Abstract
Dictyostelid social amoebae such as Dictyostelium discoideum are facultative multicellular organisms that display a number of immune functions commonly found in animals. In the vegetative growth phase, solitary amoebae track and consume food bacteria that occur in their soil environment, and are also susceptible to intracellular bacterial pathogens including those that infect humans. Individual amoebae recognize microbe-associated molecular patterns (MAMPs) to distinguish between bacterial species and adjust their physiology to optimize feeding, but it is during multicellular development that this has been most clearly demonstrated. Starved D. discoideum amoebae aggregate to form mounds, migrating slugs, and spore-filled fruiting bodies in a stereotypical and regulated developmental process. Cell cooperation during multicellular development is maintained by an allorecognition system that ensures the benefits of this group survival mechanism accrues to genetically related amoebae. Allorecognition is accomplished through a cell surface receptor–ligand pair comprised of immunoglobulin (Ig)-repeat ectodomains, and signaling through the receptor acts as a checkpoint for the transition from unicellular to multicellular life. During development, D. discoideum produces innate immune cells capable of clearing interstitial bacteria from migrating slugs and some isolates also harbor specific bacterial species as beneficial endosymbionts. The innate immune cells, when stimulated by bacteria or bacterial lipopolysaccharide, kill bacteria by producing extracellular DNA-based antimicrobial nets or extracellular traps (ETs). As with human innate immune cells, ET production requires reactive oxygen species (ROS) produced by nicotinamide adenine dinucleotide phosphate (NADPH) oxidases and Toll/interleukin-1 receptor (TIR) domain-based signaling that triggers ET release. The Dictyostelid social amoebae are part of the monophyletic clade of the Amoebozoa that have achieved multicellularity, so they provide useful comparisons to other species of the Unikont supergroup that highlight the evolutionary pressures that shaped extant immune systems over the past billion years.
This is a preview of subscription content, log in via an institution to check access.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Alibaud L, Kohler T, Coudray A, Prigent-Combaret C, Bergeret E, Perrin J, Benghezal M, Reimmann C, Gauthier Y, van Delden C, Attree I, Fauvarque MO, Cosson P (2008) Pseudomonas aeruginosa virulence genes identified in a Dictyostelium host model. Cell Microbiol 10(3):729–740. https://doi.org/10.1111/j.1462-5822.2007.01080.x. CMI1080 [pii]
Anjard C, Loomis WF (2002) Evolutionary analyses of ABC transporters of Dictyostelium discoideum. Eukaryot Cell 1(4):643–652
Anjard C, Loomis WF (2005) Peptide signaling during terminal differentiation of Dictyostelium. Proc Natl Acad Sci U S A 102(21):7607–7611
Anjard C, Loomis WF (2006) GABA induces terminal differentiation of Dictyostelium through a GABAB receptor. Development 133(11):2253–2261
Anjard C, Loomis WF (2008) Cytokinins induce sporulation in Dictyostelium. Development 135(5):819–827. https://doi.org/10.1242/dev.018051. dev.018051 [pii]
Athamna A, Ofek I, Keisari Y, Markowitz S, Dutton GG, Sharon N (1991) Lectinophagocytosis of encapsulated Klebsiella pneumoniae mediated by surface lectins of guinea pig alveolar macrophages and human monocyte-derived macrophages. Infect Immun 59(5):1673–1682
Bakthavatsalam D, Gomer RH (2010) The secreted proteome profile of developing Dictyostelium discoideum cells. Proteomics 10(13):2556–2559. https://doi.org/10.1002/pmic.200900516
Balest A, Peracino B, Bozzaro S (2011) Legionella pneumophila infection is enhanced in a RacH-null mutant of Dictyostelium. Commun Integr Biol 4(2):194–197. https://doi.org/10.4161/cib.4.2.14381. 1942-0889-4-2-14 [pii]
Bandyopadhyay P, Xiao H, Coleman HA, Price-Whelan A, Steinman HM (2004) Icm/dot-independent entry of Legionella pneumophila into amoeba and macrophage hosts. Infect Immun 72(8):4541–4551. https://doi.org/10.1128/IAI.72.8.4541-4551.2004. 72/8/4541 [pii]
Bapteste E, Brinkmann H, Lee JA, Moore DV, Sensen CW, Gordon P, Durufle L, Gaasterland T, Lopez P, Muller M, Philippe H (2002) The analysis of 100 genes supports the grouping of three highly divergent amoebae: Dictyostelium, Entamoeba, and Mastigamoeba. Proc Natl Acad Sci U S A 99(3):1414–1419. https://doi.org/10.1073/pnas.032662799. 99/3/1414 [pii]
Barclay AN (2003) Membrane proteins with immunoglobulin-like domains – a master superfamily of interaction molecules. Semin Immunol 15(4):215–223
