dsg, a gene required for cell-cell interaction early in Myxococcus development

Cheng, Yvonne; Kaiser, Dale

doi:10.1128/jb.171.7.3719-3726.1989

Cited by 51 publications

(44 citation statements)

References 25 publications

(18 reference statements)

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“…RNA from growing DK1622, DK6206, DK6216, DK6250, and DK6213 cells was probed with DNA specific for the mgl region. DNA from the dsg gene, a vital gene that is expressed during growth (9), was used to ensure that similar amounts of RNA from each strain had been loaded into the gel. Although there is some change in the distribution of RNA lengths between strains, overall amounts of mgl RNA were similar.…”

Section: Resultsmentioning

confidence: 99%

Upstream gene of the mgl operon controls the level of MglA protein in Myxococcus xanthus

Hartzell

Kaiser

1991

J Bacteriol

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The mgl operon contains two open reading frames (ORFs) which are transcribed together. A collection of nonmotile mutants helped to define the downstream ORF as the mglA gene. Single mutations at the mglA locus completely abolish motility. A series of deletion mutations was constructed to determine the role of the upstream ORF (now called mglB). A strain carrying a deletion in mglB and with an intact mglA produces small colonies. The cells are motile, but their rate of swarm spreading is reduced. Measurements of cell movement showed that mglB mutant cells advanced, on average, less than 0.1 cell length in 5 min. The mglB+ cells advanced an average of 1.3 cell lengths in the same time. Extracts of AmglB cells contain 15 to 20% as much of the 22-kDa MglA protein as do mglB+ cells, as measured in Western immunoblots and enzyme-linked immunosorbent assays. However, the amount of mgl transcript is the same in the AmglB mutants as in the mglB+ strain. Heterozygous partial diploids mglBImglA with the wild-type alleles in trans have normal motility, demonstrating that the largest of the mglB deletions is not polar on mglA. Like other motility defects, a AmglB mutation alters fruiting body development and sporulation. The mglB mutants delayed aggregation, produced small immature fruiting bodies, and sporulated at 45 to 50% wild-type levels. All aspects of the mglB mutant phenotype are explained by the reduced levels of mglA protein and the assumption that it limits the amount of gliding.Gliding motility is defined as translocation over a solid surface and involves movement in the direction of the long axis of the cell (8). In all known gliding organisms, movement is correlated with the production of slime. There is occasional reversal of direction, but motion is smooth, with no rotation apparent. No appendages, which would suggest a mechanism for gliding, have been identified. Gliding is employed by a diverse group of organisms, including Cytophaga and Flexibacter spp., the myxobacteria, and the filamentous cyanobacteria, all of which belong to evolutionarily different groups (33). These organisms range in length from 5 to 50 ,um and glide at rates of 1 to 300 pum/min. While different explanations for gliding have been proposed for different organisms (directional extrusion of slime [24], polar release of surfactant [12], and movement by contraction [8,26], for example), the molecular mechanism of gliding remains unsettled.Genes that regulate the pattern of gliding motility have been found. Two genetically independent sets of genes, called the adventurous (A) and social (S) motility systems, have been identified in Myxococcus xanthus (18,19

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Section: Resultsmentioning

confidence: 99%

Upstream gene of the mgl operon controls the level of MglA protein in Myxococcus xanthus

Hartzell

Kaiser

1991

J Bacteriol

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“…The developmentally proficient parent strain, M. xanthus DK1622 (13), and developmental mutant strains DK3260 and DK3261 (dsg) (2,15), DK5057 (asg) (9), and M380 (bsg) (8) were supplied by the laboratory of D. Kaiser. The csg mutant strain (DK2653) was supplied by L. Shimkets (28).…”

