Dictyostelium discoideum, slime mold

Taxonomy

D. discoideum belongs to the order of Dictyosteliida (dictyostelid cellular slime molds or social amoebae). Dictyosteliida contains organisms that hover on the borderline between uni- and multicellularity. Each organism starts its life as a unicellular amoeba, but they aggregate to form a multicellular fruiting body when starved. Traditionally, social amoebas have been classified according to their most notable trait, fruiting body morphology. Based on this, three genera have been proposed: Dictyostelium, with unbranched or laterally branched fruiting bodies; Polysphondylium, whose fruiting bodies consist of repetitive whorls of regularly spaced side branches; and Acytostelium, which, unlike the other genera, forms acellular fruiting body stalks.

Taxonomic lineage

cellular organisms - Eukaryota - Amoebozoa - Mycetozoa - Dictyosteliida - Dictyostelium - Dictyostelium discoideum

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Brief facts

• Dictyostelium discoideum (slime mold) are a free living amoebae whose natural habitat is the upper layer of soil rich in decaying organic material. Bacteria are the main source of food of the D. discoideum. When the food supply is abundant the slime mold organisms live in unicellar form. Once the food becomes sparse they aggregate to form a multicellular fruiting body composed of two main cell types: stalk cells that support a spore-containing sorus. Spores are protected by a tough cell wall. The stalk raises the spore head high enough for the spores to be scattered away to maximize the possibility of germination in a more favorable environment. The dispersion of spores in an environment favorable for successful germination and survival is granted by the ability of the slug to migrate towards light and heat.
• Formation of the multicellular stages of the Dictyostelids is remarkable in that it is accomplished through the aggregation of neighboring cells rather than by division of a single cell (zygote), as is the case in most multicellular organisms. The size of the multicellular organism ranges from 10,000 to 100,000 cells, or up to 2,000,000; however, slugs composed of as few as 100 cells have been reported.

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Model organism

• Dictyostelium discoideum is an important model organism for studies of actin cytoskeleton's dynamics, cell type determination, spatial patterning, altruistic cell death and other fundamental features that are essential in multicellular organisms.
• Dictyostelium avidly engulf and kills most of the bacteria. Indeed, bacterial pathogenicity was largely developed to resist predatory amoebae in the environment. The basic strategies of phagocytic cells, invented in primitive protozoan, are still used in both amoebae and mammalian phagocytic cells. It can be said that Dictyostelium is a primitive macrophage. This is why the organism is used for maintaining cultures or as a host model for several pathogens including Pseudomonas aeruginosa, Cryptococcus neoformans (at MetaPathogen), Mycobacterium spp. and Legionella pneumophila.
• Infection of Dictyostelium discoideum with intracellular pathogenic bacteria Legionella pneumophila parallels the infection of mammalian macrophages and the fresh-water amoebae Hartmannella vermiformis and Acanthamoeba castellanii. This model system of host-pathogen interaction has a critical distinction: because Dictyostelium discoideum cannot survive in temperatures higher than 27°C, the incubation temperature of the model has to be about 25.5°C. Many pathogens, however, start expressing their key virulence factors only at 37°C (temperature of human body).

Related organisms:

• Cryptococcus neoformans (facts, life cycle, bibliography at MetaPathogen)
• Legionella pneumophila (Legionnair's disease, Pontiac fever, legionellosis at MetaPathogen)

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Life cycle

Dictyostelium has 3 modes of reproduction: sexual, asexual (spores) and vegetative - mitotic division of unicellular organisms.

• Vegetative Myxamoeba stage; free-living amoebae; unicellular form; vegetative growth by mitotic division.
• Sexual Dictyostelium are both haploid and diploid organisms; the sexual cycle is initiated by the fusion of cells that are of opposite mating types (heterothallic mating); it results in the formation of a multiwalled macrocyst whose development begins with the formation of a zygote which ingest the surrounding myxamoebae as it increases in size; on germination, haploid myxamoebae escape from the ruptured macrocyst; these cells originate by cleavage of the single large protoplast of the mature macrocyst.
• Asexual
  • Aggregation Upon starvation a few amoebae acting as the aggregation center start to produce periodic cAMP pulses, which are detected, amplified and relayed by the surrounding amoebaes; individual cells move chemotactically towards increasing cAMP concentrations; the aggregate of approximately 100,000 cells undergoes a series of morphogenetic changes.
    • Stream formation Attraction of other amoebae to the forming group.
    • Loose aggregate
    • Tight aggregate
  • mound Non-differentiated slug.
  • Slug Pseudoplasmodium; typically consists of about 100,000 cells that are differentiated into 2 distinct cell types: cells in posterior of the slug will become spores, and cells in anterior which direct the pseudoplasmodium are destined to become stalk cells of the fruiting body; slug stage enables cellular slime molds to migrate towards the surface of the soil thus to have a better chance for spore dispersal.
  • Culmination The stalk cells form a cellulose framework on which the spore mass is lifted up in the air.

