Cited by 215Legionella and Acanthamoeba researchMicrobial infections and disease researchBacterial Genetics and Biotechnology

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Intracellular Growth of Legionella pneumophila in Dictyostelium discoideum, a System for Genetic Analysis of Host-Pathogen Interactions

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Solomon, Jonathan M., Rupper, Adam, Cardelli, James A., Isberg, Ralph R.·2000·Infection and Immunity

DOI 10.1128/iai.68.5.2939-2947.2000PMC PMC97507

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Abstract

Conditions were established in which Legionella pneumophila, an intracellular bacterial pathogen, could replicate within the unicellular organism Dictyostelium discoideum. By several criteria,L. pneumophila grew by the same mechanism within D. discoideum as it does in amoebae and macrophages. Bacteria grew within membrane-bound vesicles associated with rough endoplasmic reticulum, and L. pneumophila dot/icm mutants, blocked for growth in macrophages and amoebae, also did not grow in D. discoideum. Internalized L. pneumophila avoided degradation by D. discoideum and showed evidence of reduced fusion with endocytic compartments. The ability of L. pneumophila to grow within D. discoideum depended on the growth state of the cells.D. discoideum grown as adherent monolayers was susceptible to L. pneumophila infection and to contact-dependent cytotoxicity during high-multiplicity infections, whereas D. discoideum grown in suspension was relatively resistant to cytotoxicity and did not support intracellular growth. Some known D. discoideum mutants were examined for their effect on growth of L. pneumophila. The coronin mutant and the myoA/B double myosin I mutant were more permissive than wild-type strains for intracellular growth. Growth of L. pneumophila in a G β mutant was slightly reduced compared to the parent strain. This work demonstrates the usefulness of the L. pneumophila-D. discoideum system for genetic analysis of host-pathogen interactions.