Benabentos R, Hirose S, Sucgang R, Curk T, Katoh M, Ostrowski EA, Strassmann JE, Queller DC, Zupan B, Shaulsky G, Kuspa A (2009) Polymorphic members of the lag gene family mediate kin discrimination in Dictyostelium. Curr Biol 19(7):567–572. https://doi.org/10.1016/j.cub.2009.02.037. S0960-9822(09)00747-7 [pii]
Benghezal M, Fauvarque MO, Tournebize R, Froquet R, Marchetti A, Bergeret E, Lardy B, Klein G, Sansonetti P, Charette SJ, Cosson P (2006) Specific host genes required for the killing of Klebsiella bacteria by phagocytes. Cell Microbiol 8(1):139–148. https://doi.org/10.1111/j.1462-5822.2005.00607.x
Bianchi M, Hakkim A, Brinkmann V, Siler U, Seger RA, Zychlinsky A, Reichenbach J (2009) Restoration of NET formation by gene therapy in CGD controls aspergillosis. Blood 114(13):2619–2622. https://doi.org/10.1182/blood-2009-05-221606
Boehm T (2006) Quality control in self/nonself discrimination. Cell 125(5):845–858
Boulais J, Trost M, Landry CR, Dieckmann R, Levy ED, Soldati T, Michnick SW, Thibault P, Desjardins M (2010) Molecular characterization of the evolution of phagosomes. Mol Syst Biol 6:423. https://doi.org/10.1038/msb.2010.80
Bozzaro S (2013) The model organism Dictyostelium discoideum. Methods Mol Biol 983:17–37. https://doi.org/10.1007/978-1-62703-302-2_2
Bozzaro S, Eichinger L (2011) The professional phagocyte Dictyostelium discoideum as a model host for bacterial pathogens. Curr Drug Targets 12(7):942–954. doi:BSP/CDT/E-Pub/00254 [pii]
Bozzaro S, Peracino B, Eichinger L (2013) Dictyostelium host response to legionella infection: strategies and assays. Methods Mol Biol 954:417–438. https://doi.org/10.1007/978-1-62703-161-5_26
Brinkmann V, Zychlinsky A (2007) Beneficial suicide: why neutrophils die to make NETs. Nat Rev Microbiol 5(8):577–582. https://doi.org/10.1038/nrmicro1710
Brinkmann V, Reichard U, Goosmann C, Fauler B, Uhlemann Y, Weiss DS, Weinrauch Y, Zychlinsky A (2004) Neutrophil extracellular traps kill bacteria. Science 303(5663):1532–1535. https://doi.org/10.1126/science.1092385. 303/5663/1532 [pii]
Brock DA, Douglas TE, Queller DC, Strassmann JE (2011) Primitive agriculture in a social amoeba. Nature 469(7330):393–396. https://doi.org/10.1038/nature09668
Brock DA, Read S, Bozhchenko A, Queller DC, Strassmann JE (2013) Social amoeba farmers carry defensive symbionts to protect and privatize their crops. Nat Commun 4:2385. https://doi.org/10.1038/ncomms3385
Brock DA, Callison WE, Strassmann JE, Queller DC (2016) Sentinel cells, symbiotic bacteria and toxin resistance in the social amoeba Dictyostelium discoideum. Proc Biol Sci/R Soc 283(1829). https://doi.org/10.1098/rspb.2015.2727
Buracco S, Peracino B, Cinquetti R, Signoretto E, Vollero A, Imperiali F, Castagna M, Bossi E, Bozzaro S (2015) Dictyostelium Nramp1, which is structurally and functionally similar to mammalian DMT1 transporter, mediates phagosomal iron efflux. J Cell Sci 128(17):3304–3316. https://doi.org/10.1242/jcs.173153
Cabral M, Anjard C, Malhotra V, Loomis WF, Kuspa A (2010) Unconventional secretion of AcbA in Dictyostelium discoideum through a vesicular intermediate. Eukaryot Cell 9(7):1009–1017. https://doi.org/10.1128/EC.00337-09. EC.00337-09 [pii]
Carilla-Latorre S, Calvo-Garrido J, Bloomfield G, Skelton J, Kay RR, Ivens A, Martinez JL, Escalante R (2008) Dictyostelium transcriptional responses to Pseudomonas aeruginosa: common and specific effects from PAO1 and PA14 strains. BMC Microbiol 8:109. https://doi.org/10.1186/1471-2180-8-109. 1471-2180-8-109 [pii]
Casadevall A, Pirofski LA (2007) Accidental virulence, cryptic pathogenesis, martians, lost hosts, and the pathogenicity of environmental microbes. Eukaryot Cell 6(12):2169–2174. https://doi.org/10.1128/EC.00308-07. EC.00308-07 [pii]
Chen ZH, Schaap P (2015) Secreted cyclic-di-GMP induces stalk cell differentiation in the eukaryote Dictyostelium discoideum. J Bacteriol. https://doi.org/10.1128/jb.00321-15
Chen G, Zhuchenko O, Kuspa A (2007) Immune-like phagocyte activity in the social amoeba. Science 317:678–681
Chen G, Wang J, Xu X, Wu X, Piao R, Siu CH (2013) TgrC1 mediates cell-cell adhesion by interacting with TgrB1 via mutual IPT/TIG domains during development of Dictyostelium discoideum. Biochem J 452(2):259–269. https://doi.org/10.1042/bj20121674
Chen G, Xu X, Wu X, Thomson A, Siu CH (2014) Assembly of the TgrB1-TgrC1 cell adhesion complex during Dictyostelium discoideum development. Biochem J 459(2):241–249. https://doi.org/10.1042/bj20131594
Chia CP (1996) A 130-kDa plasma membrane glycoprotein involved in Dictyostelium phagocytosis. Exp Cell Res 227(2):182–189. https://doi.org/10.1006/excr.1996.0265. S0014-4827(96)90265-7 [pii]
