Lectins modulate the microbiota of social amoebae

Science ◽  
2018 ◽  
Vol 361 (6400) ◽  
pp. 402-406 ◽  
Author(s):  
Christopher Dinh ◽  
Timothy Farinholt ◽  
Shigenori Hirose ◽  
Olga Zhuchenko ◽  
Adam Kuspa
Keyword(s):  
Mammalian Cells ◽  
Cellular Response ◽  
Dna Transfer ◽  
Intracellular Bacteria ◽  
Multicellular Development ◽  
Social Amoeba ◽  
Plant Lectins ◽  
The Social ◽  
Eukaryotic Phylogeny ◽  
Social Amoebae

The social amoebaDictyostelium discoideummaintains a microbiome during multicellular development; bacteria are carried in migrating slugs and as endosymbionts within amoebae and spores. Bacterial carriage and endosymbiosis are induced by the secreted lectin discoidin I that binds bacteria, protects them from extracellular killing, and alters their retention within amoebae. This altered handling of bacteria also occurs with bacteria coated by plant lectins and leads to DNA transfer from bacteria to amoebae. Thus, lectins alter the cellular response ofD. discoideumto bacteria to establish the amoebae’s microbiome. Mammalian cells can also maintain intracellular bacteria when presented with bacteria coated with lectins, so heterologous lectins may induce endosymbiosis in animals. Our results suggest that endogenous or environmental lectins may influence microbiome homeostasis across eukaryotic phylogeny.

scholarly journals MyTH4-FERM myosins have an ancient and conserved role in filopod formation

2016 ◽  
Vol 113 (50) ◽  
pp. E8059-E8068 ◽  
Author(s):  
Karl J. Petersen ◽  
Holly V. Goodson ◽  
Ashley L. Arthur ◽  
G. W. Gant Luxton ◽  
Anne Houdusse ◽  
...  
Keyword(s):  
Mammalian Cells ◽  
Live Cell Imaging ◽  
Cell Imaging ◽  
Null Mutant ◽  
Minimal Elements ◽  
Social Amoeba ◽  
Functional Conservation ◽  
Functional Homolog ◽  
The Social ◽  
Functional Features

The formation of filopodia in Metazoa and Amoebozoa requires the activity of myosin 10 (Myo10) in mammalian cells and of Dictyostelium unconventional myosin 7 (DdMyo7) in the social amoeba Dictyostelium. However, the exact roles of these MyTH4-FERM myosins (myosin tail homology 4-band 4.1, ezrin, radixin, moesin; MF) in the initiation and elongation of filopodia are not well defined and may reflect conserved functions among phylogenetically diverse MF myosins. Phylogenetic analysis of MF myosin domains suggests that a single ancestral MF myosin existed with a structure similar to DdMyo7, which has two MF domains, and that subsequent duplications in the metazoan lineage produced its functional homolog Myo10. The essential functional features of the DdMyo7 myosin were identified using quantitative live-cell imaging to characterize the ability of various mutants to rescue filopod formation in myo7-null cells. The two MF domains were found to function redundantly in filopod formation with the C-terminal FERM domain regulating both the number of filopodia and their elongation velocity. DdMyo7 mutants consisting solely of the motor plus a single MyTH4 domain were found to be capable of rescuing the formation of filopodia, establishing the minimal elements necessary for the function of this myosin. Interestingly, a chimeric myosin with the Myo10 MF domain fused to the DdMyo7 motor also was capable of rescuing filopod formation in the myo7-null mutant, supporting fundamental functional conservation between these two distant myosins. Together, these findings reveal that MF myosins have an ancient and conserved role in filopod formation.

scholarly journals Exposure to dense bacteria lawns does not cause the social amoeba Dictyostelium discoideum to carry bacteria through the social stage

2017 ◽  
Author(s):  
Debra A Brock ◽  
Alicia Canas ◽  
Kai Jones ◽  
David C Queller ◽  
Joan E Strassmann
Keyword(s):  
Dictyostelium Discoideum ◽  
Associated Bacteria ◽  
Social Amoeba ◽  
Future Studies ◽  
Bacterial Cultures ◽  
Large Numbers ◽  
The Social ◽  
External Forces ◽  
Social Amoebae ◽  
Food Bacteria

