scholarly journals Group Maintenance in Aggregative Multicellularity

2021 ◽  
Author(s):  
Israt Jahan ◽  
Tyler Larsen ◽  
Joan Strassmann ◽  
David Queller
Keyword(s):  
Single Cell ◽  
Dictyostelium Discoideum ◽  
Myxococcus Xanthus ◽  
Clonal Organisms ◽  
Social Goods ◽  
Multicellular Organisms ◽  
Dispersed Cells

Aggregative multicellularity occurs when dispersed cells join together to form a highly cooperative unit, in contrast to clonal multicellular organisms formed by cells that remain in contact after descent from a single cell. Because aggregative groups may include non-relatives, aggregative multicellular organisms should be particularly vulnerable to the rise of cheater cells that take advantage of social goods without paying the costs, reducing cooperation, and even threatening extinction. We review the key mechanisms by which aggregative multicellular organisms control cheaters with a focus on the best studied aggregative organisms, Myxococcus xanthus and Dictyostelium discoideum. These include various passive and active mechanisms to maintain high relatedness within aggregates, to enforce cooperation on aggregate members, and the costs of cheating on other key functions. Ultimately, aggregative multicellular organisms are not that different from clonal organisms descended from a single cell.

Cell movement within aggregates of the slime mould Dictyostelium discoideum revealed by surface markers

Development ◽  
1965 ◽  
Vol 13 (1) ◽  
pp. 97-117
Author(s):  
B. M. Shaffer
Keyword(s):  
Dictyostelium Discoideum ◽  
Cell Movement ◽  
Surface Markers ◽  
Slime Mould ◽  
Culture Plate ◽  
Multicellular Organisms

Earlier workers examined the behaviour of foreign particles placed as markers on aggregates of D. discoideum that were migrating over the surface of the culture plate (Bonner, 1959; Francis, 1959, 1962). Comparable observations, made on aggregates in other conditions and at other stages, have now provided further information about the movement of individual cells within the aggregates. Before reporting them, the course of development must be described in some detail. During aggregation on an ordinary culture plate, D. discoideum amoebae crawl towards centres, in which they pack themselves together, forming rounded aggregates of no fixed shape. Papillae develop on the side of the aggregates away from the agar, and by extension, roughly perpendicular to the substratum, transform them into cylindrical multicellular organisms with tapered tips (Text-fig. 1, A—E). Such an organism, which contains from a dozen to a few hundred thousand cells, has been named a grex (Shaffer, 1962) because ‘aggregation’ is derived from the Latin aggregare, to form a grex.

Characterisation of an epithelium-like layer of cells in the multicellular Dictyostelium discoideum slug

1993 ◽  
Vol 105 (1) ◽  
pp. 243-253
Author(s):  
M. Fuchs ◽  
M.K. Jones ◽  
K.L. Williams
Keyword(s):  
Dictyostelium Discoideum ◽  
Intercellular Space ◽  
Room Temperature ◽  
Cell Layer ◽  
Freeze Substitution ◽  
Specific Cell ◽  
Peripheral Layer ◽  
Apical Membranes ◽  
Multicellular Organisms ◽  
Peripheral Cells

Ultrarapid freezing (RF) followed by freeze-substitution (FS) provide superior preservation of the Dictyostelium discoideum multicellular slug tissue over conventional methods of chemical fixation at room temperature. The peripheral cells of slugs prepared by RF and FS form a tight layer of flattened cells. This cell layer resembles epithelia of other multicellular organisms in that it has close junctional contact between cells associated with the extracellular matrix (ECM, slime sheath). This is the first report that clearly demonstrates the existence of such peripheral cellular specialisation in this otherwise well-studied model system. Junctional contacts between adjacent cells mean that there is no intercellular space evident between apical membranes of apposing cells, and basally the intermembraneous space between peripheral cells is less than 10 nm. By contrast, the intercellular space between internal cells is approximately 10–25 nm. The shape of the peripheral cells varies with their location around the slug. In the posterior prespore zone, the peripheral cells are squamous and exhibit polarity along their antero-posterior axis. In the anterior prestalk zone, peripheral cells are less flattened, project irregular filipodia between internal cells, and are polarised along their apical-basal axis. Colloidal gold immunocytochemistry with the markers MUD1, MUD50 and MUD62 demonstrated that the peripheral layer is formed of prestalk cells in the anterior region and ventrum, and mostly prespore cells along the dorsum. Thus, the peripheral layer, while having specific cell classes in different regions, is not differentiation-specific. Rather, it appears that the structure of these epithelium-like cells is influenced by interaction with molecules of the ECM (sheath).

