Volume 87, No. 4 THE QUARTERLY REVIEW OF BIOLOGY December 2012

THE KARYOMASTIGONT AS AN EVOLUTIONARY SEME

Michael Chapman Josephine Bay Paul Center, Marine Biological Laboratory Woods Hole, Massachusetts 02543 USA Department of Geosciences, University of Massachusetts Amherst, Massachusetts 01003 USA e-mail: [email protected]

Mark C. Alliegro Josephine Bay Paul Center, Marine Biological Laboratory Woods Hole, Massachusetts 01003 USA e-mail: [email protected]

IN MEMORY OF LYNN MARGULIS (1938–2011) Lynn Margulis was an American evolutionary biologist, one of the founders and perhaps the foremost exponent of modern Serial Endosymbiotic Theory (SET). SET asserts that eukaryotic cells evolved not only by classical Darwinian selection on individual genes, but also by symbiotic mergers involving at least three prokaryotic organisms: a host cell (now largely accepted as being of archaean ancestry) and its two acquired eubacterial symbionts, an ␣-proteobacterium and a cyanobacterium, ancestors respectively of mitochondria and chloroplasts. The host cell acquired not only metabolic faculties but the entire genomes of the symbionts, which thus became heritable organelles. In contrast to Darwinian gradualism, symbiogenesis is a saltatory mode of evolution whereby new species can arise in a single generation. Against considerable resistance, Lynn tirelessly promoted her ideas until, by the 1980s, they were accepted as orthodoxy. The impact of her contribu- tion to the life sciences cannot be overstated. Not many of us can claim to have changed the way our colleagues view even our own narrow fields. Yet, Lynn’s insight and perse- verance caused the whole world to think differently about living things and how they evolve. Lynn was a forceful advocate of the karyomastigont’s importance in eukaryotic evolu- tion. She knew that the authors saw a great deal of merit in her model, but also that this article represented something of a “reset” to (hopefully) a point just before all the disagreement begins. In her last private meeting with Chapman, the day before she fell ill, she eagerly asked where things stood with this manuscript. Had it already been submitted? Was it ready to go out the door? She was her ever-enthusiastic self, eager to pursue the debate, certain that she had the truth in her sights, if not all the details.

The Quarterly Review of Biology, December 2012, Vol. 87, No. 4 Copyright © 2012 by The University of Chicago Press. All rights reserved. 0033-5770/2012/8704-0002$15.00

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The world knows the Lynn Margulis who had boundless energy, a remarkable store of knowledge, and no fear of controversy. However, fewer knew the complete Lynn. She was a kind and generous person who took people into her home and graciously offered financial assistance, encouragement, and confidence. She relished cooking for friends and family and even little-known guests. Lynn was someone special who made others feel special. Out in the world she was a giant. Among friends and family, she was a kind woman with a warm maternal streak. Lynn Margulis has made a place for herself in history, and in the hearts of her friends and colleagues. She will be sorely missed.

keywords karyomastigont, eukaryogenesis, flagellum, basal body, centrosome, nucleus

abstract The problem of eukaryogenesis—the evolutionary mechanism whereby eukaryotic cells evolved from prokaryotes—remains one of the great unsolved mysteries of cell biology, possibly due to the reductionist tendency of most scientists to work only within their subdisciplines. Communication between biologists who conduct research on the nucleus and those working on the cytoskeleton or endomembrane system are sometimes wanting, and yet, all of these quintessentially eukaryotic elements of the cell are interdependent, and are physically associated in many protists as the karyomastigont organellar system: nucleus, one or more basal bodies and flagella, nuclear connector, and Golgi apparatus. Here we suggest a more holistic view of the karyomastigont as not simply an organellar system, but an evolutionary seme, the archaic state of the eukaryotic cell. We also present a scheme whereby the karyomastigont may have dissociated, giving rise in more derived cells to one or more free nuclei and discrete flagellar apparati (akaryomastigonts).