Background. Interactions between eukaryotic amoebae and bacteria are understudied and important. Bacteria inside of amoebae are protected from external forces including antibiotics. An excellent model for bacteria-amoeba interactions is the social amoeba Dictyostelium discoideum and its associated bacteria. A third of wild-collected clones of the soil-dwelling amoeba Dictyostelium discoideum exhibit a suite of characteristics that make them simple farmers of bacteria. They carry bacteria internally through the social spore-making stage. They then release these bacteria to grow and subsequently eat them, prudently stopping before they are entirely consumed so some bacteria can be carried to the next generation. D. discoideum defend their food bacteria with other inedible bacteria that produce compounds toxic to non-farmers. Both carried bacteria and social amoeba hosts have demonstrated co-evolved characteristics. Most farmer clones discovered to date carry inedible Burkholderia in addition to food bacteria, but it is not clear whether or not a preponderance of naïve bacteria might induce the farming state by overwhelming the phagocytic actions of the host amoebae. In this study we address this question with D. discoideum clones that naturally carry bacteria and those that do not. Will naïve bacteria in large numbers succeed in colonizing the amoebae? Methods. We grew five non-farmer clones and five farmer clones of wild-collected Dictyostelium discoideum on three different concentrations of a highly palatable bacterial food source, Klebsiella pneumoniae. We then tested them to see if they carried bacteria through the social stage. Results. We found that bacterial density did not have a significant effect on whether or not the clones carried bacteria through the social stage. Even those grown in very dense bacterial cultures were able to shed them successfully unless they were also carrying Burkholderia. Discussion. Our results indicate that even a preponderance of food bacteria cannot overwhelm the ability of social amoebae to digest and not carry bacteria. Apparently, only the inedible Burkholderia have that effect. This points to the importance of understanding co-infection with multiple bacteria because those that cannot induce carriage can nevertheless become carried, foiling digestive processes, but only in the presence of another bacterium. Future studies of host bacteria interactions should consider using multiple bacteria simultaneously.

scholarly journals Terpene synthase genes in eukaryotes beyond plants and fungi: Occurrence in social amoebae

2016 ◽  
Vol 113 (43) ◽  
pp. 12132-12137 ◽  
Author(s):  
Xinlu Chen ◽  
Tobias G. Köllner ◽  
Qidong Jia ◽  
Ayla Norris ◽  
Balaji Santhanam ◽  
...  
Keyword(s):  
Early Stage ◽  
Terpene Synthase ◽  
Functional Study ◽  
Terpene Biosynthesis ◽  
Terpene Synthases ◽  
Multicellular Development ◽  
Stage Of Development ◽  
The Social ◽  
Volatile Terpenes ◽  
Social Amoebae

Terpenes are structurally diverse natural products involved in many ecological interactions. The pivotal enzymes for terpene biosynthesis, terpene synthases (TPSs), had been described only in plants and fungi in the eukaryotic domain. In this report, we systematically analyzed the genome sequences of a broad range of nonplant/nonfungus eukaryotes and identified putative TPS genes in six species of amoebae, five of which are multicellular social amoebae from the order of Dictyosteliida. A phylogenetic analysis revealed that amoebal TPSs are evolutionarily more closely related to fungal TPSs than to bacterial TPSs. The social amoeba Dictyostelium discoideum was selected for functional study of the identified TPSs. D. discoideum grows as a unicellular organism when food is abundant and switches from vegetative growth to multicellular development upon starvation. We found that expression of most D. discoideum TPS genes was induced during development. Upon heterologous expression, all nine TPSs from D. discoideum showed sesquiterpene synthase activities. Some also exhibited monoterpene and/or diterpene synthase activities. Direct measurement of volatile terpenes in cultures of D. discoideum revealed essentially no emission at an early stage of development. In contrast, a bouquet of terpenes, dominated by sesquiterpenes including β-barbatene and (E,E)-α-farnesene, was detected at the middle and late stages of development, suggesting a development-specific function of volatile terpenes in D. discoideum. The patchy distribution of TPS genes in the eukaryotic domain and the evidence for TPS function in D. discoideum indicate that the TPS genes mediate lineage-specific adaptations.