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Appendix 1: anatomy ontologies

Gaudet P, Williams JG, Fey P, Chisholm RL. An anatomy ontology to represent biological knowledge in Dictyostelium discoideum. BMC Genomics. 2008; 9: 130.

Dictyostelium life cycle and the corresponding anatomical structures from the Dictyostelium anatomy ontology. A. Vegetative amoebae (DDANAT:0000002). B. Aggregation territory (DDANAT:0000003). C. Loose aggregate (DDANAT:0000004) with stream (DDANAT:0000013). D. Mound (DDANAT:0000005). E. Tipped mound (DDANAT:0000006). F. Standing slug (DDANAT:0000007). G. Migratory slug (DDANAT:0000008). H. Early culminant (DDANAT:0000009). I. Mid culminant (DDANAT:0000010). J. Fruiting body (DDANAT:0000010) with spores (DDANAT:0000414).

Subdivisions of the multicellular organism. The prestalk and prespore zones are recognizable from the tipped mound stage. This diagram represents the different subdivisions of the multicellular organism at the migratory slug stage. The subdivisions remain in the same relative positions and proportions until culmination.

Cell movements during culmination. Terminal cell differentiation takes place during the culmination stage and is correlated with cellular movements within the organism, as shown here for an early culminant. PstAB cells present in the slug are the first to migrate down the stalk tube and terminally differentiate into stalk cells, hence referred to as primary prestalk cells. They are replaced by pstA cells, which start expressing ecmB and in turn become stalk cells (secondary prestalk cells). PstA cells are in turn replaced by pstO cells. This process continues until all prestalk cells have been incorporated into the stalk.

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Appendix 2: P450 oxidoreductase (RedA) controls development beyond the mound stage

Gonzalez-Kristeller DC et al. The P450 oxidoreductase, RedA, controls development beyond the mound stage in Dictyostelium discoideum. BMC Dev Biol. 2008; 8: 8.

Disruption of redA impairs development at mound stage. (A) Exponentially growing AX4 wild type cells and the mutants redA- and redA-KO were starved on filter pads and photographed at the indicated times (h) after starvation. (B) AX4 fruiting bodies and redA- yellow mounds after 48 hours starvation on filter pads are shown at lower (left) and at 5x higher magnification (right).

AX4 cells do not rescue redA- phenotype. Exponentially growing redA- and AX4 wild type cells were starved on filter pads mixed at the indicated proportions. At the indicated times (h) after starvation cells were photographed.

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Appendix 3: duplications in the genomes of laboratory stocks of Dictyostelium discoideum

Gareth Bloomfield, Yoshimasa Tanaka, Jason Skelton, Alasdair Ivens, and Robert R Kay.
Widespread duplications in the genomes of laboratory stocks of Dictyostelium discoideum. Genome Biol. 2008; 9(4)

Relationships between the most commonly used Dictyostelium strains.
(a) Simplified genealogical tree showing the relationships between common laboratory strains derived from NC4. The branch marked 'Ax3' is more complex than shown here: sub-lineages have been given the names KAx3 and Ax4. The auxotrophic strain DH1 was engineered in an 'Ax3' background, and JH10 from 'Ax4.'
(b) Plaque morphologies. Cells were plated clonally in association with Klebsiella aerogenes on SM agar. Plaques were photographed after 4 days. Small DH1 plaques are indicated with arrowheads. Variation in diameter is a function of the rate of feeding and of the motility of the amoebae. Where the bacteria are cleared the amoebae aggregate in streams; this process had not yet begun in the slow-growing DH1 plaques.
(c) Fruiting bodies. Wild type cells - in this instance NC4(Dee) - form larger, more robust fruiting bodies than axenic mutants.

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References

• Steinert M, Heuner K. Dictyostelium as host model for pathogenesis. Cell Microbiol. 2005 Mar;7(3):307-14.
• Cosson P, Soldati T. Eat, kill or die: when amoeba meets bacteria. Curr Opin Microbiol. 2008 Jun;11(3):271-6.
• Solomon JM, Isberg RR. Growth of Legionella pneumophila in Dictyostelium discoideum: a novel system for genetic analysis of host-pathogen interactions. Cell Microbiol. 2005 Mar;7(3):307-14.
• Schaap P et al. Molecular phylogeny and evolution of morphology in the social amoebas. Science. 2006 Oct 27;314(5799):661-3.
• Chibalina MV, Anjard C, Insall RH. Gdt2 regulates the transition of Dictyostelium cells from growth to differentiation. BMC Dev Biol. 2004 Jul 5;4:8. (cover pictures)
• PubMed: free full text articles about Dictyostelium

Websites

• Pattern Formation in Dictyostelium discoideum
• dictyBase
• Model Organisms for Biomedical Research: Dictyostelium discoideum

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