scholarly journals Social selection within aggregative multicellular development drives morphological evolution

2021 ◽  
Vol 288 (1963) ◽  
Author(s):  
Marco La Fortezza ◽  
Gregory J. Velicer

Aggregative multicellular development is a social process involving complex forms of cooperation among unicellular organisms. In some aggregative systems, development culminates in the construction of spore-packed fruiting bodies and often unfolds within genetically and behaviourally diverse conspecific cellular environments. Here, we use the bacterium Myxococcus xanthus to test whether the character of the cellular environment during aggregative development shapes its morphological evolution. We manipulated the cellular composition of Myxococcus development in an experiment in which evolving populations initiated from a single ancestor repeatedly co-developed with one of several non-evolving partners—a cooperator, three cheaters and three antagonists. Fruiting body morphology was found to diversify not only as a function of partner genotype but more broadly as a function of partner social character, with antagonistic partners selecting for greater fruiting body formation than cheaters or the cooperator. Yet even small degrees of genetic divergence between distinct cheater partners sufficed to drive treatment-level morphological divergence. Co-developmental partners also determined the magnitude and dynamics of stochastic morphological diversification and subsequent convergence. In summary, we find that even just a few genetic differences affecting developmental and social features can greatly impact morphological evolution of multicellular bodies and experimentally demonstrate that microbial warfare can promote cooperation.

2021 ◽  
Author(s):  
Marco La Fortezza ◽  
Gregory Jon Velicer

The evolution of developmental systems might be shaped by both historical differences in developmental features and social selection, among other factors. In aggregative multicellularity, development is itself a social process in which unicellular organisms cooperate in carrying out complex developmental programs. In some aggregative systems, development culminates in the construction of spore-packed fruiting bodies. Fruiting body development in myxobacteria often unfolds within genetically and behaviorally diverse conspecific cellular environments that can include social defection and warfare. Here we use the bacterium Myxococcus xanthus to test whether the character of the cellular environment during aggregative development shapes morphological evolution. We manipulated the cellular composition of Myxococcus development in an experiment in which evolving populations initiated from a single ancestor repeatedly co-developed with one of several non-evolving partners - a benign cooperator, one of three cheaters or one of three antagonists. Fruiting body morphology was found to diversify as a function of developmental partners, revealing adaptation specific to distinct cellular environments. Collectively, antagonistic partners selected for higher levels of robust fruiting body formation than did cheaters or the benign cooperator. Moreover, even small degrees of genetic divergence between the distinct cheater partners were sufficient to drive treatment-level morphological divergence. Co-developmental partners not only shaped mean trait evolution but also determined the magnitude and dynamics of stochastic morphological diversification and subsequent convergence. In sum, we find that even few genetic differences affecting developmental and social features can greatly impact the morphological evolution of multicellular bodies and experimentally demonstrate that microbial warfare can promote cooperation.


2007 ◽  
Vol 189 (15) ◽  
pp. 5675-5682 ◽  
Author(s):  
James E. Berleman ◽  
John R. Kirby

ABSTRACT Myxococcus xanthus is a predatory bacterium that exhibits complex social behavior. The most pronounced behavior is the aggregation of cells into raised fruiting body structures in which cells differentiate into stress-resistant spores. In the laboratory, monocultures of M. xanthus at a very high density will reproducibly induce hundreds of randomly localized fruiting bodies when exposed to low nutrient availability and a solid surface. In this report, we analyze how M. xanthus fruiting body development proceeds in a coculture with suitable prey. Our analysis indicates that when prey bacteria are provided as a nutrient source, fruiting body aggregation is more organized, such that fruiting bodies form specifically after a step-down or loss of prey availability, whereas a step-up in prey availability inhibits fruiting body formation. This localization of aggregates occurs independently of the basal nutrient levels tested, indicating that starvation is not required for this process. Analysis of early developmental signaling relA and asgD mutants indicates that they are capable of forming fruiting body aggregates in the presence of prey, demonstrating that the stringent response and A-signal production are surprisingly not required for the initiation of fruiting behavior. However, these strains are still defective in differentiating to spores. We conclude that fruiting body formation does not occur exclusively in response to starvation and propose an alternative model in which multicellular development is driven by the interactions between M. xanthus cells and their cognate prey.


2020 ◽  
Vol 14 (2) ◽  
pp. 435-459
Author(s):  
Harold W. Keller ◽  
Relf L. Price ◽  
Billy G. Stone ◽  
Edward D. Forrester

