Michael J. Chapman

Chapman, Michael J.

Hemeroteca Cientifica Catalana

Over three sun-dappled days last summer (June 24–26, 1998),an international conference took place in the Lederle GraduateResearch Tower of the University of Massachusetts at Amherst,with funding provided by the Richard Lounsbery Foundation,New York City. Its title marked the centennial of centriole-kinetosome research and commemorated the two founders ofthe field: Mihaly Lenhossek (1863–1937), the Hungarianneurobiologist and relative of conference attendee AndrewSzent-Györgyi, and prominent French histologist Louis FélixHenneguy (1850–1928).The enigmatic centriole, a barrel-shaped structure that sitsat the mitotic poles in nearly all animal cells, presents a widevariety of form and function in different taxa. Well known asthe site of astral microtubule emergence, the same [9(3)+0]microtubule structure, the kinetosome (or basal body), subtendsall undulipodia (eukaryotic flagella and cilia). Thispolyfunctional organelle has even been shown to confer cellpolarity throughout the cell cycle, by determining the number,orientation and polarity of mitotic and interphase microtubules,even in breast cancer cells [8]. Because of the near-ubiquityand identical ultrastructure of centriole-kinetosomes (C-Ks)across eukaryotic taxa, together with the highly conservednature of the C-K proteins centrin and tubulin, evolutionistsbelieve that C-Ks originated in the earliest eukaryotes, perhapsas long as 2000 million years ago. Subsequent divergence hasled to a myriad of C-K-associated elaborations, from the calcium-modulated spasmoneme of Vorticella to theparaxonemal rod (transverse undulipodium) of Peridinium andthe cochlear kinocilium of our inner ear sensory epithelium.As mitotic structures, centrioles are altogether absent fromsome major taxa (e.g. plants, yeasts, rhodophytes [red algae],and cellular slime molds). As basal bodies of undulipodia,kinetosomes occur in the vast majority of eukaryotic phyla.Amoebomastigotes such as Naegleria, however, produce andresorb kinetosomes with every life history transition betweenamoeboid and mastigote phases [7]. Uni mutants inChlamydomonas [5] and “monster” ciliates with invertedorientation of the infraciliature [13], respectively, have shownthat a nuclear mutation can delay kinetosomal reproduction inone system, while in another, kinetosome reproduction ispartially independent of nuclear control. In short, C-K-relatedcontroversy has mushroomed over the past 100 years in concertwith our growing appreciation of the bewildering number ofvariations on the theme.In April 1898, Lenhossek published a paper entitled “ÜberFlimmerzellen” wherein he showed that kinetosomes, the bodiesat the bases of the rat sperm tails, were identical to those ofcilia lining the epididymis. He further proposed that thesekinetosomes were identical to centrioles, and that from thecentrioles originated the spindle. In the same month Henneguy,working on silkworm spermatocytes, independently publishedthe same interpretation in Archives d’Anatomie Microscopique,Tome I. The two founders of C-K theory courteously agreedto equally share the credit. Their contribution, that mitoticcentrioles and ciliary basal kinetosomes are essentially the samestructure, descends to us today as Henneguy-Lenhossek theory.As anticipated by these 19th century scientists, we can nowsay that centriole-kinetosomes give rise to all undulipodialshafts (i.e., axonemes) as well as to microtubular elements ofthe cytoskeleton.The conference began on the evening of Wednesday, June24, with open discussion entitled “The centriole’s new clothes:a century of controversy at the cell center,” moderated byChandler Fulton of Brandeis University. Discussion centeredaround the perplexing questions that still remain after manylifetimes of research: How did centriole-kinetosomes firstevolve? Why are they absent in many taxa? What kinds ofselection may have driven their secondary loss in plants, yeasts233Michael J. ChapmanDepartment of Biology, Clark University,Worcester, MA, USACorrespondence to: Michael J. Chapman. Department of Biology.Clark University. Worcester. MA 01610. USA.Tel.: +1-508-7937107. Fax:+1-508-7938861. E-mail: mchapman@clarku.eduPERSPECTIVESINTERNATL MICROBIOL (1998) 1:233–236© Springer-Verlag Ibérica 1998One hundred years of centrioles: the Henneguy–Lenhossek theory,meeting reportand slime molds? How do they reproduce in the living cell, andto what degree are they controlled by nuclear genes? Do C-K’shave their own genes or any remnant of a genetic system? Thefewer than two dozen attendees, with few exceptions, were allparticipants. They constituted an international