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“Interestingly, one of the main sources of nutrients comes from Legionella pneumophila, a Gram-negative bacterium that causes a pneumonia referred to as Legionnaires’ disease in humans (4).”
Background
Characterization of aLegionella pneumophila relAInsertion Mutant and Roles of RelA and RpoS in Virulence Gene Expression
Zusman, T., Gal‐Mor, O., & Segal, G. (2002) · Journal of Bacteriology · doi:10.1128/jb.184.1.67-75.2002 · Cited by 106
“castellanii (41) and Dictyostelium discoideum (43).”
Packaging of Live Legionella pneumophila into Pellets Expelled by Tetrahymena spp. Does Not Require Bacterial Replication and Depends on a Dot/Icm-Mediated Survival Mechanism
Berk, S. G., Faulkner, G., Garduño, E., Joy, M. C., Ortiz-Jiménez, M. A., & Garduño, R. A. (2008) · Applied and Environmental Microbiology · doi:10.1128/aem.01214-07 · Cited by 99
“pneumophila requires a functional Dot/Icm system (21, 48), a type IV secretion apparatus that allegedly delivers effector proteins required for phagocytosis-invasion, recruitment of phosphatidylinositol-4 phosphate, and initiation of intraamoebal growth, as determined in Dictyostelium discoideum (27, 33, 52, 57).”
Background
Proteomics Fingerprinting of Phagosome Maturation and Evidence for the Role of a Gα during Uptake
Gotthardt, D., Blancheteau, V., Bosserhoff, A., Ruppert, T., Delorenzi, M., & Soldati, T. (2006) · Molecular & Cellular Proteomics · doi:10.1074/mcp.m600113-mcp200 · Cited by 98
“human pathogens (17) including Legionella (18, 19), Mycobacterium (20), and Pseudomonas aeruginosa (21, 22).”
Background
Formation of the Legionella-containing vacuole: phosphoinositide conversion, GTPase modulation and ER dynamics
Steiner, B., Weber, S., & Hilbi, H. (2017) · International Journal of Medical Microbiology · doi:10.1016/j.ijmm.2017.08.004 · Cited by 98
Chapter 6 Phagocytosis and Host–Pathogen Interactions in Dictyostelium with a Look at Macrophages
Bozzaro, S., Bucci, C., & Steinert, M. (2008) · International review of cytology · doi:10.1016/s1937-6448(08)01206-9 · Cited by 96
“…that a few bacteria were pathogenic for Dictyostelium , the system has emerged as a suitable experimental model for bacterial infections only in recent years, the first two pioneering reports, both with Legionella pneumophila , being only 8 years old (Hagele et al. , 2000; Solomon et al. , 2000).”
Influential
Function and Mechanism of Action of Dictyostelium Nramp1 (Slc11a1) in Bacterial Infection
Peracino, B., Wagner, C., Balest, A., Balbo, A., Pergolizzi, B., Noegel, A. A., Steinert, M., & Bozzaro, S. (2006) · Traffic · doi:10.1111/j.1600-0854.2005.00356.x · Cited by 96
“The medium is a half-starving medium, which does not allow cell or bacterial growth, but inhibits cell aggregation over the infection period (35,36).”
Simple system – substantial share: The use of Dictyostelium in cell biology and molecular medicine
Müller‐Taubenberger, A., Kortholt, A., & Eichinger, L. (2012) · European Journal of Cell Biology · doi:10.1016/j.ejcb.2012.10.003 · Cited by 96
“Two groups independently demonstrated more than twenty years later that Dictyostelium can be infected with Legionella pneumophila (Hägele et al., 2000; Solomon et al., 2000).”
Dictyostelium Finds New Roles to Model
Williams, J. G. (2010) · Genetics · doi:10.1534/genetics.110.119297 · Cited by 95
“Dictyostelium is susceptible to Legionella infection, LCVs are formed, and some Legionella mutant strains that are avirulent for humans are avirulent for Dictyostelium (Solomon et al. 2000).”
Background
LidA, a Translocated Substrate of the Legionella pneumophila Type IV Secretion System, Interferes with the Early Secretory Pathway
Derré, I., & Isberg, R. R. (2005) · Infection and Immunity · doi:10.1128/iai.73.7.4370-4380.2005 · Cited by 93
Self-citation
Pathogen–host interactions in Dictyostelium, Legionella, Mycobacterium and other pathogens
Steinert, M. (2010) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2010.11.003 · Cited by 94
Regulation of phagocytosis and endo-phagosomal trafficking pathways in Dictyostelium discoideum
Rupper, A., & Cardelli, J. (2001) · Biochimica et Biophysica Acta (BBA) - General Subjects · doi:10.1016/s0304-4165(01)00106-4 · Cited by 103
Self-citation
Proteomic analysis of Legionella-containing phagosomes isolated from Dictyostelium
Shevchuk, O., Batzilla, C. F., Hägele, S., Kusch, H., Engelmann, S., Hecker, M., Haas, A., Heuner, K., Glöckner, G., & Steinert, M. (2009) · International Journal of Medical Microbiology · doi:10.1016/j.ijmm.2009.03.006 · Cited by 88
Characterization of IcmF of the type VI secretion system in an avian pathogenic Escherichia coli (APEC) strain
de Pace, F., de Paiva, J. B., Nakazato, G., Lancellotti, M., Sircili, M. P., Stehling, E. G., da Silveira, W. D., & Sperandio, V. (2011) · Microbiology · doi:10.1099/mic.0.050005-0 · Cited by 86
“T6SS components are encoded within clusters of genes that were initially characterized as IAHP (IcmF-associated homologous proteins), because all of them contained a gene encoding an IcmF-like (intracellular multiplication factor) component that was first reported and described in Legionella pneumophila, where it is c…”
Background
Development and evaluation of a Taqman duplex real-time PCR quantification method for reliable enumeration of Legionella pneumophila in water samples