Section: Methodsmentioning

confidence: 99%

Role of autocide AMI in development of Myxococcus xanthus

Rosenbluh

Rosenberg

1990

J Bacteriol

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A new developmental mutant of Myxococcus xanthus has been isolated by screening TnV insertion mutants for AMI-dependent development in submerged culture. This mutant (ER304) aggregated and sporulated on agar surfaces but required at least 3.8 ,ug of autocide AMI per ml for development in submerged cultures. Spore rescue of ER304 was obtained with the saturated, monounsaturated, and diunsaturated fatty acid fractions of AMI, with specific activities of 68, 115, and 700 U/mg, respectively. In addition, several model fatty acids were capable of rescuing sporulation of ER304; however, there was no correlation between specific lytic activity observed in vegetative cultures and specific rescue activity. Rescue of ER304 was effected during the first ca. 12 h after the initiation of starvation conditions; after this time, addition of AMI or model fatty acids killed the cells. Supernatant fluids of ER304 rescued development in dsg mutants (e.g., DK3260) in submerged cultures, but dsg mutant supernatant fluids were incapable of rescuing ER304 development. The data presented in this article support the idea that the primary mechanism of rescue by AMI is not via lysis, although developmental lysis may be an indirect result of the rescue event. A membrane permeability model is presented to explain the role of autocides in early developmental events in wild-type strains and in the aggregation and sporulation rescue of developmental mutants ER304 and DK3260.Myxococcus xanthus, the most extensively studied member of the Myxobacterales, is a gram-negative, gliding bacterium, characterized by a complex, multicellular development program (33). Development of M. xanthus, which culminates in the building of spore-filled fruiting bodies, is contingent upon the fulfillment of several conditions: (i) a minimal cell density, (ii) a solid substratum to support the aggregating cells, and (iii) nutritional downshift of exponentially growing cells (25). Successful completion of the developmental process depends upon the proper functioning of many genes. Some of these genes are directly involved in the intercellular signaling necessary for coordinating specific multicellular activities (16); others affect development by controlling the motility (11, 12) or cohesiveness (27) of the cells.Autocides are substances produced by vegetative M. xanthus cells which are capable of inducing lysis in the producing and related strains (29). The two major autocides, referred to as AMI and AMV, have been isolated and chemically characterized (6, 30). Autocide AMV is phosphatidylethanolamine (PE), the major component of the inner and outer cell membranes of M. xanthus. Autocide AMI, a mixture of saturated, monounsaturated, and polyunsaturated fatty acids, appears to be an enzymatic breakdown product of AMV and its active lytic moiety. In addition to its autolytic activity, autocide AMI has recently been shown to be capable of accelerating aggregation and sporulation in the wild-type strain and of rescuing aggregation and sporulation in dsg development mutan...

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“…Assay of [3-galactosidase activity in asg, bsg, csg, or dsg strains containing lacZ fusions indicates that developmental gene expression is disrupted in these cell-interaction mutants but can be restored by extracellular complementation (Gill and Cull 1986;Kuspa et al 1986;Kroos and Kaiser 1987;Cheng and Kaiser 1989). Each group arrests development at a different stage, judged by morphology and by gene expression within the panel of fusions.…”

Section: Control Of M Xanthus Fruiting Body Development Bymentioning

confidence: 99%

Cell motility is required for the transmission of C-factor, an intercellular signal that coordinates fruiting body morphogenesis of Myxococcus xanthus.

Kim¹,

Kaiser²

1990

Genes Dev.

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There are striking similarities between the developmental phenotypes of two different mutant classes of Mgxococcus xanthus. The first class, mglA mutants, are nonmotile under all conditions tested. The second class, csgA mutants, are motile but belong to a class of signal-defective developmental mutants that cannot develop alone but will develop when mixed with intact wild-type cells. Nevertheless, both csgA and mglA mutants fail to aggregate properly or to sporulate when induced to form fruiting bodies. An mg/A mutation and a csgA mutation affect expression of a panel of lacZ fusions to developmental genes in the same way, indicating that nonmotile cells and csgA cells arrest development at a similar stage. One explanation for the similarity of developmental phenotypes between these mutants is that motility is required for the csgAmediated cell interaction. In support of this hypothesis, we report that C-factor, a protein purified from nascent wild-type fruiting bodies based on its ability to rescue csgA mutant fruiting body development, also rescues sporulation and expression of I~-galactosidase from developmentally controlled lacZ fusions in mglA strains, apparently without restoring their motility. Wild-type levels of active C-factor can be purified from mglA cells, yet intact mglA cells do not rescue csgA cells upon cell-cell mixing. Intact wild-type cells are unable to restore the sporulation and 13-galactosidase expression of mglA mutants. These results support the hypothesis that donor and responder cell motility is required for C-factor transmission between cells during development. We propose that proper intercellular C-factor transmission may require a critical spatial orientation of cells achieved only after cells move into the dense, aligned organization of a nascent fruiting body.

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dsg, a gene required for cell-cell interaction early in Myxococcus development

Cited by 51 publications

References 25 publications

Upstream gene of the mgl operon controls the level of MglA protein in Myxococcus xanthus

Upstream gene of the mgl operon controls the level of MglA protein in Myxococcus xanthus

Role of autocide AMI in development of Myxococcus xanthus

Cell motility is required for the transmission of C-factor, an intercellular signal that coordinates fruiting body morphogenesis of Myxococcus xanthus.

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