quorum ofscientific writers and historians, cell motility researchers andevolutionists from Spain, Canada and the United States. Overthe next two days, this remarkable interdisciplinary milieuimparted a unique atmosphere to the proceedings. It is hard toimagine another organelle which could unite the interest ofsuch diverse scholars from such far-flung home universities.The morning of Thursday, June 25 was devoted to Historyand Philosophy, a session chaired by Michael Dolan of theUniversity of Massachusetts. The talk of Andrew Szent-Györgyi(Brandeis University, Department of Biochemistry) was entitled“My cousin Albert and his uncle”. He traced the history ofbiological and political achievement in the Szent-Györgyi andLenhossek families back over four generations. Andrew’scousin, Nobel prize winner Albert Szent-Györgyi (1893–1986),discoverer of vitamin C and metabolic intermediates of theKrebs cycle, was the nephew of Mihaly Lenhossek. Owingto Albert’s poor showing in grammar school, the uncle (adominant family man in a newly illustrious Austro-Hungarianfamily and prominent neurohistologist) predicted no future forthe nephew in science, though conceded he might make a goodproctologist or cosmetologist! Dr. Szent-Györgyi devoted mostof his lecture to a chronicle of scientific achievement on theLenhossek side of the family, which included key roles inbridging Buda and Pest and in founding the HungarianAcademy of Sciences. The C-K theory of Mihaly Lenhossek,as mentioned above, is only one of many significantachievements of the family.Following Dr. Szent-Györgyi’s vivid historical background,historian of science Jan Sapp (York University, Toronto)presented an overview of “History of Henneguy-Lenhossekcentriole-kinetosome theory” from a broader perspective. Dr.Sapp outlined two main periods of centriole research, the firstfrom 1887–1954, when these structures were ironhematoxylin-staining dots whose visualization was limitedby the light microscope. The second period dates from 1954to the present, as the electron microscope and moleculargenetics enabled new and more fundamental researchproblems to be addressed. For example, in the 1920s it wassuggested that perhaps plant centrioles were present, but toosmall to resolve. Recent in situ hybridization studies [7]coupled with years of electron microscopic observations inwhich glutaraldehyde was fixative have confirmed theirabsence. Electron microscopic studies support and refineHenneguy-Lenhossek theory. Centriole-kinetosome can bestructurally and uniquely defined: 3 sets of 24 nm-sizedtubules surround a lumen, the outside diameter is 250 nm.But central questions about centriole–kinetosome replicationand function have never been answered. Of particular interestwas Dr. Sapp’s elucidation of the definitional controversy ofthe 1970s, during which Jeremy Pickett-Heaps challengedthe conventional zoocentric view that centrioles are essentialto mitosis [14]. Pickett-Heaps introduced the concept of themicrotubule organizing center (MTOC), and proposed thatcentrioles were simply variant MTOCs.Lynn Margulis (conference host, University ofMassachusetts) next spoke on “Symbiogenesis” [15, 16],reviewing the frontiers of symbiogenetic theory of organelleswhose evolutionary origin is in question, such ashydrogenosomes, peroxisomes and C-Ks. Dr. Margulis beganwith quotes from early symbiosis researchers such as “for thereis no middle ground between symbiosis and nonsymbiosis.Either symbiosis with cyanophyceae exists, and then one hasplants, or it does not exist, and then we have animals”(Konstantin Sergeivich Mereschkowsky in [6]). She nextreviewed empirical evidence for nuclear-independent divisionand function of organelles, and posed the question, “arearchaeprotists products (amitochondriate eukaryotes) ofsymbiogenesis?” [9, 10].The afternoon session on June 25, entitled “ProtistGenetics,” was chaired by Dennis Searcy (University ofMassachusetts). The two speakers, Michael Adams (EasternConnecticut State University) and John Hall (The RockefellerUniversity) respectively discussed the molecular andtransmission genetics perspectives on Chlamydomonas and  C-Ks. Dr. Adams described Chlamydomonas as an excellentsystem for study of organellar genetics, since it is easily inducedto enter the haploid (+/–) life cycle stage in which an individualinherits 100% of its organellar and nuclear genetic materialfrom the same parent, i.e. the + and – strains are uniparental.The uni mutant, whose genetic defect on chromosome XIXgives rise to a cell with only one undulipodium, and others suchas vfl (variable flagella) and fla (defect in flagellar assembly),have become workhorses of C-K