scholarly journals New avenues for systematically inferring cell-cell communication: through single-cell transcriptomics data

2020 ◽  
Vol 11 (12) ◽  
pp. 866-880 ◽  
Author(s):  
Xin Shao ◽  
Xiaoyan Lu ◽  
Jie Liao ◽  
Huajun Chen ◽  
Xiaohui Fan
Keyword(s):  
Single Cell ◽  
Communication Networks ◽  
Cell Communication ◽  
Receptor Interaction ◽  
Communication Studies ◽  
Transcriptomics Data ◽  
Phenotype Heterogeneity ◽  
Multicellular Organisms ◽  
Communication Study ◽  
Cell Cell

AbstractFor multicellular organisms, cell-cell communication is essential to numerous biological processes. Drawing upon the latest development of single-cell RNA-sequencing (scRNA-seq), high-resolution transcriptomic data have deepened our understanding of cellular phenotype heterogeneity and composition of complex tissues, which enables systematic cell-cell communication studies at a single-cell level. We first summarize a common workflow of cell-cell communication study using scRNA-seq data, which often includes data preparation, construction of communication networks, and result validation. Two common strategies taken to uncover cell-cell communications are reviewed, e.g., physically vicinal structure-based and ligand-receptor interaction-based one. To conclude, challenges and current applications of cell-cell communication studies at a single-cell resolution are discussed in details and future perspectives are proposed.

scholarly journals Role of epigenetics in unicellular to multicellular transition in Dictyostelium

2021 ◽  
Vol 22 (1) ◽  
Author(s):  
Simon Yuan Wang ◽  
Elizabeth Ann Pollina ◽  
I-Hao Wang ◽  
Lindsay Kristina Pino ◽  
Henry L. Bushnell ◽  
...  
Keyword(s):  
Dictyostelium Discoideum ◽  
Orthologous Gene ◽  
Chromatin Accessibility ◽  
Critical Event ◽  
H3k4 Methylation ◽  
Social Amoeba ◽  
The Social ◽  
Conserved Genes ◽  
Multicellular Organisms

Abstract Background The evolution of multicellularity is a critical event that remains incompletely understood. We use the social amoeba, Dictyostelium discoideum, one of the rare organisms that readily transits back and forth between both unicellular and multicellular stages, to examine the role of epigenetics in regulating multicellularity. Results While transitioning to multicellular states, patterns of H3K4 methylation and H3K27 acetylation significantly change. By combining transcriptomics, epigenomics, chromatin accessibility, and orthologous gene analyses with other unicellular and multicellular organisms, we identify 52 conserved genes, which are specifically accessible and expressed during multicellular states. We validated that four of these genes, including the H3K27 deacetylase hdaD, are necessary and that an SMC-like gene, smcl1, is sufficient for multicellularity in Dictyostelium. Conclusions These results highlight the importance of epigenetics in reorganizing chromatin architecture to facilitate multicellularity in Dictyostelium discoideum and raise exciting possibilities about the role of epigenetics in the evolution of multicellularity more broadly.

