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Perspectives Copvright 0 1999 bv the Genetics Society of Anlerica Perspectives Anecdotal, Historical and Critical Commentaries on Genetics Edited by James F. Crow and William F. Dove ROLANDTHAXTER’S Legacy and the Origins of Multicellular Development Dale Kaiser Departments of Biochemistry and of Developmental Biology, Stanford University, Stanford, Calijornia 94305 OLAND THAXTER published a bombshell in R December,1892. He reported that Chondro- myces crocatus, before then considered an imperfect fungus because of its complex fruiting bodv, was ac- tually a bacterium (Figure 1). THAXTERhad discov- ered theunicellular vegetative stage of C. crocatus; the cells he found were relatively short and they divided by binary fission. C. crocatus was, heconcluded, a “communal bacterium.” THAXTERdescribed the lo- comotion, swarming, aggregation and process of fruit- ing body formation of C. crocatus and its relatives, which are collectively called myxobacteria, with an accuracy that has survived 100 years of scrutiny. He recognized the behavioral similarity to the myxomv- cetes and the cellular slime molds, drawing attention in all three to the transition from single cells to an integrated multicellular state. He described the be- havior of myxobacteria in fructification in terms of a “course of development” because it was “a definitely recurring aggregation of individuals capable of con- certed action toward a definiteend” (THAXI‘ER1892). This essay will emphasize some implications of THAX- TER’S demonstrations, often apparently unrecognized. The striking similarities to cellular slime mold de- velopment probably led JOHN TYLERBONNER and KENNETHB. RAPER,50 years after THAXTER’Sdiscov- ery, to take independent forays into myxobacterial development. RAPER,an eminent mycologist, had in FIGURE1 .“Chondromyces crocatus fruiting bodv. Photograph by fact discovered Dictyostelium discoidium, recognizing it HANS KEICHENRACH.GBF, Braunschweig. as a superb subject for the study of morphogenesis, ments,intercellular integration and finally coordi- cellular differentiation and intercellular communica- nated differentiation that are in some ways cornpa- tion. BONNERwas fascinated by morphogenesis and rable to higher forms” (QUINLANand RAPER 1965). sought unifying principles behind the bewildering di- Both BONNERand RAPER soughtthe factors in C. versity (BONNER1952, 1974). Both RAPER and BON- crocatus that coordinated and guided the morphoge- NER seemed to be intrigued by the unusual example netic cell movements, noting thatindividual myxobac- of morphogenetic movements exhibited by the myxo- terial swarm cells retained their physical individuality bacteria as they formed fruiting bodies. RAPERsaw throughout the process of cooperative morphogene- “examples of interdependent cellular behavior that sis, and in that respect differed from the myxomycetes involve purposeful orientation, morphogeneticmove- but resembled the cellular slime molds. Genetics 135: 249-254 (October, 1999) 250 D. Kaiser Their search was extended by HANSKUHLWEIN and are known which form spores, have a high G.C con- his students, particularly REICHENBACH,who prepared tent in their DNA, but do not build fruiting bodies, a series of time-lapse films of the behavior of different even though gliding bacteria have been systematically types of myxobacteria (REICHENBACH, HEUNERTand examined (REICHENBACHet al. 1988). That all the KUCZKA1965a,b,c,d; REICHENBACH,GALLE and HEU- myxobacteria arose fromthe same ancestor within the NERT 1976). Using time-lapse photography to con- 6 subgroup of purplebacteria is supported by an dense the roughly day-long process of fruiting body extensiveset of characters they hold in common: development into a few minutes of running time, as swarmingbehavior, closely related 16s ribosomal BONNERhad donefor D. discoideum, broughtthe RNA sequences (LUDWIGet al. 1983; WOESE1987; morphogenesis into a time scale more suggestive and SHIMKETS1993), high (66-72) mole % G.C content intriguing to the human psyche. The myxobacterial in their DNA (MANDEL and LEADBETTER1965; movies showed the simplest fruiting bodies to be MCCURDYand WOLF1967; BEHRENS,FLOSSDORF and mounds of myxospores covered by slime, while the REICHENBACH1976) and a set of notablechemo- more complex fruiting body structures enclosed systematic markers (REICHENBACHand DWORKIN myxospores within acellular skins of slime that either 1981). None of the other members of the 6 subgroup rested directly on the substratum or were raised on of purple bacteria form fruiting bodies or spores; in slime stalks. REICHENBACH(1 962) concludedthat the additiontothe myxobacteria, this phylogenetic formation of fruiting bodies generally passed through subgroup includes the bdellovibrios and the meso- several stages: