MICROBIOLOGICAL REVIEWS, Dec. 1990, p. 473-501 Vol. 54, No. 4 0146-0749/90/040473-29$02.00/0 Copyright © 1990, American Society for Microbiology Social and Developmental Biology of the Myxobacteria LAWRENCE J. SHIMKETS Department of Microbiology, University of Georgia, Athens, Georgia 30602 INTRODUCTION ............................................... 473 TAXONOMY AND LIFE CYCLE ................................................ 473 SOCIAL AND DEVELOPMENTAL BEHAVIORS ............................................... 475 Two Multigene Systems Govern Gliding-Cell Behavior ............................................... 476 Adventurous motility ............................................... 478 Social motility ................................................ 478 Other loci controlling gliding-cell behavior ............................................... 480 Cooperative Growth ............................................... 480 Rippling, a Periodic Behavior ............................................... 481 Fruiting-Body Morphogenesis ............................................... 482 M. xanthus ............................................... 483 S. aurantiaca ............................................... 485 Sporulation ............................................... 485 Cell-cell interactions during sporulation ............................................... 487 Involvement of the phase variation............................................... 489 NUTRITIONAL CONTROL OF DEVELOPMENT............................................... 489 ORGANIZATION OF THE DEVELOPMENTAL PATHWAY ............................................... 489 ANALYSIS OF THE GENOME............................................... 490 Multicopy Single-Stranded DNA................................................ 491 Genome Size ............................................... 491 Cell Cycle............................................... 494 EVOLUTIONARY CONSIDERATIONS ................................................ 494 CONCLUSIONS ............................................... 494 ACKNOWLEDGMENTS ............................................... 494 LITERATURE CITED............................................... 494 INTRODUCTION bution. Although myxobacteria are a common and perhaps even significant component of many aerated soil ecosys- The myxobacteria are distinguished from other bacteria by tems, it has been difficult to determine their actual numbers their remarkable social behaviors, most notably the forma- because of their slow growth, the lack of a selective medium, tion ofmulticellular fruiting bodies containing dormant myxo- and the propensity of the cells to stick to one another. spores. Many of these behaviors were recorded 25 years ago Neutral or slightly alkaline soils can contain as many as in a series of films by Reichenbach and colleagues that have 450,000 cells per g (157, 238), and decomposing compost inspired much of the research described in this article (198, contains more than 500,000 cells per g (238). Despite the 202, 204-207). Continued research in this area will undoubt- prevalence of myxobacteria in soil systems, virtually nothing edly provide insights into the molecular mechanisms of these is known of their contribution to soil ecology. Myxobacteria behaviors. Most studies on the biology of social behavior are microbial predators, and it is likely that they play a role have been limited to one species, Myxococcus xanthus, in controlling the population size of certain soil microorgan- which has an excellent genetic system and is amenable to a isms. variety of experimental approaches. Several studies on Myxobacteria contain a vast reservoir of antibiotics with Stigmatella aurantiaca suggest that it is a complementary unusual chemical structures (203, 217). Between 60 and 80% system worthy of continued investigation. This article will of more than 800 wild isolates produce antibiotics with focus on the social and developmental biology of the myxo- chemical structures that have not been described before bacteria, primarily these two species. Information concern- (203) (Fig. 1). Several of these antibiotics may prove to be ing aspects of myxobacterial research not covered in this clinically useful. Sorangicin inhibits transcription initiation article may be found in a book (215) and in several review in eubacteria and shows some promise as a broad-spectrum articles (47, 50, 110, 111, 158, 199, 201, 229, 230, 270, 284; antibacterial compound (102). Ambruticin is an antifungal D. R. Zusman, in M. Inouye, J. Campisi, D. Cunningham, antibiotic (211) that is effective in the treatment of systemic and M. Riley, ed., Gene Expression and Regulation of Cell mycoses (137). Growth and Development, in press; D. R. Zusman, M. J. McBride, W. R. McCleary, and