Pseudomonas aeruginosa uses type III secretion system to kill biofilm-associated amoebae

TY - JOUR

T1 - Pseudomonas aeruginosa uses type III secretion system to kill biofilm-associated amoebae

AU - Matz, Carsten

AU - Moreno, Ana Maria

AU - Alhede, Morten

AU - Manefield, Mike

AU - Hauser, Alan R

AU - Givskov, Michael

AU - Kjelleberg, Staffan

N1 - Keywords: ADP Ribose Transferases; Acanthamoeba castellanii; Animals; Antibiosis; Bacterial Proteins; Bacterial Toxins; Biofilms; Coculture Techniques; GTPase-Activating Proteins; Gene Deletion; Gene Expression Profiling; Gene Expression Regulation, Bacterial; Membrane Transport Proteins; Pseudomonas aeruginosa; RNA, Bacterial; RNA, Messenger; Sigma Factor; Virulence Factors

PY - 2008

Y1 - 2008

N2 - Bacteria and protozoa coexist in a wide range of biofilm communities of natural, technical and medical importance. Generally, this interaction is characterized by the extensive grazing activity of protozoa on bacterial prey populations. We hypothesized that the close spatial coexistence in biofilms should allow opportunistic pathogenic bacteria to utilize their eukaryote-targeting arsenal to attack and exploit protozoan host cells. Studying cocultures of the environmental pathogen Pseudomonas aeruginosa and the amoeba Acanthamoeba castellanii, we found that P. aeruginosa rapidly colonized and killed biofilm-associated amoebae by a quorum-sensing independent mechanism. Analysis of the amoeba-induced transcriptome indicated the involvement of the P. aeruginosa type III secretion system (T3SS) in this interaction. A comparison of mutants with specific defects in the T3SS demonstrated the use of the secretion apparatus and the effectors ExoU, ExoS and ExoT in the killing process, of which ExoU had the greatest impact. T3SS-mediated virulence towards A. castellanii was found to be controlled by the global regulators RpoN and RpoS and through modulation of cAMP and alginate biosynthesis. Our findings suggest that conserved virulence pathways and specifically the T3SS play a central role in bacteria-protozoa interactions in biofilms and may be instrumental for the environmental persistence and evolution of opportunistic bacterial pathogens.

AB - Bacteria and protozoa coexist in a wide range of biofilm communities of natural, technical and medical importance. Generally, this interaction is characterized by the extensive grazing activity of protozoa on bacterial prey populations. We hypothesized that the close spatial coexistence in biofilms should allow opportunistic pathogenic bacteria to utilize their eukaryote-targeting arsenal to attack and exploit protozoan host cells. Studying cocultures of the environmental pathogen Pseudomonas aeruginosa and the amoeba Acanthamoeba castellanii, we found that P. aeruginosa rapidly colonized and killed biofilm-associated amoebae by a quorum-sensing independent mechanism. Analysis of the amoeba-induced transcriptome indicated the involvement of the P. aeruginosa type III secretion system (T3SS) in this interaction. A comparison of mutants with specific defects in the T3SS demonstrated the use of the secretion apparatus and the effectors ExoU, ExoS and ExoT in the killing process, of which ExoU had the greatest impact. T3SS-mediated virulence towards A. castellanii was found to be controlled by the global regulators RpoN and RpoS and through modulation of cAMP and alginate biosynthesis. Our findings suggest that conserved virulence pathways and specifically the T3SS play a central role in bacteria-protozoa interactions in biofilms and may be instrumental for the environmental persistence and evolution of opportunistic bacterial pathogens.

U2 - 10.1038/ismej.2008.47

DO - 10.1038/ismej.2008.47

M3 - Journal article

C2 - 18480848

SN - 1751-7362

VL - 2

SP - 843

EP - 852

JO - ISME Journal

JF - ISME Journal

IS - 8

ER -