Chia CP, Gomathinayagam S, Schmaltz RJ, Smoyer LK (2005) Glycoprotein gp130 of dictyostelium discoideum influences macropinocytosis and adhesion. Mol Biol Cell 16(6):2681–2693. https://doi.org/10.1091/mbc.E04-06-0483. E04-06-0483 [pii]
Cianciotto NP, Fields BS (1992) Legionella pneumophila mip gene potentiates intracellular infection of protozoa and human macrophages. Proc Natl Acad Sci U S A 89(11):5188–5191
Cooper DNW, Haywood-Reid PL, Springer WR, Barondes SH (1986) Bacterial glycoconjugates are natural ligands for the carbohydrate binding site of discoidin I and influence its cellular compartmentalization. Dev Biol 114:416–425
Cosson P, Lima WC (2014) Intracellular killing of bacteria: is Dictyostelium a model macrophage or an alien? Cell Microbiol 16(6):816–823. https://doi.org/10.1111/cmi.12291
Cosson P, Soldati T (2008) Eat, kill or die: when amoeba meets bacteria. Curr Opin Microbiol 11(3):271–276. https://doi.org/10.1016/j.mib.2008.05.005
Curtis TP, Sloan WT, Scannell JW (2002) Estimating prokaryotic diversity and its limits. Proc Natl Acad Sci U S A 99(16):10494–10499. https://doi.org/10.1073/pnas.142680199. 142680199 [pii]
Danelishvili L, Wu M, Stang B, Harriff M, Cirillo SL, Cirillo JD, Bildfell R, Arbogast B, Bermudez LE (2007) Identification of Mycobacterium avium pathogenicity island important for macrophage and amoeba infection. Proc Natl Acad Sci U S A 104(26):11038–11043. https://doi.org/10.1073/pnas.0610746104. 0610746104 [pii]
De Tomaso AW, Nyholm SV, Palmeri KJ, Ishizuka KJ, Ludington WB, Mitchel K, Weissman IL (2005) Isolation and characterization of a protochordate histocompatibility locus. Nature 438(7067):454–459
Dickinson DJ, Nelson WJ, Weis WI (2011) A polarized epithelium organized by beta- and alpha-catenin predates cadherin and metazoan origins. Science 331(6022):1336–1339. https://doi.org/10.1126/science.1199633
Dinh C, Farinholt T, Hirose S, Zhuchenko O, Kuspa A (2018) Lectins modulate the microbiota of social amoebae. Science (in press)
DiSalvo S, Haselkorn TS, Bashir U, Jimenez D, Brock DA, Queller DC, Strassmann JE (2015) Burkholderia bacteria infectiously induce the proto-farming symbiosis of Dictyostelium amoebae and food bacteria. Proc Natl Acad Sci U S A 112(36):E5029–E5037. https://doi.org/10.1073/pnas.1511878112
Dorer MS, Isberg RR (2006) Non-vertebrate hosts in the analysis of host-pathogen interactions. Microbes Infect 8(6):1637–1646. https://doi.org/10.1016/j.micinf.2005.11.020. S1286-4579(06)00011-6 [pii]
Doyle RJ, Birdsell DC (1972) Interaction of concanavalin A with the cell wall of Bacillus subtilis. J Bacteriol 109(2):652–658
Du Q, Kawabe Y, Schilde C, Chen ZH, Schaap P (2015) The evolution of aggregative multicellularity and cell-cell communication in the Dictyostelia. J Mol Biol 427(23):3722–3733. https://doi.org/10.1016/j.jmb.2015.08.008
Dynes JL, Clark AM, Shaulsky G, Kuspa A, Loomis WF, Firtel RA (1994) LagC is required for cell-cell interactions that are essential for cell-type differentiation in Dictyostelium. Genes Dev 8:948–958
Eichinger L (2012) Model organisms to study host - pathogen interaction: prerequisites for the identification of novel drug targets. Curr Drug Targets 12(7):934–935. doi: BSP/CDT/E-Pub/00252 [pii]
Eichinger L, Pachebat JA, Glockner G, Rajandream MA, Sucgang R, Berriman M, Song J, Olsen R, Szafranski K, Xu Q, Tunggal B, Kummerfeld S, Madera M, Konfortov BA, Rivero F, Bankier AT, Lehmann R, Hamlin N, Davies R, Gaudet P, Fey P, Pilcher K, Chen G, Saunders D, Sodergren E, Davis P, Kerhornou A, Nie X, Hall N, Anjard C, Hemphill L, Bason N, Farbrother P, Desany B, Just E, Morio T, Rost R, Churcher C, Cooper J, Haydock S, van Driessche N, Cronin A, Goodhead I, Muzny D, Mourier T, Pain A, Lu M, Harper D, Lindsay R, Hauser H, James K, Quiles M, Madan Babu M, Saito T, Buchrieser C, Wardroper A, Felder M, Thangavelu M, Johnson D, Knights A, Loulseged H, Mungall K, Oliver K, Price C, Quail MA, Urushihara H, Hernandez J, Rabbinowitsch E, Steffen D, Sanders M, Ma J, Kohara Y, Sharp S, Simmonds M, Spiegler S, Tivey A, Sugano S, White B, Walker D, Woodward J, Winckler T, Tanaka Y, Shaulsky G, Schleicher M, Weinstock G, Rosenthal A, Cox EC, Chisholm RL, Gibbs R, Loomis WF, Platzer M, Kay RR, Williams J, Dear PH, Noegel AA, Barrell B, Kuspa A (2005) The genome of the social amoeba Dictyostelium discoideum. Nature 435(7038):43–57. https://doi.org/10.1038/nature03481. nature03481 [pii]
Ennis HL, Dao DN, Pukatzki SU, Kessin RH (2000) Dictyostelium amoebae lacking an F-box protein form spores rather than stalk in chimeras with wild type. Proc Natl Acad Sci U S A 97:3292–3297