genetics. A Mendelizing unilinkage group has been identified based on several sets ofcharacters useful in transmission studies.Dr. Hall enlarged on the characterization of the uni and fladefects, tracing structural defects in the undulipodial assemblyunits which prevent the mutant cell from swimming or fromreplicating its one “parent” undulipodium (in 95% of cases,uni mutants’ one undulipodium is cis to the eyespot). Dr. Hallalso discussed his DNA fluorescence studies, conceived as partof the search for autonomous C-K DNA but more recentlyinterpreted as staining elements of the nucleus which adhereto the kinetosome during replication. That the “parent”kinetosome certainly can not always serve as a template issuggested by the complete disappearance of C-Ks afterfertilization, then de novo reappearance in the zygote [4].Chandler Fulton (Brandeis University) next delivered acommentary entitled, “Naegleria makes new centrioles andcounts—but won’t tell us how!” This common freshwateramoebomastigote forms and resorbs C-Ks with every life historyshift between vegetative amoeboid and temporary mastigoteforms. Dr. Fulton has been able to isolate mutants with zero or234 INTERNATL MICROBIOL Vol. 1, 1998 Chapmanwith extra undulipodia, instead of the usual two; heat shock at37°C produced cells with up to 17. During differentiation,kinetosomes form first as a single unit, and then two; usinginhibitors, cells can be arrested at the one kinetosome stage.Thus the cells somehow count from zero to one to two. Dr.Fulton discussed roles of motility proteins centrin and tubulinin C-K development [7]. The afternoon closed with commentaryby Dr. Sapp on the historical perspective.The morning session on June 26, chaired by Luis Vidali(University of Massachusetts), was entitled “Protists:Morphogenesis and the Fossil Record.” Joseph Frankel(University of Iowa) spoke on “Kinetosomes of ciliates: mastersor slaves?” Ciliate kinetosomes are arranged in regular rowscalled kineties, whose collective arrangement forms a latticewith left- or right-handedness (polarity). A fact of great interestto general biological thought is that orientation of the ciliarylattice is independent of nuclear control in ciliates, either micro-or macronuclear. Kineties of offspring cells generally have thesame polarity as those of the parent. When conjugating ciliatesdivide prematurely, i.e. before separation of the conjugants,sometimes the partner cell’s kineties are mistakenly used astemplates (structural guidance, [1]). Such a cell divides andretains the inverted kinety, producing a de facto cortical graftwithout surgery, which demonstrates the DNA-independentnature of ciliate cortical inheritance. Dr. Frankel proposes that an additional global control system,independent of the nuclei, determines the positions of corticallandmarks in offspring cells.Commentary followed by John Hall on the ciliate geneticperspective, David Nanney (University of Illinois, Urbana) on“Ciliate cortical behavior” [12] and Mark McMenamin (Mt.Holyoke College) on “Eukaryote origins and the Proterozoicfossil record” [11].The afternoon session on June 26, chaired by MichaelChapman (Clark University), was entitled “Development asCommunity Ecology.” The first speaker was Ricardo Guerrero(University of Barcelona) who spoke on “Modern MicrobialCommunities.” Dr. Guerrero studies microbial mats andsulfureous lakes such as Lake Cisó, where different species ofbacteria (e.g. Chromatium, Chlorobium spp.) performcoordinated interdependent metabolic tasks in a diurnalphotoperiodic cycle, using sunlight for energy and hydrogensulfide as an electron source. Mat communities, which canconsist of up to seven multicolored layers of different bacterialspecies, are comparable to those of the earliest living organisms,as demonstrated by fossilized microbial mat formations(stromatolites) of the ancient cyanobacteria which gave rise tothe oxygen atmosphere [2].The next speaker, Michael Dolan (University ofMassachusetts) discussed his research in termite hindgutprotists in a talk entitled, “Calonymphid evolution anddifferential centriole-kinetosome numbers per cell.” Termitesymbionts such as Calonympha and Snyderella are interestingsubjects for C-K research, since they have variable numbersof kinetosomes and nuclei per cell. Some kinetosomes are parts of collective structures called “karyomastigonts,”which include kinetosomes, nuclear connectors, parabasalbodies (Golgi) and nuclei; other such structures, the“akaryomastigonts” are the same in all respects (samenumbered configuration of kinetosomes, Golgi, etc.) exceptthat they lack nuclei. In calonymphids, C-K reproductionoccurs and a paradesmose (thin