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Significance for Endosymbiosis Theory 7reb. Soc. C'a'. Biol., Vol. 41 (1990) 5-16 KINETOSOME-CENTRIOLAR DNA: SIGNIFICANCE FOR ENDOSYMBIOSIS THEORY LYNN MARGULIS' and MARK MCMENAMIN2 'Department of Botany, University of Massachussetts. Amherst, USA. 'Department of Geology and Geography, Mt. Holyoke College. South Hadley, USA. SUMMARY The "extreme version" of the serial endosymbiosis theory (SET) postulates three types of integration of bacterial symbionts into what became the nucleocytoplasm of nucleated cells. The first, a symbiosis between motile bacteria and less motile archaeobacterial hosts is thought to have resulted in the origin of nucleocytoplasm capable of both internal movement and motility by undulipodia. That is, microtubule-based motility systems of eukaryotic cells (kinetosome- centrioles, undulipodia including cilia, mitotic spindles, etc.) are hypothesized to have evolved from symbiotic associations of spirochetes with Therinoplasma-like archaeobacteria (protonu- cleocytoplasm). The second, a symbiosis between aerobically respiring bacteria and the nucleocy- toplasm, resulted in mitochondria of aerobic eukaryotes. The third association led to photosynthe- tic plastids from undigested cyanobacteria. Whereas the symbiotic origins of plastids and mitochondria are firmly established, the recent discovery by David LUCK and his colleagues of centriole-kinetosome DNA greatly enhances the likelihood that the last postulate concerning motility is valid. We can thus anticipate a rapid, definitive test of the "extreme version" of the SET. Unknown to most Western scientists, the hypothesis of the origin of eukaryotic cell motility from symbiotic bacteria has a Russian antecedent: the concept of symbiogenesis or origin of evolutionary novelty via hereditary symbiosis was well developed by Russian biologists late in the last century and early in this one. Indeed, Boris M. Kozo-POLYANSKI, who wrote only in Russian, suggested that cilia derived from 'flagellated cytodes", by which he meant motile bacteria. New results from molecular biology lend strong support to the SET, a theory which forms the foundation of the concept of symbiogenesis. Both the SET (which explains the genesis of the first eukaryotic cells) and symbiogenesis (a general evolutionary process involving heritable transmis- sion of symbiotically acquired characteristics) require that all eukaryotic organisms be viewed, at the cellular level, as complex microbial communities. 6 L)':NN.t1.-IRG(LI.S.LVI) .t1.IRA t1ct1L;AAMIA Personal recollections ses was named Serial Endosvrrtbiosis Theory (SET) by TAYLOR (1974). F. J. R. Impressed with the frequency of cases of (Max) TAYLOR, Canadian marine biologist nonmendelian heredity in a world of nu- and expert on dinomastigotes, attempted clear inheritance (e. g., photosynthesis mu- -with limited success- to develop the de- tants of plants and algae, "petites" in tails of the contrasting nonsymbiotic ori- yeast, cortical inheritance in Paramecium, gin of eukaryotes. As intellectual exercise etc.), as a genetics student at the Universi- he described the origin of organelles by ties of Wisconsin (1957-60) and Califor- "direct filiation" or autogenesis (TAYLOR, nia, Berkeley (1960-65), I (L.M.), explored 1976). He also distinguished different ver- the early literature for clues for the expla- sions of the views presented here: the xe- nation of cytoplasmic heredity. That there nogenous view of organelle origin, i.e., the were no "naked genes" in eukaryotic cells serial endosymbiosis idea. He collected became clear, and evidence for the presen- data concerning the possible origins of mi- ce of bacterial genetic systems inside them tochondria (from respiring bacteria) and became equally obvious. On the basis of plastids (from cyanobacteria). The concept literature reviews of cytoplasmic heredity of the origin of plastids (but not mitochon- and my consequent predictions of organe- dria) or the origin of both plastids and llar DNA, I wrote the statement of the mitochondria by symbiosis was labeled the origin of nucleated ("mitosing") cells from "mild version" of the SET. TAYLOR called bacterial symbiotic associations in 1965. It my theory the "extreme version" of the was first published by James DANIELL], SET for I insisted that the kinetosomes, co-originator of the lipoprotein bilayer cilia and related microtubule organelles membrane theory, in the Journal oJ'Theo- (Fig. 1) were also of symbiotic origin from retical Biology after approximately 15 re- motile bacteria. jections of the manuscript (MARGULIS, un- As far as I knew at the time, mine was an der the previous name of SAGAN, 1967). entirely original contribution. In the 60's The expanded version of the theory of the cell symbiosis ideas were to some ex- origin of eukaryotic