vegetative growth of a multicellular philic sulfate-reducing bacteria (WOFSE 1987; STACK- swarm, inductionby starvation to begin development, EBRANDT 1992; WIDDELand BAK 1992). cell accumulation, rearrangement of cells within the In contrast to the monophyletic origin of myxobac- originally undifferentiated mass (includingproduc- teria, cell aggregation of eukaryotes leading to fruit- tion of slime stalks or sporangiole walls) and, finally, ing bodies appears, on cytostructural grounds,to have myxospore formation. REICHENBACH(1 965)also dis- evolved several times among the cellular slime molds covered thatthe ripples noted in myxobacterial (OLIVE1975). BONNER(1982) has argued that there swarms were traveling waves generated by many is likely to have been an independent originfrom myxobacteria during theaggregation phase. single-celled amoebaefor each group because of Work with dispersed (i.e., non-clumping) strains of uniqueaggregation attractants; he distinguishes at My3cococcus xanthus enabled DWORKIN,ROSENBERG least eight different attractants. and their students tostudy this bacterium’s nutrition No matter how many independent events there and metabolism, prerequisites for understanding the were among the cellular slime molds, it is clear that role of starvation in the induction phase of fruiting the changesfrom single to multicellular organism body development (summarized by DWORKIN1984). were taken independently fromthe myxobacteria. To Genetic studies of mutants defective in fruiting body date there has been no report of lateral gene transfer development becamepossible through theisolation of between myxobacteria and the slime molds. The cell transducing myxophages (CAMPOSand ZUSMAN 1975; biology of the slime molds and the myxobacteria are MARTINet al. 1978), the introduction of transposons very different, as THAXTERfirst discovered. The for- from Escherichia coli into M. xanthus (KUNER and mer are eukaryotic amoebae with a flexible cell mem- KAISER 1981) and the infusion of gene cloning tech- brane and a well defined cytoskeleton. We now rec- niques (GILLand SHIMKETS1993). ognize that the latter are rigid-walled, rod-shaped, THAXTER’Sdiscovery called attention to the transi- Gram-negative procaryotic cells that lack the struc- tion from single cells to an integrated multicellular tural anatomic features of a cytoskeleton. Molecular unit. There is general agreement that this step has studies of small ribosomal rRNA sequences as well as been taken many times in the course of organic evo- physiological and morphological studies show that the lution. For example,the sponges probably arose from myxobacteria arose among the purple sulfur eubac- solitary cells separately from all other animals, and teria, while the cellular slime molds arose among the the seed plants, the fungi, and the algae all gained protists. The two groups are thus separated by a wide their multicellular conditionindependently (WHIT- evolutionary gap (Figure 2) (WOESE1987). Features TAKER 1969). Comparing these independent experi- common to these two types of microorganisms prom- ments of nature should provide insight into the gen- ise insight into basic biological attributes of multicel- eral attributes of multicellular life. lular development.The width of the phylogenetic gap Myxobacteria, which belong to the 6 subgroup of decreases the effects of chance evolutionary “tinker- purple bacteria, are a well defined and unique exper- ing” UACOB1982), theaccidents of mutational history. iment in multicellularity. All myxobacteria construct The point is that features shared by different orga- multicellular fruiting bodies (LUDWIGet al. 1983), nisms will be the more robust andfunctionally inform- which is to say that no aerobic gliding bacterial species ative the less the organisms share a common descent. Perspectives 25 1 the aggregate in a species-specificpattern, thendiffer- entiation of individual cells into spores. .Both pass several chemical signals between their BACTERIA - purple bacteria cells. In D. discoideum, the signals include cAMP and - DIF (WILLIAMSand JERMYN 1991). cAMP seems not gram pOsitive bacteria cyanobacteria to be significant in myxobacteria in the way it is in D. deinococci discoideum. Instead, in M. xanthus a mixture of eight Thermotogales amino acids (called A-factor) is a signal early in devel- “ARCHAEA opment, and a 17-kDa surface protein known as C- factor is a signal later during the aggregation and sporulation phases (KIM, KAISER and KUSPA 1992; animals KAISERand KROOS 1993). EUCARYA The cells respond tosignal reception by expressing ~ cellular slime molds * new batteries of genes. ln D. discoideum there are flagellates microsporidia CAMP-dependent andDIF-dependent genes(DE- VREOTES 1989; WILLIAMSand JERMYN 1991). In M.
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