Ennis HL, Dao DN, Wu MY, Kessin RH (2003) Mutation of the Dictyostelium fbxA gene affects cell-fate decisions and spatial patterning. Protist 154:419–429
Farbrother P, Wagner C, Na J, Tunggal B, Morio T, Urushihara H, Tanaka Y, Schleicher M, Steinert M, Eichinger L (2006) Dictyostelium transcriptional host cell response upon infection with Legionella. Cell Microbiol 8(3):438–456. https://doi.org/10.1111/j.1462-5822.2005.00633.x. CMI633 [pii]
Fields BS (1996) The molecular ecology of Legionellae. Trends Microbiol 4(7):286–290. doi: 0966842X9610041X [pii]
Fortunato A, Queller DC, Strassmann JE (2003a) A linear dominance hierarchy among clones in chimeras of the social amoeba Dictyostelium discoideum. J Evol Biol 16:438–445
Fortunato A, Strassmann JE, Santorelli L, Queller DC (2003b) Co-occurrence in nature of different clones of the social amoeba, Dictyostelium discoideum. Mol Ecol 12(4):1031–1038
Foster KR, Shaulsky G, Strassmann JE, Queller DC, Thompson CR (2004) Pleiotropy as a mechanism to stabilize cooperation. Nature 431(7009):693–696
Fritz-Laylin LK, Prochnik SE, Ginger ML, Dacks JB, Carpenter ML, Field MC, Kuo A, Paredez A, Chapman J, Pham J, Shu S, Neupane R, Cipriano M, Mancuso J, Tu H, Salamov A, Lindquist E, Shapiro H, Lucas S, Grigoriev IV, Cande WZ, Fulton C, Rokhsar DS, Dawson SC (2010) The genome of Naegleria gruberi illuminates early eukaryotic versatility. Cell 140(5):631–642. https://doi.org/10.1016/j.cell.2010.01.032
Gabius HJ, Springer WR, Barondes SH (1985) Receptor for the cell binding site of discoidin. Cell 42:449–456
Gao LY, Harb OS, Abu Kwaik Y (1997) Utilization of similar mechanisms by Legionella pneumophila to parasitize two evolutionarily distant host cells, mammalian macrophages and protozoa. Infect Immun 65(11):4738–4746
Geltosky J, Weseman J, Bakke A, Lerner R (1979) Identification of a cell surface glycoprotein involved in cell aggregation in Dictyostelium discoideum. Cell 18:391–398
Gerstenmaier L, Pilla R, Herrmann L, Herrmann H, Prado M, Villafano GJ, Kolonko M, Reimer R, Soldati T, King JS, Hagedorn M (2015) The autophagic machinery ensures nonlytic transmission of mycobacteria. Proc Natl Acad Sci U S A 112(7):E687–E692. https://doi.org/10.1073/pnas.1423318112
Gilbert OM, Foster KR, Mehdiabadi NJ, Strassmann JE, Queller DC (2007) High relatedness maintains multicellular cooperation in a social amoeba by controlling cheater mutants. Proc Natl Acad Sci U S A 104(21):8913–8917
Goldmann O, Medina E (2012) The expanding world of extracellular traps: not only neutrophils but much more. Front Immunol 3:420. https://doi.org/10.3389/fimmu.2012.00420
Greub G, La Scola B, Raoult D (2004) Amoebae-resisting bacteria isolated from human nasal swabs by amoebal coculture. Emerg Infect Dis 10(3):470–477. https://doi.org/10.3201/eid1003.020792
Grimson MJ, Coates JC, Reynolds JP, Shipman M, Blanton RL, Harwood AJ (2000) Adherens junctions and beta-catenin-mediated cell signalling in a non-metazoan organism. Nature 408:727–731
Grubhoffer L, Hypsa V, Volf P (1997) Lectins (hemagglutinins) in the gut of the important disease vectors. Parasite 4(3):203–216
Gruenheit N, Parkinson K, Stewart B, Howie JA, Wolf JB, Thompson CR (2017) A polychromatic ‘greenbeard’ locus determines patterns of cooperation in a social amoeba. Nat Commun 8:14171. https://doi.org/10.1038/ncomms14171
Gust AA, Willmann R, Desaki Y, Grabherr HM, Nurnberger T (2012) Plant LysM proteins: modules mediating symbiosis and immunity. Trends Plant Sci 17(8):495–502. https://doi.org/10.1016/j.tplants.2012.04.003
Harrison CF, Chiriano G, Finsel I, Manske C, Hoffmann C, Steiner B, Kranjc A, Patthey-Vuadens O, Kicka S, Trofimov V, Ouertatani-Sakouhi H, Soldati T, Scapozza L, Hilbi H (2015) Amoebae-based screening reveals a novel family of compounds restricting intracellular Legionella pneumophila. ACS Infect Dis 1(7):327–338. https://doi.org/10.1021/acsinfecdis.5b00002
Hasselbring BM, Patel MK, Schell MA (2011) Dictyostelium discoideum as a model system for identification of Burkholderia pseudomallei virulence factors. Infect Immun 79(5):2079–2088. https://doi.org/10.1128/IAI.01233-10. IAI.01233-10 [pii]
Heidel AJ, Lawal HM, Felder M, Schilde C, Helps NR, Tunggal B, Rivero F, John U, Schleicher M, Eichinger L, Platzer M, Noegel AA, Schaap P, Glockner G (2011) Phylogeny-wide analysis of social amoeba genomes highlights ancient origins for complex intercellular communication. Genome Res 21(11):1882–1891. https://doi.org/10.1101/gr.121137.111