The developmental regulation of single-cell motility in Dictyostelium discoideum

1986 ◽  
Vol 113 (1) ◽  
pp. 218-227 ◽  
Author(s):  
Barbara Varnum ◽  
Kevin B. Edwards ◽  
David R. Soll
Keyword(s):  
Cell Motility ◽  
Single Cell ◽  
Dictyostelium Discoideum ◽  
Developmental Regulation

scholarly journals Multilevel selection favors fragmentation modes that maintain cooperative interactions in multispecies communities

2021 ◽  
Vol 17 (9) ◽  
pp. e1008896
Author(s):  
Gil J. B. Henriques ◽  
Simon van Vliet ◽  
Michael Doebeli
Keyword(s):  
Single Cell ◽  
Optimal Strategies ◽  
Single Species ◽  
Multilevel Selection ◽  
Case Group ◽  
Cooperative Interactions ◽  
Size Dependent ◽  
Species Groups ◽  
Ecological Success ◽  
Multicellular Organisms

Reproduction is one of the requirements for evolution and a defining feature of life. Yet, across the tree of life, organisms reproduce in many different ways. Groups of cells (e.g., multicellular organisms, colonial microbes, or multispecies biofilms) divide by releasing propagules that can be single-celled or multicellular. What conditions determine the number and size of reproductive propagules? In multicellular organisms, existing theory suggests that single-cell propagules prevent the accumulation of deleterious mutations (e.g., cheaters). However, groups of cells, such as biofilms, sometimes contain multiple metabolically interdependent species. This creates a reproductive dilemma: small daughter groups, which prevent the accumulation of cheaters, are also unlikely to contain the species diversity that is required for ecological success. Here, we developed an individual-based, multilevel selection model to investigate how such multi-species groups can resolve this dilemma. By tracking the dynamics of groups of cells that reproduce by fragmenting into smaller groups, we identified fragmentation modes that can maintain cooperative interactions. We systematically varied the fragmentation mode and calculated the maximum mutation rate that communities can withstand before being driven to extinction by the accumulation of cheaters. We find that for groups consisting of a single species, the optimal fragmentation mode consists of releasing single-cell propagules. For multi-species groups we find various optimal strategies. With migration between groups, single-cell propagules are favored. Without migration, larger propagules sizes are optimal; in this case, group-size dependent fissioning rates can prevent the accumulation of cheaters. Our work shows that multi-species groups can evolve reproductive strategies that allow them to maintain cooperative interactions.

scholarly journals A Critical-like Collective State Leads to Long-range Cell Communication in Dictyostelium discoideum Aggregation

2016 ◽  
Author(s):  
Giovanna De Palo ◽  
Darvin Yi ◽  
Robert G. Endres
Keyword(s):  
Single Cell ◽  
Dictyostelium Discoideum ◽  
Long Range ◽  
Early Development ◽  
Cell Communication ◽  
Multiscale Model ◽  
Wild Type ◽  
Social Amoeba ◽  
Range Cell ◽  
Cell Cell

AbstractThe transition from single-cell to multicellular behavior is important in early development but rarely studied. The starvation-induced aggregation of the social amoeba Dictyostelium discoideum into a multicellular slug is known to result from single-cell chemotaxis towards emitted pulses of cyclic adenosine monophosphate (cAMP). However, how exactly do transient short-range chemical gradients lead to coherent collective movement at a macroscopic scale? Here, we developed a multiscale model verified by quantitative microscopy to describe wide-ranging behaviors from chemotaxis and excitability of individual cells to aggregation of thousands of cells. To better understand the mechanism of long-range cell-cell communication and hence aggregation, we analyzed cell-cell correlations, showing evidence of self-organization at the onset of aggregation (as opposed to following a leader cell). Surprisingly, cell collectives, despite their finite size, show features of criticality known from phase transitions in physical systems. By comparing wild-type and mutant cells with impaired aggregation, we found the longest cellcell communication distance in wild-type cells, suggesting that criticality provides an adaptive advantage and optimally sized aggregates for the dispersal of spores.Author SummaryCells are often coupled to each other in cell collectives, such as aggregates during early development, tissues in the developed organism, and tumors in disease. How do cells communicate over macroscopic distances much larger than the typical cell-cell distance to decide how they should behave? Here, we developed a multiscale model of social amoeba, spanning behavior from individuals to thousands of cells. We show that local cell-cell coupling via secreted chemicals may be tuned to a critical value, resulting in emergent long-range communication and heightened sensitivity. Hence, these aggregates are remarkably similar to bacterial biofilms and neuronal networks, all communicating in a pulse-like fashion. Similar organizing principles may also aid our understanding of the remarkable robustness in cancer development.