scholarly journals Symbiont location, host fitness, and possible coadaptation in a symbiosis between social amoebae and bacteria

eLife ◽  
2018 ◽  
Vol 7 ◽  
Author(s):  
Longfei Shu ◽  
Debra A Brock ◽  
Katherine S Geist ◽  
Jacob W Miller ◽  
David C Queller ◽  
...  
Keyword(s):  
Dictyostelium Discoideum ◽  
Host Responses ◽  
Bacterial Symbionts ◽  
Disease Dynamics ◽  
Fitness Costs ◽  
Social Amoeba ◽  
Host Fitness ◽  
The Social ◽  
Natural Isolates ◽  
Social Amoebae

Recent symbioses, particularly facultative ones, are well suited for unravelling the evolutionary give and take between partners. Here we look at variation in natural isolates of the social amoeba Dictyostelium discoideum and their relationships with bacterial symbionts, Burkholderia hayleyella and Burkholderia agricolaris. Only about a third of field-collected amoebae carry a symbiont. We cured and cross-infected amoebae hosts with different symbiont association histories and then compared host responses to each symbiont type. Before curing, field-collected clones did not vary significantly in overall fitness, but infected hosts produced morphologically different multicellular structures. After curing and reinfecting, host fitness declined. However, natural B. hayleyella hosts suffered fewer fitness costs when reinfected with B. hayleyella, indicating that they have evolved mechanisms to tolerate their symbiont. Our work suggests that amoebae hosts have evolved mechanisms to tolerate specific acquired symbionts; exploring host-symbiont relationships that vary within species may provide further insights into disease dynamics.

scholarly journals Molecular networking in the neuronal ceroid lipofuscinoses: insights from mammalian models and the social amoeba Dictyostelium discoideum

2020 ◽  
Vol 27 (1) ◽  
Author(s):  
Robert J. Huber
Keyword(s):  
Dictyostelium Discoideum ◽  
Mammalian Cells ◽  
Batten Disease ◽  
Neuronal Ceroid Lipofuscinoses ◽  
Common Disease ◽  
Cellular Mechanisms ◽  
Molecular Networking ◽  
Social Amoeba ◽  
Cellular Models ◽  
The Social

Abstract The neuronal ceroid lipofuscinoses (NCLs), commonly known as Batten disease, belong to a family of neurological disorders that cause blindness, seizures, loss of motor function and cognitive ability, and premature death. There are 13 different subtypes of NCL that are associated with mutations in 13 genetically distinct genes (CLN1-CLN8, CLN10-CLN14). Similar clinical and pathological profiles of the different NCL subtypes suggest that common disease mechanisms may be involved. As a result, there have been many efforts to determine how NCL proteins are connected at the cellular level. A main driving force for NCL research has been the utilization of mammalian and non-mammalian cellular models to study the mechanisms underlying the disease. One non-mammalian model that has provided significant insight into NCL protein function is the social amoeba Dictyostelium discoideum. Accumulated data from Dictyostelium and mammalian cells show that NCL proteins display similar localizations, have common binding partners, and regulate the expression and activities of one another. In addition, genetic models of NCL display similar phenotypes. This review integrates findings from Dictyostelium and mammalian models of NCL to highlight our understanding of the molecular networking of NCL proteins. The goal here is to help set the stage for future work to reveal the cellular mechanisms underlying the NCLs.

scholarly journals An evolutionarily significant unicellular strategy in response to starvation in Dictyostelium social amoebae

F1000Research ◽  
2014 ◽  
Vol 3 ◽  
pp. 133 ◽  
Author(s):  
Darja Dubravcic ◽  
Minus van Baalen ◽  
Clément Nizak
Keyword(s):  
Cell Fate ◽  
Genetic Factors ◽  
Development Program ◽  
Population Level ◽  
Time Lapse ◽  
Evolutionary Significance ◽  
Multicellular Development ◽  
The Social ◽  
Fluctuating Environments ◽  
Social Amoebae