Hirose S, Benabentos R, Ho HI, Kuspa A, Shaulsky G (2011) Self-recognition in social amoebae is mediated by allelic pairs of tiger genes. Science 333(6041):467–470. https://doi.org/10.1126/science.1203903. science.1203903 [pii]
Hirose S, Santhanam B, Katoh-Kurosawa M, Shaulsky G, Kuspa A (2015) Allorecognition, via TgrB1 and TgrC1, mediates the transition from unicellularity to multicellularity in the social amoeba Dictyostelium discoideum. Development 142(20):3561–3570. https://doi.org/10.1242/dev.123281
Hirose S, Chen G, Kuspa A, Shaulsky G (2017) The polymorphic proteins TgrB1 and TgrC1 function as a ligand-receptor pair in Dictyostelium allorecognition. J Cell Sci 130(23):4002–4012. https://doi.org/10.1242/jcs.208975
Hirsch JG (1959) Immunity to infectious diseases: review of some concepts of Metchnikoff. Bacteriol Rev 23:48–60
Ho HI, Shaulsky G (2015) Temporal regulation of kin recognition maintains recognition-cue diversity and suppresses cheating. Nat Commun 6:7144. https://doi.org/10.1038/ncomms8144
Ho HI, Hirose S, Kuspa A, Shaulsky G (2013) Kin recognition protects cooperators against cheaters. Curr Biol 23(16):1590–1595. https://doi.org/10.1016/j.cub.2013.06.049
Hughes AL, Nei M (1988) Pattern of nucleotide substitution at major histocompatibility complex class I loci reveals overdominant selection. Nature 335(6186):167–170
Katoh M, Shaw C, Xu Q, Van Driessche N, Morio T, Kuwayama H, Obara S, Urushihara H, Tanaka Y, Shaulsky G (2004) An orderly retreat: dedifferentiation is a regulated process. Proc Natl Acad Sci U S A 101(18):7005–7010. https://doi.org/10.1073/pnas.0306983101. 0306983101 [pii]
Katoh M, Chen G, Roberge E, Shaulsky G, Kuspa A (2007) Developmental commitment in Dictyostelium discoideum. Eukaryot Cell 6(11):2038–2045. https://doi.org/10.1128/EC.00223-07. EC.00223-07 [pii]
Kawabe Y, Schilde C, Du Q, Schaap P (2015) A conserved signalling pathway for amoebozoan encystation that was co-opted for multicellular development. Sci Rep 5:9644. https://doi.org/10.1038/srep09644
Kessin RH (2001) Dictyostelium – evolution, cell biology, and the development of multicellularity. Cambridge Univ. Press, Cambridge, UK
Koonin EV (2010) The origin and early evolution of eukaryotes in the light of phylogenomics. Genome Biol 11(5):209. https://doi.org/10.1186/gb-2010-11-5-209
Kuzdzal-Fick JJ, Fox SA, Strassmann JE, Queller DC (2011) High relatedness is necessary and sufficient to maintain multicellularity in Dictyostelium. Science 334(6062):1548–1551. https://doi.org/10.1126/science.1213272
Le Bouguenec C (2005) Adhesins and invasins of pathogenic Escherichia coli. Int J Med Microbiol 295(6–7):471–478
Leiba J, Sabra A, Bodinier R, Marchetti A, Lima WC, Melotti A, Perrin J, Burdet F, Pagni M, Soldati T, Lelong E, Cosson P (2017) Vps13F links bacterial recognition and intracellular killing in Dictyostelium. Cell Microbiol. https://doi.org/10.1111/cmi.12722
Li CL, Santhanam B, Webb AN, Zupan B, Shaulsky G (2016) Gene discovery by chemical mutagenesis and whole-genome sequencing in Dictyostelium. Genome Res 26(9):1268–1276. https://doi.org/10.1101/gr.205682.116
Lima WC, Lelong E, Cosson P (2011) What can Dictyostelium bring to the study of pseudomonas infections? Semin Cell Dev Biol 22(1):77–81. https://doi.org/10.1016/j.semcdb.2010.11.006
Lima WC, Balestrino D, Forestier C, Cosson P (2014) Two distinct sensing pathways allow recognition of Klebsiella pneumoniae by Dictyostelium amoebae. Cell Microbiol 16(3):311–323. https://doi.org/10.1111/cmi.12226
Liu Z (2013) Genetic and biochemical analysis of the response of Dictyostelium discoideum to bacteria. Doctoral dissertation. Baylor College of Medicine, Houston
Liu Z, Nam EA, Yun S, Qin J, Shaulsky G, Kuspa A (2018) A component of the TirA bacterial response pathway in Dictyostelium discoideum, EpdR, that is related to bacterial exopolysaccharide depolymerases. (submitted)
Loomis WF, Smith DW (1990) Molecular phylogeny of Dictyostelium dscoideum by protein sequence comparison. Proc Natl Acad Sci U S A 87:9093–9097
Ludtmann MH, Otto GP, Schilde C, Chen ZH, Allan CY, Brace S, Beesley PW, Kimmel AR, Fisher P, Killick R, Williams RS (2014) An ancestral non-proteolytic role for presenilin proteins in multicellular development of the social amoeba Dictyostelium discoideum. J Cell Sci 127(Pt 7):1576–1584. https://doi.org/10.1242/jcs.140939
MacIntyre DL, Miyata ST, Kitaoka M, Pukatzki S (2010) The Vibrio cholerae type VI secretion system displays antimicrobial properties. Proc Natl Acad Sci U S A 107(45):19520–19524. https://doi.org/10.1073/pnas.1012931107. 1012931107 [pii]
