ReviewPathogen–host interactions in Dictyostelium, Legionella, Mycobacterium and other pathogens
Introduction
Protozoa impose a tremendous selection pressure in the prokaryote world. As a result various bacteria developed strategies to escape or survive the attack of predatory protozoa. Moreover, some species evolved strategies to exploit host cell resources [1]. The intracellular niche within protozoa can provide microbes with nutrients and represents as shelter against unfavorable living conditions. Moreover, in some cases protozoa may serve as a vehicle for the colonization of new habitats. Since phagocytosis and endosomal trafficking are highly conserved throughout the evolution of eukaryotes, protozoa may be viewed as “ancient virulence school” for microbes which later developed into human pathogens. Accordingly, many cellular defense mechanisms active in animal immune phagocytes have been identified in protozoa. On the other hand, many of the bacterial virulence factors required for pathogenicity in mammals are equally important for pathogen survival during the interactions with protozoa [2]. For the study of some pathogens like Legionella pneumophila and Mycobacterium marinum the social amoeba Dictyostelium discoideum has become a prime model organism, which in many aspects allows the extrapolation to human macrophages (Fig. 1). Meanwhile, the research was extended to numerous other pathogens [3], [4], [5], [6], [7].
Section snippets
Dictyostelium, an infection model for many reasons
The success of D. discoideum as model organism is due to its intrinsic biological features, but also to the remarkable experimental tools available. Unlike other protozoa, such as Acanthamoeba castellanii or Hartmannella vermiformis, D. discoideum is amenable to genetic manipulation. Accordingly, D. discoideum has long been regarded as model organism for the study of signal transduction, cytoskeletal functions and phagocytosis. However, since this model can be infected by various pathogens and
Legionella directed phagosome biogenesis
L. pneumophila is an environmental gram-negative bacterium that parasitizes within different protozoa species. Upon transmission to humans, which is by inhalation of contaminated aerosols, L. pneumophila causes a severe and life-threatening pneumonia [38]. Comparative experiments with several infection models including D. discoideum and human macrophages have shown that the modulation of diverse host cell functions is a prerequisite for biogenesis of the Legionella-specific replicative vacuole.
Conclusion and outlook
The D. discoideum model integrates complex activities of a multicellular organism in a single cell. It allows to test the susceptibility of a given host cell mutant to various bacterial pathogens with a high degree of reproducibility. On the other hand D. discoideum is remarkably effective for identifying novel bacterial virulence determinants. In this review we have highlighted several new proteins and genes which show that knowledge acquired through the study of the D. discoideum model
Acknowledgements
The author wish to thank Christina Nitzsche for critical reading of the manuscript. The work was supported by the Deutsche Forschungsgemeinschaft (DFG).
References (66)
- et al.
Eat, kill, or die: when amoeba meets bacteria
Curr Opin Microbiol
(2008) - et al.
Surrogate hosts: protozoa and invertebrates as models for studying pathogen–host interactions
Int J Med Microbiol
(2003) Conservatism in slime mold development
Cell
(1981)- et al.
Morphogenesis and differentiation of Dictyostelium cells interacting with immobilized glucosides: dependence on DIF production
Differentiation
(1992) Fluid-phase uptake and transit in axenic Dictyostelium cells
Biochem Biophys Acta
(2001)Conserved features of endocytosis in Dictyostelium
Int Rev Cytol
(2002)- et al.
Phagocytosis and host–pathogen interactions in Dictyostelium with a look at macrophages
Int Rev Cell Mol Biol
(2008) - et al.
Phagocyte meets prey: uptake, internalization, and killing of bacteria by Dictyostelium amoebae
Eur J Cell Biol
(2006) - et al.
A novel phosphatidylinositol 4,5-bisphosphate-binding domain targeting the Phg2 kinase to the membrane in Dictyostelium cells
Eur J Cell Biol
(2005) - et al.
