjeeSN

EmoriTG

CulverDH

GaynesRP

JarvisWR

1991 Secular trends in nosocomial primary bloodstream infections in the United States, 1980–1989. National Nosocomial Infections Surveillance System. Am J Med 91 86S 89S

2. Beck-SagueC

JarvisWR

1993 Secular trends in the epidemiology of nosocomial fungal infections in the United States, 1980–1990. National Nosocomial Infections Surveillance System. J Infect Dis 167 1247 1251

3. WisplinghoffH

BischoffT

TallentSM

SeifertH

WenzelRP

2004 Nosocomial bloodstream infections in US hospitals: analysis of 24,179 cases from a prospective nationwide surveillance study. Clin Infect Dis 39 309 317

4. PfallerMA

DiekemaDJ

2007 Epidemiology of invasive candidiasis: a persistent public health problem. Clin Microbiol Rev 20 133 163

5. ViudesA

PemanJ

CantonE

UbedaP

Lopez-RibotJL

2002 Candidemia at a tertiary-care hospital: epidemiology, treatment, clinical outcome and risk factors for death. Eur J Clin Microbiol Infect Dis 21 767 774

6. WeySB

MoriM

PfallerMA

WoolsonRF

WenzelRP

1988 Hospital-acquired candidemia. The attributable mortality and excess length of stay. Arch Intern Med 148 2642 2645

7. PappasPG

RexJH

LeeJ

HamillRJ

LarsenRA

2003 A prospective observational study of candidemia: epidemiology, therapy, and influences on mortality in hospitalized adult and pediatric patients. Clin Infect Dis 37 634 643

8. KojicEM

DarouicheRO

2004 Candida infections of medical devices. Clin Microbiol Rev 17 255 267

9. RamageG

MartinezJP

Lopez-RibotJL

2006 Candida biofilms on implanted biomaterials: a clinically significant problem. FEMS Yeast Res 6 979 986

10. RamageG

SavilleSP

ThomasDP

Lopez-RibotJL

2005 Candida biofilms: an update. Eukaryot Cell 4 633 638

11. CrumpJA

CollignonPJ

2000 Intravascular catheter-associated infections. Eur J Clin Microbiol Infect Dis 19 1 8

12. DatoVM

DajaniAS

1990 Candidemia in children with central venous catheters: role of catheter removal and amphotericin B therapy. Pediatr Infect Dis J 9 309 314

13. EppesSC

TroutmanJL

GutmanLT

1989 Outcome of treatment of candidemia in children whose central catheters were removed or retained. Pediatr Infect Dis J 8 99 104

14. HawserSP

BaillieGS

DouglasLJ

1998 Production of extracellular matrix by Candida albicans biofilms. J Med Microbiol 47 253 256

15. HawserSP

DouglasLJ

1994 Biofilm formation by Candida species on the surface of catheter materials in vitro. Infect Immun 62 915 921

16. HonraetK

GoetghebeurE

NelisHJ

2005 Comparison of three assays for the quantification of Candida biomass in suspension and CDC reactor grown biofilms. J Microbiol Methods 63 287 295

17. KlotzSA

DrutzDJ

ZajicJE

1985 Factors governing adherence of Candida species to plastic surfaces. Infect Immun 50 97 101

18. NikawaH

NishimuraH

HamadaT

KumagaiH

SamaranayakeLP

1997 Effects of dietary sugars and, saliva and serum on Candida bioflim formation on acrylic surfaces. Mycopathologia 139 87 91

19. RamageG

WickesBL

Lopez-RibotJL

2008 A seed and feed model for the formation of Candida albicans biofilms under flow conditions using an improved modified Robbins device. Rev Iberoam Micol 25 37 40

20. UppuluriP

ChaturvediAK

Lopez-RibotJL

2009 Design of a simple model of Candida albicans biofilms formed under conditions of flow: development, architecture, and drug resistance. Mycopathologia 168 101 109

21. ChandraJ

KuhnDM

MukherjeePK

HoyerLL

McCormickT

2001 Biofilm formation by the fungal pathogen Candida albicans: development, architecture, and drug resistance. J Bacteriol 183 5385 5394

22. BlankenshipJR

MitchellAP

2006 How to build a biofilm: a fungal perspective. Curr Opin Microbiol 9 588 594

23. NobileCJ

MitchellAP

2005 Regulation of cell-surface genes and biofilm formation by the C. albicans transcription factor Bcr1p. Curr Biol 15 1150 1155