scholarly journals Role of Epigenetics in Unicellular to Multicellular Transition in Dictyostelium

2020 ◽  
Author(s):  
Simon Yuan Wang ◽  
Elizabeth Ann Pollina ◽  
I-Hao Wang ◽  
Henry L. Bushnell ◽  
Ken Takashima ◽  
...  
Keyword(s):  
Dictyostelium Discoideum ◽  
Epigenetic Regulation ◽  
Chromatin Accessibility ◽  
Critical Event ◽  
H3k4 Methylation ◽  
Social Amoeba ◽  
The Social ◽  
Conserved Genes ◽  
Multicellular Organisms

AbstractThe evolution of multicellularity is a critical event that remains incompletely understood. We use the social amoeba, Dictyostelium discoideum, one of the rare organisms that exists in both unicellular and multicellular stages, to examine the role of epigenetics in regulating multicellularity. While transitioning to multicellular states, patterns of H3K4 methylation and H3K27 acetylation significantly change. By combining transcriptomics, epigenomics, chromatin accessibility, and syntenic analyses with other unicellular and multicellular organisms, we identify 52 conserved genes, which are specifically accessible and expressed during multicellular states. We validated that four of these genes, including the H3K27 deacetylase hdaD, are necessary and that an SMC-like gene, smcl1, is sufficient for multicellularity. These results highlight the importance of epigenetics in reorganizing chromatin architecture to facilitate the evolution of multicellularity.One Sentence SummaryEpigenetic regulation of multicellularity

scholarly journals Genetic and Molecular Analysis of cglB, a Gene Essential for Single-Cell Gliding in Myxococcus xanthus

1999 ◽  
Vol 181 (14) ◽  
pp. 4381-4390 ◽  
Author(s):  
Ana M. Rodriguez ◽  
Alfred M. Spormann
Keyword(s):  
Single Cell ◽  
Myxococcus Xanthus ◽  
Gliding Motility ◽  
Open Reading Frames ◽  
Wild Type Allele ◽  
Wild Type ◽  
Isolated Cells ◽  
Type Allele ◽  
C Terminus ◽  
Mutant Cells

ABSTRACT Gliding movements of individual isolated Myxococcus xanthus cells depend on the genes of the A-motility system (agl and cgl genes). Mutants carrying defects in those genes are unable to translocate as isolated cells on solid surfaces. The motility defect of cgl mutants can be transiently restored to wild type by extracellular complementation upon mixing mutant cells with wild-type or other motility mutant cells. To develop a molecular understanding of the function of a Cgl protein in gliding motility, we cloned the cglB wild-type allele by genetic complementation of the mutant phenotype. The nucleotide sequence of a 2.85-kb fragment was determined and shown to encode two complete open reading frames. The CglB protein was determined to be a 416-amino-acid putative lipoprotein with an unusually high cysteine content. The CglB antigen localized to the membrane fraction. The swarming and gliding defects of a constructed ΔcglBmutant were fully restored upon complementation with thecglB wild-type allele. Experiments with a cglBallele encoding a CglB protein with a polyhistidine tag at the C terminus showed that this allele also promoted wild-type levels of swarming and single-cell gliding, but was unable to stimulate ΔcglB cells to move. Possible functions of CglB as a mechanical component or as a signal protein in single cell gliding are discussed.

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