Mathieu SV, Aragao KS, Imberty A, Varrot A (2010) Discoidin I from Dictyostelium discoideum and interactions with oligosaccharides: specificity, affinity, crystal structures, and comparison with discoidin II. J Mol Biol 400(3):540–554. https://doi.org/10.1016/j.jmb.2010.05.042
Mege RM, Ishiyama N (2017) Integration of cadherin adhesion and cytoskeleton at adherens junctions. Cold Spring Harb Perspect Biol 9(5). https://doi.org/10.1101/cshperspect.a028738
Mehdiabadi NJ, Jack CN, Farnham TT, Platt TG, Kalla SE, Shaulsky G, Queller DC, Strassmann JE (2006) Social evolution: kin preference in a social microbe. Nature 442(7105):881–882
Metchnikoff E (1905) Immunity in infective diseases. Cambridge University Press, London
Miyata ST, Kitaoka M, Brooks TM, McAuley SB, Pukatzki S (2011) Vibrio cholerae requires the type VI secretion system virulence factor VasX to kill Dictyostelium discoideum. Infect Immun 79(7):2941–2949. https://doi.org/10.1128/IAI.01266-10. IAI.01266-10 [pii]
Molmeret M, Horn M, Wagner M, Santic M, Abu Kwaik Y (2005) Amoebae as training grounds for intracellular bacterial pathogens. Appl Environ Microbiol 71(1):20–28. https://doi.org/10.1128/AEM.71.1.20-28.2005. 71/1/20 [pii]
Nasser W, Santhanam B, Miranda R, Parikh A, Juneja K, Rot G, Dinh C, Chen R, Zupan B, Shaulsky G, Kuspa A (2013) Bacterial discrimination by Dictyostelid amoebae reveals the complexity of ancient interspecies interactions. Curr Biol 23(10):862–872
Ofek I, Sharon N (1988) Lectinophagocytosis: a molecular mechanism of recognition between cell surface sugars and lectins in the phagocytosis of bacteria. Infect Immun 56(3):539–547
Ostrowski EA, Katoh M, Shaulsky G, Queller DC, Strassmann JE (2008) Kin discrimination increases with genetic distance in a social amoeba. PLoS Biol 6(11):e287
Ostrowski EA, Shen Y, Tian X, Sucgang R, Jiang H, Qu J, Katoh-Kurasawa M, Brock DA, Dinh C, Lara-Garduno F, Lee SL, Kovar CL, Dinh HH, Korchina V, Jackson L, Patil S, Han Y, Chaboub L, Shaulsky G, Muzny DM, Worley KC, Gibbs RA, Richards S, Kuspa A, Strassmann JE, Queller DC (2015) Genomic signatures of cooperation and conflict in the social amoeba. Curr Biol 25(12):1661–1665. https://doi.org/10.1016/j.cub.2015.04.059
Pang X, Xiao X, Liu Y, Zhang R, Liu J, Liu Q, Wang P, Cheng G (2016) Mosquito C-type lectins maintain gut microbiome homeostasis. Nat Microbiol 1:16023. https://doi.org/10.1038/nmicrobiol.2016.23
Parkinson K, Bolourani P, Traynor D, Aldren NL, Kay RR, Weeks G, Thompson CR (2009) Regulation of Rap1 activity is required for differential adhesion, cell-type patterning and morphogenesis in Dictyostelium. J Cell Sci 122(Pt 3):335–344. https://doi.org/10.1242/jcs.036822
Penn DJ, Damjanovich K, Potts WK (2002) MHC heterozygosity confers a selective advantage against multiple-strain infections. Proc Natl Acad Sci U S A 99(17):11260–11264. https://doi.org/10.1073/pnas.162006499
Peracino B, Buracco S, Bozzaro S (2013) The Nramp (Slc11) proteins regulate development, resistance to pathogenic bacteria and iron homeostasis in Dictyostelium discoideum. J Cell Sci 126(Pt 1):301–311. https://doi.org/10.1242/jcs.116210
Pozos TC, Ramakrishan L (2004) New models for the study of mycobacterium-host interactions. Curr Opin Immunol 16(4):499–505
Pukatzki S, Kessin RH, Mekalanos JJ (2002) The human pathogen Pseudomonas aeruginosa utilizes conserved virulence pathways to infect the social amoeba Dictyostelium discoideum. Proc Natl Acad Sci U S A 99:3159–3164
Pukatzki S, Ma AT, Sturtevant D, Krastins B, Sarracino D, Nelson WC, Heidelberg JF, Mekalanos JJ (2006) Identification of a conserved bacterial protein secretion system in Vibrio cholerae using the Dictyostelium host model system. Proc Natl Acad Sci U S A 103(5):1528–1533. https://doi.org/10.1073/pnas.0510322103. 0510322103 [pii]
Queller DC, Ponte E, Bozzaro S, Strassmann JE (2003) Single-gene greenbeard effects in the social amoeba Dictyostelium discoideum. Science 299(5603):105–106
Raper KB (1937) Growth and development of Dictyostelium discoideum with different bacterial associates. J Agric Res 55:289–316
Robery S, Tyson R, Dinh C, Kuspa A, Noegel AA, Bretschneider T, Andrews PL, Williams RS (2013) A novel human receptor involved in bitter tastant detection identified using Dictyostelium discoideum. J Cell Sci 126(Pt 23):5465–5476. https://doi.org/10.1242/jcs.136440
Rogozin IB, Basu MK, Csuros M, Koonin EV (2009) Analysis of rare genomic changes does not support the unikont-bikont phylogeny and suggests cyanobacterial symbiosis as the point of primary radiation of eukaryotes. Genome Biol Evol 1:99–113. https://doi.org/10.1093/gbe/evp011