Coronin and vacuolin identify consecutive stages of a late, actin-coated endocytic compartment in Dictyostelium
Curr Biol
(1997)
Proteomics fingerprinting of phagosome maturation and evidence for the role of a Galpha during uptake
Mol Cell Proteomics
Proteomic analysis of Legionella-containing phagosomes isolated from Dictyostelium
Int J Med Microbiol
Various bacterial pathogens and symbionts infect the amoeba Dictyostelium discoideum
Int J Med Microbiol
Legionella pathogenicity: genome structure, regulatory networks and the host cell response
Int J Med Microbiol
Legionella pneumophila adaptation to intracellular life and the host response: clues from genomics and transcriptomics
FEBS Lett
A Coronin7 homolog with functions in actin-driven processes
J Biol Chem
Growth of Legionella pneumophila in Dictyostelium discoideum: a novel system for genetic analysis of host–pathogen interactions
Trends Microbiol
Microorganisms resistant to free-living amoebae
Clin Microbiol Rev
Recent insights into host–pathogen interactions from Dictyostelium
Cell Microbiol
Environmental predators as models for bacterial pathogenesis
Environ Microbiol
Intracellular replication of Mycobacterium marinum within Dictyostelium discoideum: efficient replication in the absence of host coronin
Infect Immun
Dictyostelium discoideum: a new host model system for intracellular pathogens of the genus Legionella
Cell Microbiol
Immune-like phagocyte activity in the social amoeba
Science
The regulation of phagosome maturation in Dictyostelium
J Muscle Res Cell Motil
Chemotaxis: signalling the way forward
Nat Rev Mol Cell Biol
Calreticulin and calnexin in the endoplasmic reticulum are important for phagocytosis
EMBO J
Dynamic properties of Legionella-containing phagosomes in Dictyostelium amoebae
Cell Microbiol
High-resolution dissection of phagosome maturation reveals distinct membrane trafficking phases
Mol Biol Cell
Dictyostelium as host model for pathogenesis
Cell Microbiol
Dictyostelium discoideum: a model phagocyte and a model for host–pathogen interactions
The genome of the social amoeba Dictyostelium discoideum
Nature
Proteome analysis of Legionella vacuoles purified by magnetic immunoseparation reveals secretory and endosomal GTPases
Traffic
Dictyostelium transcriptional host cell response upon infection with Legionella
Cell Microbiol
Cited by (68)
Iron metabolism in the social amoeba Dictyostelium discoideum: A role for ferric chelate reductases
2022, European Journal of Cell BiologyEfficient inactivation of intracellular bacteria in dormant amoeba spores by FeP
2022, Journal of Hazardous MaterialsCitation Excerpt :Amoebae can also serve as vectors to facilitate the transmission of microorganisms such as bacteria, fungi, and even human pathogens (Abd et al., 2003; Balczun and Scheid, 2017; Guimaraes et al., 2016; Molmeret et al., 2005; Shi et al., 2021; Shu et al., 2021; Strassmann and Shu, 2017; Thomas et al., 2010; Tosetti et al., 2014). For example, Legionella pneumophila, notorious for Legionnaires' disease, can use amoebae as their hosts to replicate and transmit (Fields et al., 2002; Mengue et al., 2016; Steinert, 2011; Steinert and Heuner, 2005). A large number of pathogens have been reported in amoebae (Kahane et al., 2001; La Scola et al., 2003; Marciano-Cabral and Cabral, 2003; Nguyen-Viet et al., 2008; Raoult, 2010), which can survive within amoeba stably or transiently and remain virulent (Steinert, 2011; Wheat et al., 2014).
An observational study of phagocytes and Klebsiella pneumoniae relationships: different behaviors
2017, Microbes and InfectionCitation Excerpt :Their life cycle consists of two stages: an actively dividing trophozoite (feeding on bacteria, fungi, algae) and a dormant cyst. The FLA, including amoebae of the Acanthamoeba genus, may support bacterial growth in environmental ecosystems [7,8], the bacteria that can resist the amoebae microbicidal ability being named amoebae-resisting bacteria (ARB). These protozoa can also serve as reservoirs and/or vehicles for some microorganisms [9].
Symbiotic bacteria, immune-like sentinel cells, and the response to pathogens in a social amoeba
2023, Royal Society Open ScienceImaging Flow Cytometry of Legionella-Containing Vacuoles in Intact and Homogenized Wild-Type and Mutant Dictyostelium
2023, Methods in Molecular Biology