scholarly journals Social amoebae establish a protective interface with their bacterial associates by lectin agglutination

2019 ◽  
Vol 5 (7) ◽  
pp. eaav4367 ◽  
Author(s):  
Timothy Farinholt ◽  
Christopher Dinh ◽  
Adam Kuspa
Keyword(s):  
Defense Mechanisms ◽  
Tissue Level ◽  
Adhesion Protein ◽  
Social Amoeba ◽  
Extracellular Traps ◽  
Gut Epithelium ◽  
The Social ◽  
Inflammatory Processes ◽  
A Cell ◽  
Social Amoebae

Both animals and amoebae use phagocytosis and DNA-based extracellular traps as anti-bacterial defense mechanisms. Whether, like animals, amoebae also use tissue-level barriers to reduce direct contact with bacteria has remained unclear. We have explored this question in the social amoeba Dictyostelium discoideum, which forms plaques on lawns of bacteria that expand as amoebae divide and bacteria are consumed. We show that CadA, a cell adhesion protein that functions in D. discoideum development, is also a bacterial agglutinin that forms a protective interface at the plaque edge that limits exposure of vegetative amoebae to bacteria. This interface is important for amoebal survival when bacteria-to-amoebae ratios are high, optimizing amoebal feeding behavior, and protecting amoebae from oxidative stress. Lectins also control bacterial access to the gut epithelium of mammals to limit inflammatory processes; thus, this strategy of antibacterial defense is shared across a broad spectrum of eukaryotic taxa.

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 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.

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 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 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.

scholarly journals Cellular allorecognition and its roles in Dictyostelium development and social evolution

2019 ◽  
Vol 63 (8-9-10) ◽  
pp. 383-393 ◽  
Author(s):  
Peter Kundert ◽  
Gad Shaulsky
Keyword(s):  
Social Evolution ◽  
Model Organism ◽  
Biological Processes ◽  
Functional Heterogeneity ◽  
Selective Force ◽  
Genomic Locus ◽  
Multicellular Development ◽  
Social Amoeba ◽  
The Social ◽  
A Cell

The social amoeba Dictyostelium discoideum is a tractable model organism to study cellular allorecognition, which is the ability of a cell to distinguish itself and its genetically similar relatives from more distantly related organisms. Cellular allorecognition is ubiquitous across the tree of life and affects many biological processes. Depending on the biological context, these versatile systems operate both within and between individual organisms, and both promote and constrain functional heterogeneity. Some of the most notable allorecognition systems mediate neural self-avoidance in flies and adaptive immunity in vertebrates. D. discoideum’s allorecognition system shares several structures and functions with other allorecognition systems. Structurally, its key regulators reside at a single genomic locus that encodes two highly polymorphic proteins, a transmembrane ligand called TgrC1 and its receptor TgrB1. These proteins exhibit isoform-specific, heterophilic binding across cells. Functionally, this interaction determines the extent to which co-developing D. discoideum strains co-aggregate or segregate during the aggregation phase of multicellular development. The allorecognition system thus affects both development and social evolution, as available evidence suggests that the threat of developmental cheating represents a primary selective force acting on it. Other significant characteristics that may inform the study of allorecognition in general include that D. discoideum’s allorecognition system is a continuous and inclusive trait, it is pleiotropic, and it is temporally regulated.

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.

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