Behets, J., Declerck, P., Delaedt, Y., Creemers, B., & Ollevier, F. (2006) · Journal of Microbiological Methods · doi:10.1016/j.mimet.2006.07.002 · Cited by 83
Invertebrates as animal models forStaphylococcus aureuspathogenesis: a window into host–pathogen interaction
GarcÃa-Lara, J., Needham, A. J., & Foster, S. J. (2004) · FEMS Immunology & Medical Microbiology · doi:10.1016/j.femsim.2004.11.003 · Cited by 79
“[82] Solomon, J.”
Influential
Burkholderia cepacia complex isolates survive intracellularly without replication within acidic vacuoles of Acanthamoeba polyphaga
Lamothe, J., Thyssen, S. M., & Valvano, M. A. (2004) · Cellular Microbiology · doi:10.1111/j.1462-5822.2004.00424.x · Cited by 79
“This result is in agreement with a recent report indicating that L. pneumophila internalized in the free living Dictyostelium discoideum does not colocalize with a monoclonal antibody staining the VATPase (Solomon et al., 2000).”
BackgroundResult
Increasing Diversity within Chlamydiae
Corsaro, D., Valassina, M., & Venditti, D. (2003) · Critical Reviews in Microbiology · doi:10.1080/713610404 · Cited by 77
MavN is a Legionella pneumophila vacuole-associated protein required for efficient iron acquisition during intracellular growth
Isaac, D. T., Laguna, R. K., Valtz, N., & Isberg, R. R. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1511389112 · Cited by 72
“discoideum strain Ax4 was cultured as described (75), as were primary BMDMs (3).”
BackgroundSelf-citation
Dictyostelium discoideum strains lacking the RtoA protein are defective for maturation of the Legionella pneumophila replication vacuole
Li, Z., Solomon, J. M., & Isberg, R. R. (2005) · Cellular Microbiology · doi:10.1111/j.1462-5822.2004.00472.x · Cited by 72
“pneumophila as described previously (Solomon et al., 2000).”
BackgroundMethodInfluentialSelf-citation
Diverse protist grazers select for virulence-related traits in Legionella
Amaro, F., Wang, W., Gilbert, J. A., Anderson, O. R., & Shuman, H. A. (2015) · The ISME Journal · doi:10.1038/ismej.2014.248 · Cited by 73
“pneumophila replicates within and kills many phylogenetically diverse water and soil protists (Rowbotham, 1980; Fields, 1996; Solomon et al., 2000; Molmeret et al., 2005).”
Background
Bacterial Discrimination by Dictyostelid Amoebae Reveals the Complexity of Ancient Interspecies Interactions
Nasser, W., Santhanam, B., Miranda, E. R., Parikh, A., Juneja, K., Rot, G., Dinh, C., Chen, R., Zupan, B., Shaulsky, G., et al. (2013) · Current Biology · doi:10.1016/j.cub.2013.04.034 · Cited by 73
“discoideum has proven to be useful for studying aspects of host-pathogen interactions [3–5] and has been used to identify and study bacterial virulence factors [5–8].”
Calnexin, calreticulin and cytoskeleton-associated proteins modulate uptake and growth of Legionella pneumophila in Dictyostelium discoideum
Fajardo, M., Schleicher, M., Noegel, A., Bozzaro, S., Killinger, S., Heuner, K., Hacker, J., & Steinert, M. (2004) · Microbiology · doi:10.1099/mic.0.27111-0 · Cited by 73
Genome-wide transcriptional changes induced by phagocytosis or growth on bacteria in Dictyostelium
Sillo, A., Bloomfield, G., Balest, A., Balbo, A., Pergolizzi, B., Peracino, B., Skelton, J., Ivens, A., & Bozzaro, S. (2008) · BMC Genomics · doi:10.1186/1471-2164-9-291 · Cited by 69
RabD, aDictyosteliumRab14-related GTPase, regulates phagocytosis and homotypic phagosome and lysosome fusion
Harris, E. N., & Cardelli, J. A. (2002) · Journal of Cell Science · doi:10.1242/jcs.00050 · Cited by 70
“For instance, Legionella replicates and prevents phagosomelysosome fusion in Dictyostelium (Hagele et al., 2000; Solomon et al., 2000), mimicking the situation observed in mammalian cells (Roy et al., 1998).”
BackgroundSelf-citation
Amoebae as a tool to isolate new bacterial species, to discover new virulence factors and to study the host–pathogen interactions
Tosetti, N., Croxatto, A., & Greub, G. (2014) · Microbial Pathogenesis · doi:10.1016/j.micpath.2014.07.009 · Cited by 70
Surface Translocation byLegionella pneumophila: a Form of Sliding Motility That Is Dependent upon Type II Protein Secretion
Stewart, C. R., Rossier, O., & Cianciotto, N. P. (2008) · Journal of Bacteriology · doi:10.1128/jb.01531-08 · Cited by 68
“Since a variety of data indicate that the Dot/Icm and Lvh systems are expressed at 25 to 37°C (24, 96, 112 ), these results, along with those obtained from assaying the flagellum and pilus mutants, also indicate that the surface translocation defect of the L. pneumophila T2S mutants is not a nonspecific effect of a mu…”
Result
Inorganic polyphosphate in Dictyostelium discoideum : Influence on development, sporulation, and predation
Zhang, H., Gómez-García, M. R., Brown, M. R., & Kornberg, A. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0500023102 · Cited by 68
Use of aDictyosteliumModel for Isolation of Genetic Loci Associated with Phagocytosis and Virulence inKlebsiella pneumoniae
Pan, Y., Lin, T., Hsu, C., & Wang, J. (2010) · Infection and Immunity · doi:10.1128/iai.00906-10 · Cited by 66
“A Dictyostelium model has been used previously to study virulence in extracellular bacteria, such as Yersinia (50), Pseudomonas (2), and Vibrio (44), and in intracellular bacteria, such as Legionella (28, 48) and Mycobacterium (20, 41).”
Method
