#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

Social Motility in African Trypanosomes


African trypanosomes are devastating human and animal pathogens that cause significant human mortality and limit economic development in sub-Saharan Africa. Studies of trypanosome biology generally consider these protozoan parasites as individual cells in suspension cultures or in animal models of infection. Here we report that the procyclic form of the African trypanosome Trypanosoma brucei engages in social behavior when cultivated on semisolid agarose surfaces. This behavior is characterized by trypanosomes assembling into multicellular communities that engage in polarized migrations across the agarose surface and cooperate to divert their movements in response to external signals. These cooperative movements are flagellum-mediated, since they do not occur in trypanin knockdown parasites that lack normal flagellum motility. We term this behavior social motility based on features shared with social motility and other types of surface-induced social behavior in bacteria. Social motility represents a novel and unexpected aspect of trypanosome biology and offers new paradigms for considering host-parasite interactions.


Vyšlo v časopise: Social Motility in African Trypanosomes. PLoS Pathog 6(1): e32767. doi:10.1371/journal.ppat.1000739
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1000739

Souhrn

African trypanosomes are devastating human and animal pathogens that cause significant human mortality and limit economic development in sub-Saharan Africa. Studies of trypanosome biology generally consider these protozoan parasites as individual cells in suspension cultures or in animal models of infection. Here we report that the procyclic form of the African trypanosome Trypanosoma brucei engages in social behavior when cultivated on semisolid agarose surfaces. This behavior is characterized by trypanosomes assembling into multicellular communities that engage in polarized migrations across the agarose surface and cooperate to divert their movements in response to external signals. These cooperative movements are flagellum-mediated, since they do not occur in trypanin knockdown parasites that lack normal flagellum motility. We term this behavior social motility based on features shared with social motility and other types of surface-induced social behavior in bacteria. Social motility represents a novel and unexpected aspect of trypanosome biology and offers new paradigms for considering host-parasite interactions.


Zdroje

1. ShapiroJA

1998 Thinking about bacterial populations as multicellular organisms. Annu Rev Microbiol 52 81 104

2. HarsheyRM

2003 Bacterial motility on a surface: many ways to a common goal. Annu Rev Microbiol 57 249 273

3. BasslerBL

LosickR

2006 Bacterially speaking. Cell 125 237 246

4. ShaulskyG

KessinRH

2007 The cold war of the social amoebae. Curr Biol 17 R684 692

5. ReynoldsTB

FinkGR

2001 Bakers' yeast, a model for fungal biofilm formation. Science 291 878 881

6. BlankenshipJR

MitchellAP

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

7. VelicerGJ

YuYT

2003 Evolution of novel cooperative swarming in the bacterium Myxococcus xanthus. Nature 425 75 78

8. KaiserD

2003 Coupling cell movement to multicellular development in myxobacteria. Nat Rev Microbiol 1 45 54

9. FirtelRA

MeiliR

2000 Dictyostelium: a model for regulated cell movement during morphogenesis. Curr Opin Genet Dev 10 421 427

10. RauprichO

MatsushitaM

WeijerCJ

SiegertF

EsipovSE

1996 Periodic phenomena in Proteus mirabilis swarm colony development. J Bacteriol 178 6525 6538

11. FraserGM

HughesC

1999 Swarming motility. Curr Opin Microbiol 2 630 635

12. HenrichsenJ

1972 Bacterial surface translocation: a survey and a classification. Bacteriol Rev 36 478 503

13. RashidMH

KornbergA

2000 Inorganic polyphosphate is needed for swimming, swarming, and twitching motilities of Pseudomonas aeruginosa. Proc Natl Acad Sci U S A 97 4885 4890

14. NudlemanE

WallD

KaiserD

2005 Cell-to-cell transfer of bacterial outer membrane lipoproteins. Science 309 125 127

15. ZusmanDR

ScottAE

YangZ

KirbyJR

2007 Chemosensory pathways, motility and development in Myxococcus xanthus. Nat Rev Microbiol 5 862 872

16. HarsheyRM

1994 Bees aren't the only ones: swarming in gram-negative bacteria. Mol Microbiol 13 389 394

17. VerstraetenN

BraekenK

DebkumariB

FauvartM

FransaerJ

2008 Living on a surface: swarming and biofilm formation. Trends Microbiol 16 496 506

18. KohlerT

CurtyLK

BarjaF

van DeldenC

PechereJC

2000 Swarming of Pseudomonas aeruginosa is dependent on cell-to-cell signaling and requires flagella and pili. J Bacteriol 182 5990 5996

19. LegrosD

OllivierG

Gastellu-EtchegorryM

PaquetC

BurriC

2002 Treatment of human African trypanosomiasis–present situation and needs for research and development. Lancet Infect Dis 2 437 440

20. GibsonW

BaileyM

2003 The development of Trypanosoma brucei within the tsetse fly midgut observed using green fluorescent trypanosomes. Kinetoplastid Biol Dis 2 1

21. Van Den AbbeeleJ

ClaesY

van BockstaeleD

Le RayD

CoosemansM

1999 Trypanosoma brucei spp. development in the tsetse fly: characterization of the post-mesocyclic stages in the foregut and proboscis. Parasitology 118(Pt 5) 469 478

22. VickermanK

1985 Developmental cycles and biology of pathogenic trypanosomes. Br Med Bull 41 105 114

23. VickermanK

TetleyL

HendryKA

TurnerCM

1988 Biology of African trypanosomes in the tsetse fly. Biol Cell 64 109 119

24. RoditiI

LehaneMJ

2008 Interactions between trypanosomes and tsetse flies. Curr Opin Microbiol 11 345 351

25. HendryKA

VickermanK

1988 The requirement for epimastigote attachment during division and metacyclogenesis in Trypanosoma congolense. Parasitol Res 74 403 408