The social amoeba Dictyostelium discoideum is widely studied for its multicellular development program as a response to starvation. Aggregates of up to 106 cells form fruiting bodies containing (i) dormant spores (~80%) that can persist for months in the absence of nutrients, and (ii) dead stalk cells (~20%) that promote the dispersion of the spores towards nutrient-rich areas.It is often overlooked that not all cells aggregate upon starvation. Using a new quantitative approach based on time-lapse fluorescence microscopy and a low ratio of reporting cells, we have quantified this fraction of non-aggregating cells. In realistic starvation conditions, up to 15% of cells do not aggregate, which makes this third cell fate a significant component of the population-level response of social amoebae to starvation. Non-aggregating cells have an advantage over cells in aggregates since they resume growth earlier upon arrival of new nutrients, but have a shorter lifespan under prolonged starvation. We find that phenotypic heterogeneities linked to cell nutritional state bias the representation of cells in the aggregating vs. non-aggregating fractions, and thus affect population partitioning. Next, we report that the fraction of non-aggregating cells depends on genetic factors that regulate the timing of starvation, signal sensing efficiency and aggregation efficiency. In addition, interactions between clones in mixtures of non-isogenic cells affect the partitioning of each clone into both fractions. We further build a numerical model to test the evolutionary significance of the non-aggregating cell fraction. The partitioning of cells into aggregating and non-aggregating fractions is optimal in fluctuating environments with an unpredictable duration of starvation periods. Our study highlights the unicellular component of the response of social amoebae to starvation, and thus extends its evolutionary and ecological framework.

scholarly journals Microbiome management in the social amoeba Dictyostelium discoideum compared to humans

2019 ◽  
Vol 63 (8-9-10) ◽  
pp. 447-450 ◽  
Author(s):  
Timothy Farinholt ◽  
Christopher Dinh ◽  
Adam Kuspa
Keyword(s):  
Recent Work ◽  
Dictyostelium Discoideum ◽  
Immune Cells ◽  
Molecular Mechanisms ◽  
Innate Immune ◽  
Innate Immune Cells ◽  
Social Amoeba ◽  
The Social ◽  
Physical Barriers ◽  
Social Amoebae

Social amoebae and humans use common strategies to orchestrate their interactions with the bacteria in their respective environments and within their bodies. These strategies include the elimination of bacteria by phagocytosis, the establishment of mutualistic interactions, the elaboration of physical barriers, and the deployment of innate immune cells. Many of the molecular mechanisms that humans and social amoebae employ differ, but there are striking similarities that may inform studies in each organism. In this topical review we highlight the similarities and consider what we might learn by comparing these highly divergent species. We focus on recent work in Dictyostelium discoideum with hopes of stimulating work in this area and with the expectation that new mechanistic details uncovered in social amoebae-bacteria interactions will inform microbiome management in humans.

scholarly journals An ancestral non-proteolytic role for presenilin proteins in multicellular development of the social amoeba Dictyostelium discoideum

2014 ◽  
Vol 127 (7) ◽  
pp. 1576-1584 ◽  
Author(s):  
M. H. R. Ludtmann ◽  
G. P. Otto ◽  
C. Schilde ◽  
Z.-H. Chen ◽  
C. Y. Allan ◽  
...  
Keyword(s):  
Dictyostelium Discoideum ◽  
Multicellular Development ◽  
Social Amoeba ◽  
The Social

scholarly journals Sex Determination in the Social Amoeba Dictyostelium discoideum

Science ◽  
2010 ◽  
Vol 330 (6010) ◽  
pp. 1533-1536 ◽  
Author(s):  
Gareth Bloomfield ◽  
Jason Skelton ◽  
Alasdair Ivens ◽  
Yoshimasa Tanaka ◽  
Robert R. Kay
Keyword(s):  
Sex Determination ◽  
Dictyostelium Discoideum ◽  
Genetic Locus ◽  
Model Organism ◽  
Mating Types ◽  
Type Locus ◽  
Social Amoeba ◽  
The Third ◽  
The Social ◽  
Social Amoebae

The genetics of sex determination remain mysterious in many organisms, including some that are otherwise well studied. Here we report the discovery and analysis of the mating-type locus of the model organism Dictyostelium discoideum. Three forms of a single genetic locus specify this species' three mating types: two versions of the locus are entirely different in sequence, and the third resembles a composite of the other two. Single, unrelated genes are sufficient to determine two of the mating types, whereas homologs of both these genes are required in the composite type. The key genes encode polypeptides that possess no recognizable similarity to established protein families. Sex determination in the social amoebae thus appears to use regulators that are unrelated to any others currently known.

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