24. RichardML

NobileCJ

BrunoVM

MitchellAP

2005 Candida albicans biofilm-defective mutants. Eukaryot Cell 4 1493 1502

25. SavilleSP

ThomasDP

Lopez RibotJL

2006 A role for Efg1p in Candida albicans interactions with extracellular matrices. FEMS Microbiol Lett 256 151 158

26. GjermansenM

RagasP

SternbergC

MolinS

Tolker-NielsenT

2005 Characterization of starvation-induced dispersion in Pseudomonas putida biofilms. Environ Microbiol 7 894 906

27. SauerK

CullenMC

RickardAH

ZeefLA

DaviesDG

2004 Characterization of nutrient-induced dispersion in Pseudomonas aeruginosa PAO1 biofilm. J Bacteriol 186 7312 7326

28. DaviesDG

MarquesCN

2009 A fatty acid messenger is responsible for inducing dispersion in microbial biofilms. J Bacteriol 191 1393 1403

29. GjermansenM

RagasP

Tolker-NielsenT

2006 Proteins with GGDEF and EAL domains regulate Pseudomonas putida biofilm formation and dispersal. FEMS Microbiol Lett 265 215 224

30. MorganR

KohnS

HwangSH

HassettDJ

SauerK

2006 BdlA, a chemotaxis regulator essential for biofilm dispersion in Pseudomonas aeruginosa. J Bacteriol 188 7335 7343

31. SauerK

CamperAK

EhrlichGD

CostertonJW

DaviesDG

2002 Pseudomonas aeruginosa displays multiple phenotypes during development as a biofilm. J Bacteriol 184 1140 1154

32. GrangerBL

FlennikenML

DavisDA

MitchellAP

CutlerJE

2005 Yeast wall protein 1 of Candida albicans. Microbiology 151 1631 1644

33. SellamA

Al-NiemiT

McInnerneyK

BrumfieldS

NantelA

2009 A Candida albicans early stage biofilm detachment event in rich medium. BMC Microbiol 9 25

34. CarlislePL

BanerjeeM

LazzellA

MonteagudoC

Lopez-RibotJL

2009 Expression levels of a filament-specific transcriptional regulator are sufficient to determine Candida albicans morphology and virulence. Proc Natl Acad Sci U S A 106 599 604

35. ShenJ

CowenLE

GriffinAM

ChanL

KohlerJR

2008 The Candida albicans pescadillo homolog is required for normal hypha-to-yeast morphogenesis and yeast proliferation. Proc Natl Acad Sci U S A 105 20918 20923

36. BirdRB

StewartWE

LightfootEN

1960 “Transport Phenomena”. 36 40 John Wiley & Sons, NY

37. PierceCG

UppuluriP

TristanAR

WormleyFLJr

MowatE

2008 A simple and reproducible 96-well plate-based method for the formation of fungal biofilms and its application to antifungal susceptibility testing. Nat Protoc 3 1494 1500

38. FrangosJA

McIntireLV

EskinSG

1988 Shear stress induced stimulation of mammalian cell metabolism. Biotechnol Bioeng 32 1053 1060

39. HornbyJM

JensenEC

LisecAD

TastoJJ

JahnkeB

2001 Quorum sensing in the dimorphic fungus Candida albicans is mediated by farnesol. Appl Environ Microbiol 67 2982 2992

40. RamageG

SavilleSP

WickesBL

Lopez-RibotJL

2002 Inhibition of Candida albicans biofilm formation by farnesol, a quorum-sensing molecule. Appl Environ Microbiol 68 5459 5463

41. GrubbSE

MurdochC

SudberyPE

SavilleSP

Lopez-RibotJL

2008 Candida albicans-endothelial cell interactions: a key step in the pathogenesis of systemic candidiasis. Infect Immun 76 4370 4377

42. SanchezAA

JohnstonDA

MyersC

EdwardsJEJr

MitchellAP

2004 Relationship between Candida albicans virulence during experimental hematogenously disseminated infection and endothelial cell damage in vitro. Infect Immun 72 598 601

43. BanerjeeM

ThompsonDS

LazzellA

CarlislePL

PierceC

2008 UME6, a novel filament-specific regulator of Candida albicans hyphal extension and virulence. Mol Biol Cell 19 1354 1365

44. Alonso-ValleH

AchaO

Garcia-PalomoJD

Farinas-AlvarezC

Fernandez-MazarrasaC

2003 Candidemia in a tertiary care hospital: epidemiology and factors influencing mortality. Eur J Clin Microbiol Infect Dis 22 254 257

45. MacphailGL

TaylorGD

Buchanan-ChellM

RossC

WilsonS

2002 Epidemiology, treatment and outcome of candidemia: a five-year review at three Canadian hospitals. Mycoses 45 141 145

46. VossA

le NobleJL

Verduyn LunelFM

FoudraineNA

MeisJF

1997 Candidemia in intensive care unit patients: risk factors for mortality. Infection 25 8 11

47. DouglasLJ

2003 Candida biofilms and their role in infection. Trends Microbiol 11 30 36

48. DowJM

CrossmanL

FindlayK

HeYQ

FengJX

2003 Biofilm dispersal in Xanthomonas campestris is controlled by cell-cell signaling and is required for full virulence to plants. Proc Natl Acad Sci U S A 100 10995 11000

49. WangY

DaiY

ZhangY

HuY

YangB

2007 Effects of quorum sensing autoinducer degradation gene on virulence and biofilm formation of Pseudomonas aeruginosa. Sci China C Life Sci 50 385 391