Rosengarten RD, Moreno MA, Lakkis FG, Buss LW, Dellaporta SL (2011) Genetic diversity of the allodeterminant alr2 in Hydractinia symbiolongicarpus. Mol Biol Evol 28(2):933–947. https://doi.org/10.1093/molbev/msq282
Saitoh T, Komano J, Saitoh Y, Misawa T, Takahama M, Kozaki T, Uehata T, Iwasaki H, Omori H, Yamaoka S, Yamamoto N, Akira S (2012) Neutrophil extracellular traps mediate a host defense response to human immunodeficiency virus-1. Cell Host Microbe 12(1):109–116. https://doi.org/10.1016/j.chom.2012.05.015
Santorelli LA, Thompson CR, Villegas E, Svetz J, Dinh C, Parikh A, Sucgang R, Kuspa A, Strassmann JE, Queller DC, Shaulsky G (2008) Facultative cheater mutants reveal the genetic complexity of cooperation in social amoebae. Nature 451(7182):1107–1110
Schaap P, Winckler T, Nelson M, Alvarez-Curto E, Elgie B, Hagiwara H, Cavender J, Milano-Curto A, Rozen DE, Dingermann T, Mutzel R, Baldauf SL (2006) Molecular phylogeny and evolution of morphology in the social amoebas. Science 314(5799):661–663. https://doi.org/10.1126/science.1130670. 314/5799/661 [pii]
Schilde C, Schaap P (2013) The Amoebozoa. Methods Mol Biol 983:1–15. https://doi.org/10.1007/978-1-62703-302-2_1
Shaulsky G, Kessin RH (2007) The cold war of the social amoebae. Curr Biol 17(16):R684–R692
Sillo A, Bloomfield G, Balest A, Balbo A, Pergolizzi B, Peracino B, Skelton J, Ivens A, Bozzaro S (2008) Genome-wide transcriptional changes induced by phagocytosis or growth on bacteria in Dictyostelium. BMC Genomics 9:291. https://doi.org/10.1186/1471-2164-9-291. 1471-2164-9-291 [pii]
Sillo A, Matthias J, Konertz R, Bozzaro S, Eichinger L (2011) Salmonella typhimurium is pathogenic for Dictyostelium cells and subverts the starvation response. Cell Microbiol 13(11):1793–1811. https://doi.org/10.1111/j.1462-5822.2011.01662.x
Simon S, Hilbi H (2015) Subversion of cell-autonomous immunity and cell migration by Legionella pneumophila effectors. Front Immunol 6:447. https://doi.org/10.3389/fimmu.2015.00447
Snyder ML (2013) Bacterial discrimination: Dictyostelium’s discerning taste. Curr Biol 23(10):R443–R446. https://doi.org/10.1016/j.cub.2013.04.021
Song J, Xu Q, Olsen R, Loomis WF, Shaulsky G, Kuspa A, Sucgang R (2005) Comparing the Dictyostelium and Entamoeba genomes reveals an ancient split in the Conosa lineage. PLoS Comput Biol 1(7):e71. https://doi.org/10.1371/journal.pcbi.0010071
Stallforth P, Brock DA, Cantley AM, Tian X, Queller DC, Strassmann JE, Clardy J (2013) A bacterial symbiont is converted from an inedible producer of beneficial molecules into food by a single mutation in the gacA gene. Proc Natl Acad Sci U S A 110(36):14528–14533. https://doi.org/10.1073/pnas.1308199110
Stechmann A, Cavalier-Smith T (2002) Rooting the eukaryote tree by using a derived gene fusion. Science 297(5578):89–91
Stechmann A, Cavalier-Smith T (2003) The root of the eukaryote tree pinpointed. Curr Biol 13(17):R665–R666
Steenbergen JN, Nosanchuk JD, Malliaris SD, Casadevall A (2003) Cryptococcus neoformans virulence is enhanced after growth in the genetically malleable host Dictyostelium discoideum. Infect Immun 71:4862–4872
Steinbacher S, Seckler R, Miller S, Steipe B, Huber R, Reinemer P (1994) Crystal structure of P22 tailspike protein: interdigitated subunits in a thermostable trimer. Science 265(5170):383–386
Steinert M, Heuner K (2005) Dictyostelium as host model for pathogenesis. Cell Microbiol 7:307–314
Stowell SR, Arthur CM, McBride R, Berger O, Razi N, Heimburg-Molinaro J, Rodrigues LC, Gourdine JP, Noll AJ, von Gunten S, Smith DF, Knirel YA, Paulson JC, Cummings RD (2014) Microbial glycan microarrays define key features of host-microbial interactions. Nat Chem Biol 10(6):470–476. https://doi.org/10.1038/nchembio.1525
Strassmann JE (2016) Kin discrimination in Dictyostelium social amoebae. J Eukaryot Microbiol. https://doi.org/10.1111/jeu.12307
Strassmann JE, Queller DC (2011) Evolution of cooperation and control of cheating in a social microbe. Proc Natl Acad Sci U S A 108(Suppl 2):10855–10862. https://doi.org/10.1073/pnas.1102451108
Strassmann JE, Shu L (2017) Ancient bacteria-amoeba relationships and pathogenic animal bacteria. PLoS Biol 15(5):e2002460. https://doi.org/10.1371/journal.pbio.2002460
Strassmann JE, Zhu Y, Queller DC (2000) Altruism and social cheating in the social amoeba Dictyostelium discoideum. Nature 408:965–967