ER remodeling by the large GTPase atlastin promotes vacuolar growth of Legionella pneumophila
Steiner, B., Swart, A. L., Welin, A., Weber, S., Personnic, N., Kaech, A., Freyre, C. A. C., Ziegler, U., Klemm, R. W., & Hilbi, H. (2017) · EMBO Reports · doi:10.15252/embr.201743903 · Cited by 62
Evolution of the Arsenal of Legionella pneumophila Effectors To Modulate Protist Hosts
Best, A., & Kwaik, Y. A. (2018) · mBio · doi:10.1128/mbio.01313-18 · Cited by 67
Free-living freshwater amoebae differ in their susceptibility to the pathogenic bacteriumLegionella pneumophila
Dey, R., Bodennec, J., Mameri, M. R., & Pernin, P. (2008) · FEMS Microbiology Letters · doi:10.1111/j.1574-6968.2008.01387.x · Cited by 65
“…reported the multiplication of L. pneumophila within various protozoa such as amoebae, ciliates (Fields, 1996) or cellular slime mould Dictyostelium discoideum (Hagele et al., 2000; Solomon et al., 2000), which has led to free-living amoebae being considered as natural reservoirs for this pathogen.”
Background
Genetic Models in Pathogenesis
Pradel, E., & Ewbank, J. J. (2004) · Annual Review of Genetics · doi:10.1146/annurev.genet.38.072902.092528 · Cited by 64
The Frustrated Host Response to Legionella pneumophila Is Bypassed by MyD88-Dependent Translation of Pro-inflammatory Cytokines
Asrat, S., Dugan, A. S., & Isberg, R. R. (2014) · PLoS Pathogens · doi:10.1371/journal.ppat.1004229 · Cited by 63
Self-citation
Phylogenetic Reconstruction of the Legionella pneumophila Philadelphia-1 Laboratory Strains through Comparative Genomics
Rao, C., Benhabib, H., & Ensminger, A. W. (2013) · PLoS ONE · doi:10.1371/journal.pone.0064129 · Cited by 63
“pPpacS-EGFP is a 8946 bp non-integrating plasmid, generated by replacing the IPTG-inducible promoter in a mobA version of the pAM239 plasmid [56] with the native Legionella promoter upstream of the highly expressed gene, pacS.”
Background
Legionella pneumophila adaptation to intracellular life and the host response: Clues from genomics and transcriptomics
Jules, M., & Buchrieser, C. (2007) · FEBS Letters · doi:10.1016/j.febslet.2007.05.026 · Cited by 70
“pneumophila [58,62].”
Indispensable Role for the Eukaryotic-Like Ankyrin Domains of the Ankyrin B Effector ofLegionella pneumophilawithin Macrophages and Amoebae
Price, C. T. D., Khodor, S. A., Al‐Quadan, T., & Kwaik, Y. A. (2010) · Infection and Immunity · doi:10.1128/iai.01450-09 · Cited by 63
Multiple Legionella pneumophila Type II Secretion Substrates, Including a Novel Protein, Contribute to Differential Infection of the Amoebae Acanthamoeba castellanii, Hartmannella vermiformis, and Naegleria lovaniensis
Tyson, J. Y., Pearce, M. M., Vargas, P., Bagchi, S., Mulhern, B. J., & Cianciotto, N. P. (2013) · Infection and Immunity · doi:10.1128/iai.00045-13 · Cited by 60
Diversity of Free-Living Environmental Bacteria and Their Interactions With a Bactivorous Amoeba
Brock, D. A., Haselkorn, T. S., Garcia, J. R., Bashir, U., Douglas, T. E., Galloway, J., Brodie, F., Queller, D. C., & Strassmann, J. E. (2018) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2018.00411 · Cited by 59
“discoideum has been employed as amodel inmany host-pathogen studies (Solomon et al., 2000; Alibaud et al., 2008; Hagedorn et al., 2009; Jia et al., 2009; Hasselbring et al., 2011), and has recently been found to engage in symbiotic associations with bacteria throughout their life history (Brock et al.”
Background
Macrophage-Induced Genes ofLegionella pneumophila:Protection from Reactive Intermediates and Solute Imbalance during Intracellular Growth
Rankin, S., Li, Z., & Isberg, R. R. (2002) · Infection and Immunity · doi:10.1128/iai.70.7.3637-3648.2002 · Cited by 58
Self-citation
IcmF and DotU Are Required for Optimal Effector Translocation and Trafficking of the Legionella pneumophila Vacuole
VanRheenen, S. M., Duménil, G., & Isberg, R. R. (2004) · Infection and Immunity · doi:10.1128/iai.72.10.5972-5982.2004 · Cited by 58
“discoideum was infected as previously described (53).”
Self-citation
The Type VI Secretion System Modulates Flagellar Gene Expression and Secretion in Citrobacter freundii and Contributes to Adhesion and Cytotoxicity to Host Cells
Liu, L., Hao, S., Lan, R., Wang, G., Xiao, D., Sun, H., & Xu, J. (2015) · Infection and Immunity · doi:10.1128/iai.03071-14 · Cited by 56
Characterization of theicmHandicmFGenes Required forLegionella pneumophilaIntracellular Growth, Genes That Are Present in Many Bacteria Associated with Eukaryotic Cells
Zusman, T., Feldman, M., Halperin, E., & Segal, G. (2004) · Infection and Immunity · doi:10.1128/iai.72.6.3398-3409.2004 · Cited by 55
“As a consequence of all these features, the icm/dot genes were found to be essential for intracellular multiplication in all of the hosts examined: HL- 60- and U937-derived human macrophages (50, 67), murine bone marrow-derived macrophages (63), and the protozoan hosts Acanthamoeba castellanii (55) and Dictyostelium d…”
Detection of Protozoan Hosts for Legionella pneumophila in Engineered Water Systems by Using a Biofilm Batch Test
Valster, R. M., Wullings, B. A., & van der Kooij, D. (2010) · Applied and Environmental Microbiology · doi:10.1128/aem.00926-10 · Cited by 54
“(38, 44, 53), and Vahlkampfia jugosa (43); the slime mold Dictyostelium discoideum (20, 48); and two species of the ciliate genus Tetrahymena (15, 26) can serve as hosts for L.”
Background