50. RamageG

Vande WalleK

WickesBL

Lopez-RibotJL

2001 Standardized method for in vitro antifungal susceptibility testing of Candida albicans biofilms. Antimicrob Agents Chemother 45 2475 2479

51. Ymele-LekiP

RossJM

2007 Erosion from Staphylococcus aureus biofilms grown under physiologically relevant fluid shear forces yields bacterial cells with reduced avidity to collagen. Appl Environ Microbiol 73 1834 1841

52. TelgmannU

HornH

MorgenrothE

2004 Influence of growth history on sloughing and erosion from biofilms. Water Res 38 3671 3684

53. GrubbSE

MurdochC

SudberyPE

SavilleSP

Lopez-RibotJL

2009 Adhesion of Candida albicans to Endothelial Cells under Physiological Conditions of Flow. Infect Immun

54. LawrenceMB

SmithCW

EskinSG

McIntireLV

1990 Effect of venous shear stress on CD18-mediated neutrophil adhesion to cultured endothelium. Blood 75 227 237

55. BaillieGS

DouglasLJ

1998 Effect of growth rate on resistance of Candida albicans biofilms to antifungal agents. Antimicrob Agents Chemother 42 1900 1905

56. JacksonDW

SuzukiK

OakfordL

SimeckaJW

HartME

2002 Biofilm formation and dispersal under the influence of the global regulator CsrA of Escherichia coli. J Bacteriol 184 290 301

57. JamesGA

KorberDR

CaldwellDE

CostertonJW

1995 Digital image analysis of growth and starvation responses of a surface-colonizing Acinetobacter sp. J Bacteriol 177 907 915

58. ZhaoX

DanielsKJ

OhSH

GreenCB

YeaterKM

2006 Candida albicans Als3p is required for wild-type biofilm formation on silicone elastomer surfaces. Microbiology 152 2287 2299

59. LiF

SvarovskyMJ

KarlssonAJ

WagnerJP

MarchilloK

2007 Eap1p, an adhesin that mediates Candida albicans biofilm formation in vitro and in vivo. Eukaryot Cell 6 931 939

60. RamageG

VandeWalleK

Lopez-RibotJL

WickesBL

2002 The filamentation pathway controlled by the Efg1 regulator protein is required for normal biofilm formation and development in Candida albicans. FEMS Microbiol Lett 214 95 100

61. NobileCJ

SchneiderHA

NettJE

SheppardDC

FillerSG

2008 Complementary adhesin function in C. albicans biofilm formation. Curr Biol 18 1017 1024

62. VatsN

LeeSF

2000 Active detachment of Streptococcus mutans cells adhered to epon-hydroxylapatite surfaces coated with salivary proteins in vitro. Arch Oral Biol 45 305 314

63. ApplegateDH

BryersJD

1991 Effects of carbon and oxygen limitations and calcium concentrations on biofilm removal processes. Biotechnol Bioeng 37 17 25

64. ThormannKM

DuttlerS

SavilleRM

HyodoM

ShuklaS

2006 Control of formation and cellular detachment from Shewanella oneidensis MR-1 biofilms by cyclic di-GMP. J Bacteriol 188 2681 2691

65. RomeoT

GongM

LiuMY

Brun-ZinkernagelAM

1993 Identification and molecular characterization of csrA, a pleiotropic gene from Escherichia coli that affects glycogen biosynthesis, gluconeogenesis, cell size, and surface properties. J Bacteriol 175 4744 4755

66. BakerCS

MorozovI

SuzukiK

RomeoT

BabitzkeP

2002 CsrA regulates glycogen biosynthesis by preventing translation of glgC in Escherichia coli. Mol Microbiol 44 1599 1610

67. StoodleyP

WilsonS

Hall-StoodleyL

BoyleJD

Lappin-ScottHM

2001 Growth and detachment of cell clusters from mature mixed-species biofilms. Appl Environ Microbiol 67 5608 5613

68. ShapiroRS

UppuluriP

ZaasAK

CollinsC

SennH

2009 Hsp90 orchestrates temperature-dependent Candida albicans morphogenesis via Ras1-PKA signaling. Curr Biol 19 621 629

69. CowenLE

CarpenterAE

MatangkasombutO

FinkGR

LindquistS

2006 Genetic architecture of Hsp90-dependent drug resistance. Eukaryot Cell 5 2184 2188

70. CowenLE

SinghSD

KohlerJR

CollinsC

ZaasAK

2009 Harnessing Hsp90 function as a powerful, broadly effective therapeutic strategy for fungal infectious disease. Proc Natl Acad Sci U S A 106 2818 2823

71. DuYC

StillmanB

2002 Yph1p, an ORC-interacting protein: potential links between cell proliferation control, DNA replication, and ribosome biogenesis. Cell 109 835 848

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Hygiena a epidemiológia Infekčné lekárstvo Laboratórium

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