Abstract:Colony formation was the first step towards evolution of multicellularity in many macroscopic organisms. Dictyostelid social amoebas have used this strategy for over 600 Myr to form fruiting structures of increasing complexity. To understand in which order multicellular complexity evolved, we measured 24 phenotypic characters over 99 dictyostelid species. Using phylogenetic comparative methods, we show that the last common ancestor (LCA) of Dictyostelia probably erected small fruiting structures directly from … Show more
“…Indeed, several Dictyostelid species produce fruiting bodies only hundreds of microns long
[10]. Fruiting bodies may also increase spore transport by raising them to increase contact with passing invertebrates.…”
BackgroundMany microbial phenotypes are the product of cooperative interactions among cells, but their putative fitness benefits are often not well understood. In the cellular slime mold Dictyostelium discoideum, unicellular amoebae aggregate when starved and form multicellular fruiting bodies in which stress-resistant spores are held aloft by dead stalk cells. Fruiting bodies are thought to be adaptations for dispersing spores to new feeding sites, but this has not been directly tested. Here we experimentally test whether fruiting bodies increase the rate at which spores are acquired by passing invertebrates.ResultsDrosophila melanogaster accumulate spores on their surfaces more quickly when exposed to intact fruiting bodies than when exposed to fruiting bodies physically disrupted to dislodge spore masses from stalks. Flies also ingest and excrete spores that still express a red fluorescent protein marker.ConclusionsMulticellular fruiting bodies created by D. discoideum increase the likelihood that invertebrates acquire spores that can then be transported to new feeding sites. These results thus support the long-hypothesized dispersal benefits of altruism in a model system for microbial cooperation.
“…Indeed, several Dictyostelid species produce fruiting bodies only hundreds of microns long
[10]. Fruiting bodies may also increase spore transport by raising them to increase contact with passing invertebrates.…”
BackgroundMany microbial phenotypes are the product of cooperative interactions among cells, but their putative fitness benefits are often not well understood. In the cellular slime mold Dictyostelium discoideum, unicellular amoebae aggregate when starved and form multicellular fruiting bodies in which stress-resistant spores are held aloft by dead stalk cells. Fruiting bodies are thought to be adaptations for dispersing spores to new feeding sites, but this has not been directly tested. Here we experimentally test whether fruiting bodies increase the rate at which spores are acquired by passing invertebrates.ResultsDrosophila melanogaster accumulate spores on their surfaces more quickly when exposed to intact fruiting bodies than when exposed to fruiting bodies physically disrupted to dislodge spore masses from stalks. Flies also ingest and excrete spores that still express a red fluorescent protein marker.ConclusionsMulticellular fruiting bodies created by D. discoideum increase the likelihood that invertebrates acquire spores that can then be transported to new feeding sites. These results thus support the long-hypothesized dispersal benefits of altruism in a model system for microbial cooperation.
“…The finding that the other N-glycomic changes were not shared across the CSMs and that the structures do not converge to a common pattern, suggests that they do not subserve shared general developmental mechanisms such as chemotaxis, cell adhesion, cell sorting, morphogenesis, and cell differentiation. Nevertheless, individual species have distinctive developmental features [24] that might be supported by their glycan differences. For example, Pp assembles small lateral fruiting bodies on a larger vertical fruiting body, Dp forms an extended stalk, and As does not form specialized stalk cells; any of these differences might be supported by specialized glycans.…”
Section: Discussionmentioning
confidence: 99%
“…a . The social amoebae are classified into 4 groups denoted in parentheses) based on the phylogeny of a core group of housekeeping genes (adapted from Romeralo et al [24]). The last common ancestors of these groups date back 300–550 million years.…”
Section: Figmentioning
confidence: 99%
“…Recently, the genomes of additional social amoebae have been sequenced [23, 2], opening the door to apply genomics to glycogene identification to enable a genetic approach to addressing these questions. Their phylogeny, which spans the diversity of known CSMs [24], is represented in Fig. 1a.…”
Multiple species of cellular slime mold (CSM) amoebae share overlapping subterranean environments near the soil surface. Despite similar life-styles, individual species form independent starvation-induced fruiting bodies whose spores can renew the life cycle. N-glycans associated with the cell surface glycocalyx have been predicted to contribute to interspecific avoidance, resistance to pathogens, and prey preference. N-glycans from five CSM species that diverged 300–600 million years ago and whose genomes have been sequenced were fractionated into neutral and acidic pools and profiled by MALDI-TOF-MS. Glycan structure models were refined using linkage specific antibodies, exoglycosidase digestions, MALDI-MS/MS, and chromatographic studies. Amoebae of the type species Dictyostelium discoideum express modestly trimmed high mannose N-glycans variably modified with core α3-linked Fuc and peripherally decorated with 0–2 residues each of β-GlcNAc, Fuc, methylphosphate and/or sulfate, as reported previously. Comparative analyses of D. purpureum, D. fasciculatum, Polysphondylium pallidum, and Actyostelium subglobosum revealed that each displays a distinctive spectrum of high-mannose species with quantitative variations in the extent of these modifications, and qualitative differences including retention of Glc, mannose methylation, and absence of a peripheral GlcNAc, fucosylation, or sulfation. Starvation-induced development modifies the pattern in all species but, except for universally observed increased mannose-trimming, the N-glycans do not converge to a common profile. Correlations with glycogene repertoires will enable future reverse genetic studies to eliminate N-glycomic differences to test their functions in interspecific relations and pathogen evasion.
“…Many species in these groups have retained encystation, the unicellular life cycle of their amoebozoan ancestors as an additional survival strategy. Group 4 species form larger solitary and unbranched fruiting bodies with up to five cell types and have lost encystation entirely [10]. Fig.…”
BackgroundThe developmental cycle of Dictyostelid amoebae represents an early form of multicellularity with cell type differentiation. Mutant studies in the model Dictyostelium discoideum revealed that its developmental program integrates the actions of genes involved in signal transduction, adhesion, motility, autophagy and cell wall and matrix biosynthesis. However, due to functional redundancy and fail safe options not required in the laboratory, this single organism approach cannot capture all essential genes.To understand how multicellular organisms evolved, it is essential to recognize both the conserved core features of their developmental programs and the gene modifications that instigated phenotypic innovation. For complex organisms, such as animals, this is not within easy reach, but it is feasible for less complex forms, such as the Dictyostelid social amoebas.ResultsWe compared global profiles of gene expression during the development of four social amoebae species that represent 600 mya of Dictyostelia evolution, and identified orthologous conserved genes with similar developmental up-regulation of expression using three different methods. For validation, we disrupted five genes of this core set and examined the phenotypic consequences.ConclusionAt least 71 of the developmentally regulated genes that were identified with all methods were likely to be already present in the last ancestor of all Dictyostelia. The lack of phenotypic changes in null mutants indicates that even highly conserved genes either participate in functionally redundant pathways or are necessary for developmental progression under adverse, non-standard laboratory conditions. Both mechanisms provide robustness to the developmental program, but impose a limit on the information that can be obtained from deleting single genes.Electronic supplementary materialThe online version of this article (doi:10.1186/s12864-016-3223-z) contains supplementary material, which is available to authorized users.
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