Arcyria versicolor (Trichiales: Trichiaceae) is a distinct myxomycete species described by William Phillips in 1877. The genus Arcyria dates back to Linnaeus in 1753 through the species A. denudata. Arcyria sporangia are brightly colored red, yellow, grey or white, mostly stalked, often in large groups easily seen with the naked eye. Approximately 54 species are known, many are common, and distributed worldwide. Collectors often encounter these colorful species on decaying logs as clusters of many sporangia often covering extensive areas. Arcyria versicolor, collected in the Valles Caldera National Preserve located in the Jemez Mountains of north central New Mexico, is a new record for the state. The nomenclatural history of this species is reviewed and the justification for selection of the species name versicolor is discussed. Arcyria versicolor is accepted as the valid species name and A. vitellina a synonym after examination of type specimens. Environmental parameters for coloration are discussed in general for fruiting bodies of Arcyria and more specifically for nivicolous snowbank species. Transitional stages of plasmodial color to mature fruiting body formation are described for Arcyria versicolor. More than 140 specimens of Arcyria versicolor fruiting bodies were examined with light microscopy and in part illustrated with multifocal computer stacked imaging. Higher magnifications were highlighted using scanning electron microscopy. A more complete and accurate species description is provided for Arcyria versicolor. Differences of fruiting body morphology including habit, color, dehiscence, peridial inner and outer surface features, capillitial ornamentation and size, spore color, size, and ornamentation, and stalk spore-like bodies are described and illustrated. Observation of type specimens from the type locality is illustrated, discussed, and nomenclatural evaluation given for the name selected. Mountain myxomycetes are reviewed based on the observations of T.H. Macbride and his early 1914 paper published in Mycologia. Collection data is presented that compares the dark-spored and light spored nivicolous myxomycetes in the French Alps. The history of renown collectors of nivicolous myxomycetes in western mountains of U.S.A. documents the discovery and study of this special ecological group of myxomycetes. This current paper is the first in a series from an ongoing research project entitled Myxomycetes of New Mexico.


2006 ◽  
Vol 189 (2) ◽  
pp. 611-619 ◽  
Author(s):  
Oleksii Sliusarenko ◽  
David R. Zusman ◽  
George Oster

ABSTRACT When starved, Myxococcus xanthus cells assemble themselves into aggregates of about 105 cells that grow into complex structures called fruiting bodies, where they later sporulate. Here we present new observations on the velocities of the cells, their orientations, and reversal rates during the early stages of fruiting body formation. Most strikingly, we find that during aggregation, cell velocities slow dramatically and cells orient themselves in parallel inside the aggregates, while later cell orientations are circumferential to the periphery. The slowing of cell velocity, rather than changes in reversal frequency, can account for the accumulation of cells into aggregates. These observations are mimicked by a continuous agent-based computational model that reproduces the early stages of fruiting body formation. We also show, both experimentally and computationally, how changes in reversal frequency controlled by the Frz system mutants affect the shape of these early fruiting bodies.


2017 ◽  
Vol 5 (40) ◽  
Author(s):  
Anke Treuner-Lange ◽  
Marc Bruckskotten ◽  
Oliver Rupp ◽  
Alexander Goesmann ◽  
Lotte Søgaard-Andersen

ABSTRACT Members of the Myxococcales order initiate a developmental program in response to starvation that culminates in formation of spore-filled fruiting bodies. To investigate the genetic basis for fruiting body formation, we present the complete 8.9-Mb genome sequence of Myxococcus macrosporus strain DSM 14697, generated using the PacBio sequencing platform.


1998 ◽  
Vol 180 (5) ◽  
pp. 1241-1247 ◽  
Author(s):  
Barbara Silakowski ◽  
Heidi Ehret ◽  
Hans Ulrich Schairer

ABSTRACT Stigmatella aurantiaca is a gram-negative bacterium which forms, under conditions of starvation in a multicellular process, characteristic three-dimensional structures: the fruiting bodies. For studying this complex process, mutants impaired in fruiting body formation have been induced by transposon insertion with a Tn5-derived transposon. The gene affected (fbfB) in one of the mutants (AP182) was studied further. Inactivation of fbfB results in mutants which form only clumps during starvation instead of wild-type fruiting bodies. This mutant phenotype can be partially rescued, if cells of mutants impaired in fbfB function are mixed with those of some independent mutants defective in fruiting before starvation. The fbfBgene is expressed about 14 h after induction of fruiting body formation as determined by measuring β-galactosidase activity in a merodiploid strain harboring the wild-type gene and anfbfB-Δtrp-lacZ fusion gene or by Northern (RNA) analysis with the Rhodobacter capsulatus pufBA fragment fused tofbfB as an indicator. The predicted polypeptide FbfB has a molecular mass of 57.8 kDa and shows a significant homology to the galactose oxidase (GaoA) of the fungus Dactylium dendroides. Galactose oxidase catalyzes the oxidation of galactose and primary alcohols to the corresponding aldehydes.


Author(s):  
Shuai Zhou ◽  
Xiaoyu Zhang ◽  
Fuying Ma ◽  
Shangxian Xie ◽  
Chuanhong Tang ◽  
...  