Authors: Solomon, J. M., Rupper, A., Cardelli, J. A., & Isberg, R. R.
Affiliations: Tufts University (US)
Louisiana State University (US)
ORCID: Solomon, Jonathan M.
Isberg, Ralph R.
Venue: Infection and Immunity
Publisher: American Society for Microbiology
Published: 2000-05
Volume: 68
Issue: 5
Pages: 2939-2947
ISSN: 0019-9567 (ISSN-L)
1098-5522
DOI: 10.1128/iai.68.5.2939-2947.2000
PMC: PMC97507
OpenAlex: W2104752214
Cited by: 215
References: 59
Citations by year: 2026: 2 · 2025: 5 · 2024: 3 · 2023: 2 · 2022: 1 · 2021: 2 · 2020: 6 · 2019: 4 · 2018: 7 · 2017: 8 · 2016: 2 · 2015: 6 · 2014: 13 · 2013: 15 · 2012: 6
FWCI: 7.33
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: journals.asm.org/non-commercial-tdm-license (tdm)
Locations: Infection and Immunity (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Funders: University of Minnesota
University of Connecticut
Johns Hopkins University
Medical Research Council
National Institute of Diabetes and Digestive and Kidney Diseases (DK-39232)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Endocrinology › Legionella and Acanthamoeba research
Life Sciences › Immunology and Microbiology › Microbiology › Microbial infections and disease research
Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
Keywords: Legionella pneumophila, Dictyostelium discoideum, intracellular bacterial growth, host-pathogen interaction, Dot/Icm system, rough endoplasmic reticulum, membrane vesicles, endocytic compartments, G protein beta subunit
MeSH terms: Animals, Culture Media, Dictyostelium, Genes, Bacterial, Intracellular Fluid, Intracellular Membranes, Lysosomes, Membrane Proteins, Legionella pneumophila

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Intracellular Growth of Legionella pneumophila in Dictyostelium discoideum, a System for Genetic Analysis of Host-Pathogen Interactions

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