Sucgang R, Kuo A, Tian X, Salerno W, Parikh A, Feasley CL, Dalin E, Tu H, Huang E, Barry K, Lindquist E, Shapiro H, Bruce D, Schmutz J, Salamov A, Fey P, Gaudet P, Anjard C, Babu MM, Basu S, Bushmanova Y, van der Wel H, Katoh-Kurasawa M, Dinh C, Coutinho PM, Saito T, Elias M, Schaap P, Kay RR, Henrissat B, Eichinger L, Rivero F, Putnam NH, West CM, Loomis WF, Chisholm RL, Shaulsky G, Strassmann JE, Queller DC, Kuspa A, Grigoriev IV (2011) Comparative genomics of the social amoebae Dictyostelium discoideum and Dictyostelium purpureum. Genome Biol 12(2):R20. https://doi.org/10.1186/gb-2011-12-2-r20
Swanson MS, Hammer BK (2000) Legionella pneumophila pathogenesis: a fateful journey from amoebae to macrophages. Annu Rev Microbiol 54:567–613. https://doi.org/10.1146/annurev.micro.54.1.567. 54/1/567 [pii]
Taylor-Mulneix DL, Bendor L, Linz B, Rivera I, Ryman VE, Dewan KK, Wagner SM, Wilson EF, Hilburger LJ, Cuff LE, West CM, Harvill ET (2017) Bordetella bronchiseptica exploits the complex life cycle of Dictyostelium discoideum as an amplifying transmission vector. PLoS Biol 15(4):e2000420. https://doi.org/10.1371/journal.pbio.2000420
Thomas JM, Ashbolt NJ (2011) Do free-living amoebae in treated drinking water systems present an emerging health risk? Environ Sci Technol 45(3):860–869. https://doi.org/10.1021/es102876y
Thomas V, Herrera-Rimann K, Blanc DS, Greub G (2006) Biodiversity of amoebae and amoeba-resisting bacteria in a hospital water network. Appl Environ Microbiol 72(4):2428–2438. https://doi.org/10.1128/AEM.72.4.2428-2438.2006. 72/4/2428 [pii]
Tian X, Strassmann JE, Queller DC (2013) Dictyostelium development shows a novel pattern of evolutionary conservation. Mol Biol Evol 30(4):977–984. https://doi.org/10.1093/molbev/mst007
Tosetti N, Croxatto A, Greub G (2014) Amoebae as a tool to isolate new bacterial species, to discover new virulence factors and to study the host-pathogen interactions. Microb Pathog 77:125–130. https://doi.org/10.1016/j.micpath.2014.07.009
Waheed A, Ludtmann MH, Pakes N, Robery S, Kuspa A, Dinh C, Baines D, Williams RS, Carew MA (2014) Naringenin inhibits the growth of Dictyostelium and MDCK-derived cysts in a TRPP2 (polycystin-2)-dependent manner. Br J Pharmacol 171(10):2659–2670. https://doi.org/10.1111/bph.12443
Walk A, Callahan J, Srisawangvong P, Leuschner J, Samaroo D, Cassilly D, Snyder ML (2011) Lipopolysaccharide enhances bactericidal activity in Dictyostelium discoideum cells. Dev Comp Immunol 35(8):850–856. https://doi.org/10.1016/j.dci.2011.03.018
Wang N, Soderbom F, Anjard C, Shaulsky G, Loomis WF (1999) SDF-2 induction of terminal differentiation in Dictyostelium discoideum is mediated by the membrane-spanning sensor kinase DhkA. Mol Cell Biol 19:4750–4756
Wang J, Hou L, Awrey D, Loomis WF, Firtel RA, Siu CH (2000) The membrane glycoprotein gp150 is encoded by the lagC gene and mediates cell-cell adhesion by heterophilic binding during Dictyostelium development. Dev Biol 227(2):734–745
Zhang X, Soldati T (2013) Detecting, visualizing and quantitating the generation of reactive oxygen species in an amoeba model system. J Vis Exp: JoVE 81:e50717. https://doi.org/10.3791/50717
Zhang X, Soldati T (2016) Of amoebae and men: extracellular DNA traps as an ancient cell-intrinsic defense mechanism. Front Immunol 7:269. https://doi.org/10.3389/fimmu.2016.00269
Zhang X, Krause KH, Xenarios I, Soldati T, Boeckmann B (2013) Evolution of the ferric reductase domain (FRD) superfamily: modularity, functional diversification, and signature motifs. PLoS One 8(3):e58126. https://doi.org/10.1371/journal.pone.0058126
Zhang X, Zhuchenko O, Kuspa A, Soldati T (2016) Social amoebae trap and kill bacteria by casting DNA nets. Nat Commun 7:10938. https://doi.org/10.1038/ncomms10938
Acknowledgments
I would like to thank all of the past and present members of my laboratory and the laboratory of Gadi Shaulsky for their insights and their contributions to our understanding of amoebae–bacteria interactions. The author extends a special thanks to Christopher Dinh for discovering the influence of lectins on bacterial carriage and for the images in Figs. 3 and 4a. I am immensely grateful to William F. Loomis for introducing me to Dictyostleium forty years ago and for providing me his illuminating insights for thirty-eight of those years.
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2018 Springer International Publishing AG, part of Springer Nature
About this chapter
Cite this chapter
Kuspa, A. (2018). Allorecognition and Innate Immunity in the Dictyostelid Social Amoebae. In: Cooper, E. (eds) Advances in Comparative Immunology. Springer, Cham. https://doi.org/10.1007/978-3-319-76768-0_2
Download citation
DOI: https://doi.org/10.1007/978-3-319-76768-0_2
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-319-76767-3
Online ISBN: 978-3-319-76768-0
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)