To systemically understand the biosynthetic pathways of bioactive substances, including triterpenoids and polysaccharides, in Ganoderma lucidum, the correlation between substrate degradation, carbohydrate and triterpenoid metabolism during growth was analyzed by combining changes in metabolite content and changes in related enzyme expression in G. lucidum over 5 growth phases. Changes in low-polarity triterpenoid content were correlated with changes in glucose and mannitol content in fruiting bodies. Additionally, changes in medium-polarity triterpenoid content were correlated with changes in the lignocellulose content of the substrate and with the glucose, trehalose and mannitol contents of fruiting bodies. Weighted gene coexpression network analysis (WGCNA) indicated that changes in trehalose and polyol content were related to carbohydrate catabolism and polysaccharide synthesis. Changes in triterpenoid content were related to expression of the carbohydrate catabolic enzymes, laccase, cellulase, hemicellulase, and polysaccharide synthase and to the expression of several cytochrome P450 monooxygenases (CYPs). It was concluded that the products of cellulose and hemicellulose degradation participate in polyol, trehalose and polysaccharide synthesis during initial fruiting body formation. These carbohydrates accumulate in the early phase of fruiting body formation and are utilized when the fruiting bodies mature and a large number of spores are ejected. An increase in carbohydrate metabolism provides additional precursors for the synthesis of triterpenoids. Importance Most studies of G. lucidum have focused on its medicinal function and on the mechanism of its activity, whereas the physiological metabolism and synthesis of bioactive substances during the growth of this species have been less studied. Therefore, theoretical guidance for cultivation methods to increase the production of bioactive compounds remains lacking. This study integrated changes in the lignocellulose, carbohydrate and triterpenoid contents of G. lucidum with enzyme expression from transcriptomics data using WGCNA. The findings helped us better understand the connections between substrate utilization and the synthesis of polysaccharides and triterpenoids during the cultivation cycle of G. lucidum. The results of WGCNA suggest that the synthesis of triterpenoids can be enhanced not only through regulating the expression of enzymes in the triterpenoid pathway, but also through regulating carbohydrate metabolism and substrate degradation. This study provides a potential approach and identifies enzymes that can be targeted to regulate lignocellulose degradation and accelerate the accumulation of bioactive substances by regulating substrate degradation in G. lucidum.


Development ◽  
1978 ◽  
Vol 48 (1) ◽  
pp. 153-160
Author(s):  
M. Saito ◽  
K. Yanagisawa

Dictyostelium purpureum S5 and S6, mating type strains, form fruiting-bodies in a monoclonal culture, but produce macrocysts in a mix culture. The effects of Concanavalin A (Con A) on both fruiting-body formation and macrocyst formation, and changes of Con Amediated cell agglutinability during development were studied. It was found that Con A inhibits macrocyst formation but not fruiting-body formation, and that macrocyst-forming cells are much more susceptible to Con A agglutination than are fruiting-body-forming cells during the aggregation stages. When fruiting-body-forming cells are treated with either trypsin or α-chymotrypsin, their Con A agglutinability is enhanced to the same extent as that of macrocyst-forming cells. It was also found that when S6 cells are treated with proteases they sometimes produce normal macrocysts even in a monoclonal culture. The results obtained in these experiments showed that the surface properties of fruitingbody- forming cells and macrocyst-forming cells are different, and that the cell surface might play an important role in determining the two developmental courses.


2005 ◽  
Vol 4 (9) ◽  
pp. 1599-1602 ◽  
Author(s):  
Silvia Gabella ◽  
Simona Abbà ◽  
Sebastien Duplessis ◽  
Barbara Montanini ◽  
Francis Martin ◽  
...  

ABSTRACT cDNA arrays were used to explore mechanisms controlling fruiting body development in the truffle Tuber borchii. Differences in gene expression were higher between reproductive and vegetative stage than between two stages of fruiting body maturation. We suggest hypotheses about the importance of various physiological processes during the development of fruiting bodies.


2006 ◽  
Vol 189 (1) ◽  
pp. 169-178 ◽  
Author(s):  
Marielena Chavira ◽  
Nga Cao ◽  
Karen Le ◽  
Tanveer Riar ◽  
Navid Moradshahi ◽  
...  

ABSTRACT Myxococcus xanthus, a gram-negative soil bacterium, responds to amino acid starvation by entering a process of multicellular development which culminates in the assembly of spore-filled fruiting bodies. Previous studies utilizing developmental inhibitors (such as methionine, lysine, or threonine) have revealed important clues about the mechanisms involved in fruiting body formation. We used Biolog phenotype microarrays to screen 384 chemicals for complete inhibition of fruiting body development in M. xanthus. Here, we report the identification of a novel inhibitor of fruiting body formation and sporulation, β-d-allose. β-d-Allose, a rare sugar, is a member of the aldohexose family and a C3 epimer of glucose. Our studies show that β-d-allose does not affect cell growth, viability, agglutination, or motility. However, β-galactosidase reporters demonstrate that genes activated between 4 and 14 h of development show significantly lower expression levels in the presence of β-d-allose. Furthermore, inhibition of fruiting body formation occurs only when β-d-allose is added to submerged cultures before 12 h of development. In competition studies, high concentrations of galactose and xylose antagonize the nonfruiting response to β-d-allose, while glucose is capable of partial antagonism. Finally, a magellan-4 transposon mutagenesis screen identified glcK, a putative glucokinase gene, required for β-d-allose-mediated inhibition of fruiting body formation. Subsequent glucokinase activity assays of the glcK mutant further supported the role of this protein in glucose phosphorylation.


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