K. A. O'Connor, Symp. Soc. Gen. Microbiol., in press; B. C. Lampson, S. Inouye, TAXONOMY AND LIFE CYCLE and M. Inouye, submitted for publication). All myxobacterial species appear to be related on the basis The resistance of myxospores to desiccation and freezing of their DNA base composition, which is 67 to 71 mol% enables myxobacteria to survive seasonally harsh environ- G+C (145, 159), and 16S rRNA oligonucleotide cataloging ments such as arid deserts and arctic tundra and may have (140). Comparison of the 16S rRNA molecules from a variety been the major factor contributing to their worldwide distri- of myxobacteria indicate that they are a distinct taxonomic 473 474 SHIMKETS MICROBIOL. REV. ow (A) - ; (B) 0N (L) HO~~~~~- ON M OH 02N OH 33A 7 o (C) 0 Cl 0 4 s (N) ~0 HO' - 2 46 27 6 COOH H _ ~~~~~~~~~CH2Om 523R 45 44 HO H 18 23 NN 0 ~~~~~~~~~~H (E) (G) N H CO NH2 HN MeO 0 0 OMe OMe 123 OMe OH 0 H OH MeO 0 OH '"OH 610 CH (F) CH30 N 13- CH3 0 NH R OCH3 (K) 231 OMe 0 CH3 N ANH2 0 ,I, <U%,NX(NY%N)H& 0N j IH- (J) (P) FIG. 1. Antibiotics isolated from the myxobacteria (203). (A) Angiolam A; (B) myxalamid; (C) sorangicin A; (D) aurachin C; (E) stigmatellin A; (F) myxovirescin; (G) myxothiazol A; (H) corallopyronin A; (J) myxovalargin; (K) saframycin Mxl; (L) 3-formylindole; (M) 5-nitroresorcinol; (N) pyrrolnitrin (previously identified in Pseudomonas spp.); (0) althiomycin (previously identified in Streptomyces spp.); (P) ambruticin. group that is more closely related to the bdellovibrios and There is considerable disagreement about the nomencla- the sulfur- and sulfate-reducing bacteria than to other groups ture used in the taxonomy of the myxobacteria. Assigning of gliding bacteria (60, 187, 276). On the basis of the 16S phylogenetic relationships is complicated by the fact that rRNA data it has been suggested that the myxobacteria and type materials are sometimes represented by herbarium bdellovibrios are aerobic descendents of an ancestral sulfur- specimens of fruiting bodies, which provide little informa- metabolizing bacterium (276). tion about the overall phenotype and genotype of the cell. VOL. 54, 1990 SOCIAL AND DEVELOPMENTAL BIOLOGY OF MYXOBACTERIA 475 TABLE 1. Taxonomy of the myxobacteria by transverse binary fission. Fruiting-body morphogenesis is initiated by nutrient deprivation, and tens of thousands of Taxonomy in Taxonomy in The Prokaryotes (201) Bergey's Manual (158) cells direct their movement toward a discrete aggregation focus where they pile atop one another to form a raised Order Myxobacterales Order Myxococcales mound. Within this mound the rod-shaped cells begin to Suborder Cystobacterineae Family I. Myxococcaceae shorten and assume a spherical shape (Fig. 2). The myxo- Family I. Myxococcaceae Genus Myxococcus spores are dormant, refractile, and resistant to a variety of Genus Myxococcus Family II. Archangiaceae Genus Corallococcus Genus Archangium environmental insults, such as heat, desiccation, and freez- Genus Angiococcus Family III. Cystobacteraceae ing, that would kill vegetative cells (248). Myxospores ger- Family II. Archangiaceae Genus I. Cystobacter minate when a nutrient source becomes available; they do Genus Archangium Genus II. Melittangium this by shedding the spore coat and elongating into a Family III. Cystobacteraceae Genus III. Stigmatella rod-shaped cell. Some of the developmental events associ- Genus Cystobacter Family IV. Polyangiaceae ated with aggregation and fruiting-body formation can be Genus Melittangium Genus I. Polyangium bypassed with chemical inducers or mutations that stimulate Genus Stigmatella Genus II. Nannocystis cells to convert directly to myxospores. Secondary alcohols Suborder Sorangineae Genus III. Chondromyces such as induce formation in about 90 Family Sorangiaceae glycerol myxospore Genus Sorangium min, compared with 48 h during fruiting-body morphogen- Genus Polyangium esis (49). A dominant mutation known as csp-SOO has been Genus Haploangium described that results in sporulation upon temperature shift Genus Chondromyces down to 15°C and bypasses early developmental steps (209). Genus Nannocystis The primary difference in the life cycle of S. aurantiaca is the morphological complexity of the fruiting body. Follow- ing aggregation of cells into a raised mound, an elaborate The establishment of a collection of type strains that can be treelike structure is formed. The myxospores are contained subjected to rigorous molecular analysis will undoubtedly in saclike structures, referred to as sporangioles (158) or help resolve the taxonomy of these organisms (64). sporangia (201), that are borne on top of a large stalk. The two most recent versions of myxobacterial taxonomy Sporulation can be induced in the absence of fruiting-body are summarized