cells organelles (mito- tent still disreputable. Some scientists, like chondria, plastids, centrioles in nucleocy- Hans (who was my professor at the toplasm) was developed into a book origin- University of Wisconsin, Madison), knew ally under contract, and then rejected, well E.B. WILSON'S (1928) masterpiece by Academic Press. Eventually published by The Cell in Development and heredity, and Yale University Press (MARGULIS, 1970), saw to it that articles written describing the theory itself was supported during the the discovery of DNA outside the cell nu- decades of the 70's and 80's by many new cleus in the early 1970's mentioned ideas results derived from molecular biological, of organellar origin by symbiosis. Al- genetic and ultrastructural studies. The re- though some authors did cite historical vised version of the work became the mo- views of cell symbiosis, and noted ideas of nograph Symbiosis in Cell Evolution the origin of mitochondria and plastids as (MARGULIS, 1981). Because of the impor- presented by American (e. g.: WALLIN, tance of the discovery of kinetosome/ 1927) and French authors (e. g.: PORTER, centriole DNA described here, a second 1918), these scientists writing in the 1960's edition of the 1981 book is scheduled for and 1970's were extremely skeptical of he- publication in 1992. reditary endosymbiosis (Chapter 2 in The theory of the derivation of nuclea- MARGULIS, 1981). Indeed TAYLOR and I ted cells from a series of bacterial symbio- were conscious of both prejudice against KINETOSOME-CENTRIOLAR DNA: SIGNIEIC.ANCE FOR ENDOSYMBIOSIS THEORY 7 a KINETOSOME CENTRIOLE Microtubule organelles Figure I. Microtubule-based organelles of eukaryotes from heterokont cells of algae and other protoctists, ciliated epithelium of animals, centrioles of animal and protoctist cells and mitotic spindles. If a shaft (axoneme) is present the basal structure is called a kinetosome, if absent it is a centriole. and ignorance of cell symbiosis theories by sequence data (Fox, 1985), it has become "mainstream" experimental scientists. clear that the acquisition of centriole/ Yet, neither of us had knowledge of our kinetosome/undulipodia preceded that of Eastern European predecessors: the mitochondria and that mitochondria, deri- "symbiogeneticists" such as MERESCH- ved from several types of respiring bacte- KOVSKII and Kozo-POLYANSKI in Russia ria, are most likely polyphyletic within the who, from the late 19th century until the protoctista (Fig. 2). 1950's (Kozo-POLYANSKI died in 1957) The recent spectacular discovery of ki- developed detailed proposals for the origin netosomal-centriolar DNA, reported re- of evolutionary novelty, including cell or- cently from the laboratory of David LUCK ganelles, by establishment of hereditary at Rockefeller University (HALL et symbiosis. al., 1989) clarifies and refines the experi- mental evidence favoring the "extreme SET", and presents a severe challenge for Undulipodia before mitochondria competing hypotheses. Our purpose here is The original statement of the SET, on to place this work, achieved by genetic, the basis of a preconception of monophyly cytological and molecular biological stu- of mitochondria, hypothesized the acquisi- dies in the chlorophyte protist Chlamydo- tion of these organelles prior to that of monas, in its appropriate historical con- centriole/kinetosome/undulipodia. Becau- text. The genetics of the motility system in se of the explosion of information on the Chlamydomonas needs to be better eukaryotic microorganisms (protists and known; we hope to integrate these arcane other protoctists, including so many lack- genetic discoveries with the history of cell ing mitochondria altogether, MARGULIS evolution concepts both in the USSR and cl al., 1990) and from ribosomal RNA the West. S L1"h'N .11.4KG ('l./.5 .4^'/) ,M1f.^IRl^^ A1r .11F,^'.4AfLti' S.E.T. Serial Endosymbiosis Theory PROTOCTISTS ANIMALS FUNGI o""1""/ ,,^,.,",^...n` Figure 2. Serial endosymbiosis theory: diagram of the extreme version of eukaryotic cells origins with the order of organellar acquisition superimposed. Kinetosomal DNA Chlaml^domonas smithii wildtypes. In shit hybridization using cloned segments from Recently, the presence of a large quan- two regions of the uni DNA as probes loca- tity of DNA, 6-8 megabases, in the centrio- lized, with fluorescence microscopy, the le/kinetosomes of Chlamvdomonas rein- uni DNA to the two kinetosomes. In hardtii has been reported (HALL et Chlair^t^dornonas undulipodial motility is a/., 1989). Taking advantage of the fact lost during mitosis; these kinetosomes al- that in Chlarnvdartonas rc^inhar^dtii mu- ter their morphology during the process of tants affecting kinetosomal assembly and cell division and become the centrioles at undulipodia formation are clustered
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