26. Bloodgood

1981 Flagella-Dependent Gliding Motility in Chlamydomonas. Protoplasma 106 183 192

27. O'Toole

2008 How Pseudomonas aeruginosa Regulates Surface Behaviors. Microbe 3 65 71

28. VassellaE

OberleM

UrwylerS

RenggliCK

StuderE

2009 Major surface glycoproteins of insect forms of Trypanosoma brucei are not essential for cyclical transmission by tsetse. PLoS ONE 4 e4493 doi:10.1371/journal.pone.0004493

29. CarruthersVB

CrossGA

1992 High-efficiency clonal growth of bloodstream- and insect-form Trypanosoma brucei on agarose plates. Proc Natl Acad Sci U S A 89 8818 8821

30. HillKL

2003 Biology and mechanism of trypanosome cell motility. Eukaryot Cell 2 200 208

31. CaiazzaNC

ShanksRM

O'TooleGA

2005 Rhamnolipids modulate swarming motility patterns of Pseudomonas aeruginosa. J Bacteriol 187 7351 7361

32. Be'erA

ZhangHP

FlorinEL

PayneSM

Ben-JacobE

2009 Deadly competition between sibling bacterial colonies. Proc Natl Acad Sci U S A 106 428 433

33. InghamCJ

Ben JacobE

2008 Swarming and complex pattern formation in Paenibacillus vortex studied by imaging and tracking cells. BMC Microbiol 8 36

34. HutchingsNR

DonelsonJE

HillKL

2002 Trypanin is a cytoskeletal linker protein and is required for cell motility in African trypanosomes. J Cell Biol 156 867 877

35. MurilloLA

NewportG

LanCY

HabelitzS

DunganJ

2005 Genome-wide transcription profiling of the early phase of biofilm formation by Candida albicans. Eukaryot Cell 4 1562 1573

36. RalstonKS

KabututuZP

MelehaniJH

OberholzerM

HillKL

2009 The Trypanosoma brucei flagellum: moving parasites in new directions. Annu Rev Microbiol 63 335 362

37. GingerML

PortmanN

McKeanPG

2008 Swimming with protists: perception, motility and flagellum assembly. Nat Rev Microbiol 6 838 850

38. VassellaE

ReunerB

YutzyB

BoshartM

1997 Differentiation of African trypanosomes is controlled by a density sensing mechanism which signals cell cycle arrest via the cAMP pathway. J Cell Sci 110(Pt 21) 2661 2671

39. DeanS

MarchettiR

KirkK

MatthewsKR

2009 A surface transporter family conveys the trypanosome differentiation signal. Nature 459 213 217

40. SeebeckT

SchaubR

JohnerA

2004 cAMP signalling in the kinetoplastid protozoa. Curr Mol Med 4 585 599

41. OberholzerM

BregyP

MartiG

MincaM

PeierM

2007 Trypanosomes and mammalian sperm: one of a kind? Trends Parasitol 23 71 77

42. PaindavoineP

RolinS

Van AsselS

GeuskensM

JauniauxJC

1992 A gene from the variant surface glycoprotein expression site encodes one of several transmembrane adenylate cyclases located on the flagellum of Trypanosoma brucei. Mol Cell Biol 12 1218 1225

43. ParsonsM

RubenL

2000 Pathways involved in environmental sensing in trypanosomatids. Parasitol Today 16 56 62

44. FragosoCM

Schumann BurkardG

OberleM

RenggliCK

HilzingerK

2009 PSSA-2, a membrane-spanning phosphoprotein of Trypanosoma brucei, is required for efficient maturation of infection. PLoS ONE 4 e7074 doi:10.1371/journal.pone.0007074

45. BerrimanM

GhedinE

Hertz-FowlerC

BlandinG

RenauldH

2005 The genome of the African trypanosome Trypanosoma brucei. Science 309 416 422

46. GibsonW

PeacockL

FerrisV

WilliamsK

BaileyM

2006 Analysis of a cross between green and red fluorescent trypanosomes. Biochem Soc Trans 34 557 559

47. GibsonW

PeacockL

FerrisV

WilliamsK

BaileyM

2008 The use of yellow fluorescent hybrids to indicate mating in Trypanosoma brucei. Parasit Vectors 1 4

48. WirtzE

LealS

OchattC

CrossGA

1999 A tightly regulated inducible expression system for conditional gene knock-outs and dominant-negative genetics in Trypanosoma brucei. Mol Biochem Parasitol 99 89 101

49. RalstonKS

LernerAG

DienerDR

HillKL

2006 Flagellar motility contributes to cytokinesis in Trypanosoma brucei and is modulated by an evolutionarily conserved dynein regulatory system. Eukaryot Cell 5 696 711

50. RalstonKS

HillKL

2006 Trypanin, a component of the flagellar Dynein regulatory complex, is essential in bloodstream form African trypanosomes. PLoS Pathog 2 e101 doi:10.1371/journal.ppat.0020101

Štítky
Hygiena a epidemiológia Infekčné lekárstvo Laboratórium

Článok vyšiel v časopise

PLOS Pathogens


2010 Číslo 1
Najčítanejšie tento týždeň
Najčítanejšie v tomto čísle
Kurzy

Zvýšte si kvalifikáciu online z pohodlia domova

Aktuální možnosti diagnostiky a léčby litiáz
nový kurz
Autori: MUDr. Tomáš Ürge, PhD.

Všetky kurzy
Prihlásenie
Zabudnuté heslo

Zadajte e-mailovú adresu, s ktorou ste vytvárali účet. Budú Vám na ňu zasielané informácie k nastaveniu nového hesla.

Prihlásenie

Nemáte účet?  Registrujte sa

#ADS_BOTTOM_SCRIPTS#