spindle) links offspring nucleias all the nuclei—up to hundreds—in a single cell divide.Michael Dolan has treated calonymphids with various DNA-specific stains. He has also demonstrated accumulation ofDAPI in the Golgi apparatus. No conclusive akaryomastigontsignal attributable to C-K-specific DNA has been found, infact Dolan suspects the genetic determinants of the C-Ks arein the nucleus even in these amitochondriate cells. However,the fact that organellar gene sequences of prokaryotes arepresent in the nucleus does not preclude a symbiotic modelfor C-K origins.The next speaker, Radhey Gupta (McMaster University),presented molecular sequence data interpreted as evidenceagainst the three-domain model of life (Archaea, Bacteria andEukarya, [17]). Through sequence comparisons of several highlyconserved proteins (e.g., Hsp70, glutamine synthase I,asparaginyl tRNA synthase, diaminopimelate epimerase), Dr. Gupta has shown a close evolutionary relationship betweenarchaebacteria and Gram-positive bacteria, i.e., those bacteriabounded by a single membrane. In contrast, all true Gram-negative bacteria (those bounded by two different membranes,with an enclosed periplasmic space) form a distinct clade. Hisnew proposal recognizes only two domains of life, Prokaryaand Eukarya, with a subdivision of Prokarya into Monoderm(single-membrane) and Diderm subdomains [3]. The final speaker of the conference was Dorion Sagan ofSciencewriters, who used a pack of playing cards to illustratethe relationship between parts and the whole.Just as symbiogenesis theory has shown the geneticallyconglomerate nature of eukaryotes, our concept of theindividual must now be expanded to include technology. The Internet, satellite links and other global communicationdevices unite our planet in a living phenomenon that transcendslife science. As Dorion Sagan terms the phenomenon,“superordination” has made one large de facto organism of us all.In summary, “One hundred years of centrioles” marked thecentennial of research into a puzzling organelle, whose functionand evolutionary origins are still fertile ground for new studiesin cytology and molecular genetics. References1. Frankel J (1973) Dimensions of cortical control in Euplotes: the role ofpreexisting structure, the clonal life cycle and the genotype. J Exp Zool183:71–94235One hundred years of centrioles INTERNATL MICROBIOL Vol. 1, 19982. Guerrero R, Urmeneta J, Rampone G (1993) Distribution of microbialmats at the Ebro Delta, Spain. BioSystems 31:135–1443. Gupta R (1998) Life’s third domain (Archaea): An established fact or anendangered paradigm? A new proposal for classification of organismsbased on protein sequences and cell structure. Theor Pop Biol (In press).4. Hall JL, Ramanis Z, Luck DJL (1989) Basal body/centriolar DNA:Molecular genetic studies in Chlamydomonas. Cell 59:121–1325. Hall JL, Luck DJL (1995) Basal body-associated DNA In situ studies inChlamydomonas reinhardtii. Proc Natl Acad Sci USA 92:5129–51336. Khakhina LN (1992) Concepts of Symbiogenesis: A Historical andCritical Study of the Research of Russian Botanists. New Haven: YaleUniversity Press, p 447. Levy YY, Lai EY, Remillard SP, Heintzelman MB, Fulton C (1996)Centrin is a conserved protein that forms diverse associations withcentrioles and MTOCs in Naegleria and other organisms. Cell MotilCytoskeleton 33:298–3238. Lingle WL, Lutz WH, Ingle JN, Maihle NJ, Salisbury JL (1998) Centrosomehypertrophy in human breast tumors: Implications for genomic stabilityand cell polarity. Proc Natl Acad Sci USA 95:2950–29559. Margulis L (1993) Symbiosis in Cell Evolution. New York: W.H. Freeman10. Margulis L (1996) Archeal–eubacterial mergers in the origin of Eukarya:Phylogenetic classification of life. Proc Natl Acad Sci USA 93:1071–107611. McMenamin M, McMenamin D (1994) Hypersea: Life on Land. NewYork: Columbia University Press, pp 46–5012. Nanney DL (1966) Corticotype transmission in Tetrahymena. Genetics54:955–96813. Ng SF, Frankel J (1977) 180° rotation of ciliary rows and itsmorphogenetic implications in Tetrahymena pyriformis. Proc Natl AcadSci USA 74:1115–111914. Pickett-Heaps J (1974) The evolution of mitosis and the eukaryoticcondition. BioSystems 6:37–4815. Sapp J (1987) Beyond the Gene: History of Cytoplasmic Inheritance.New York: Oxford University Press16. Sapp J (1994) Evolution by Association: A History of Symbiosis. NewYork: Oxford University Press, pp 149–18417. Woese C, Kandler O, Wheelis M (1990) Towards a natural system oforganisms: Proposal for the Domains Archea, Bacteria and Eukarya. ProcNatl Acad Sci USA 87:4576–4579236 INTERNATL MICROBIOL Vol. 1, 1998 Chapman

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