Introduction may be called an undulipodium by the latter. RODUCTIVE debate on the nature of Indeed, the single term flagellum represents Pthe last eukaryotic common ancestor two vastly different organelles in bacteria and (LECA) has been hampered by artificial bor- eukaryotic cells, their only common charac- ders between biological disciplines. Cell biolo- teristics being that they are elongate and mo- gists specializing in the cytoskeleton, nucleus, tile. Integral to the debate on eukaryogenesis is membranes, etc. have been unable to pro- the origin of the microtubule-based cytoskele- duce a unified theory of eukaryogenesis to ton. Prokaryotes possess proteins with struc- date, and the subject is even more clouded tures and properties similar to tubulin, but we among the broader disciplines of cell biol- understand comparatively little of their func- ogy, protistology, and bacteriology. There tion and origin. Moreover, there are but few has always been some amount of crosstalk reports of microtubule-like structures in bacte- between disciplines, of course, and the bor- rial cells (Bermudes et al. 1994). So how did ders separating disciplines may fade with the transition occur between the bacterial state time (see Kutschera 2009, 2011). Still, sepa- and eukaryotes that, so far as we know, univer- rate histories and perspectives on eukaryogen- sally possess microtubules composed of tubulin esis can conflict with one another in detail, proteins? Our purpose here is not to cham- thus obscuring points of agreement and pion a particular theory, nor is this a treatise on hindering advancement in the character- the semantics of different biological disci- ization of LECA. plines. Rather, our aim is to acquaint—or reac- In some cases, the problem may arise from quaint—investigators with two important terms simple differences in terminology. For exam- that have been in use for some time, albeit not ple, the basal body of cell biology literature broadly across disciplines: seme and karyomas- has long been known as the kinetosome to tigont. A new conceptual perspective, driven by protozoologists. A flagellum to the former recent observations and relevant to the debate

This content downloaded on Tue, 1 Jan 2013 20:03:14 PM All use subject to JSTOR Terms and Conditions December 2012THE KARYOMASTIGONT AS AN EVOLUTIONARY SEME 317 on eukaryogenesis, is growing up around these since semes can merge into a functional con- terms. What is a mastigont (much less a karyo- tinuum over evolutionary time, as may be the mastigont)? What is a seme? In short, they are case for the endomembrane system. Thus, basic functional units, the former structural, the components of a seme may have differ- the latter evolutionary. We aim to show how ent origins, but become blended as a func- the perspective of the karyomastigont seme sug- tional evolutionary unit. Or, components gests a highly pragmatic way of thinking about that originated together (by symbiogenesis, the structural and evolutionary relationships of for example) may become disengaged ac- cell motility organelles. cording to new needs and constraints within which the seme operates. It is just such a the seme debate that pervades our understanding of “Seme” is a term introduced by Hanson the microtubule-based motility system. In (1976) to identify a coherent phylogenetic animal cells, this seme consists of microtu- unit. He defines a seme as “an information- bules, the centrosome (microtubule organiz- containing entity in an interbreeding pop- ing center, MTOC), centrioles, and several ulation of organisms . . . [that] will be used microtubule assemblages that vary depend- in reference to a structural or functional part ing on cell type and physiological activity. of an organism” (Hanson 1977:89). A seme is a These include cilia and flagella, the basal functional unit upon which natural selection bodies from which they arise (themselves de- may act, or which may confer some evoluti- rived from centrioles), and the mitotic spin- onary advantage. Examples of semes include dle. There is evidence to suggest that certain body parts (e.g., pectoral fins), organs or tis- intranuclear structures may be considered sues (such as liver), cellular organelles or or- part of this system as well (Allen 1951, 1953; ganelle systems, or macromolecular complexes Tanaka 1973; Laane and Haugli 1974; Al- (such as ribosomes). Although defining the liegro et al. 2010, 2012). phylogenetic history of individual molecules Shared composition, concerted function, may generate useful data, it can also distract and physical linkage join these microtubule- us from functional units (semes), especially based motility components into a system. Yet units that are linked only discretely. This also they are not all directly connected in the cell holds true at the organelle level. Addition- nor even present at the same time. The mi- ally, the more we have come to understand totic spindle is present for only a short pe- the roles of symbiogenesis and lateral gene riod during the cell cycle, and only rarely transfer as evolutionary forces shaping cells concurrent with a cilium or flagellum. Cilia and their genomes, the clearer the necessity and flagella may themselves come and go dur- to define units, as best we can, with a com- ing the life cycle of a cell. They may be at some mon functional purpose and evolutionary distance in the cytoplasm from the centriole, origin. Thus, Hanson’s seme. but their basal body, in which all cilia and fla- Yet, “seme” is a term too seldom used. gella are rooted, is structurally almost identical Although the cell biology literature is more to the centriole. Once again, shared composi- and more replete with discussion of the evo- tion, concerted function, and physical linkage lutionary history and pressures that shaped (although sometimes transient), join these the cell and its components, the term “seme” structures into a seme. is still not well known. The seme concept is, nonetheless, an intuitive part of all evolution- mastigont and karyomastigont ary discourse. When we discuss the origin We may call this seme the microtubule- and evolutionary history of mitochondria, based motility seme, or coin another term their ultrastructure, biochemistry, or genet- for it. Or we may choose to use the name ics, we are discussing a seme. Likewise, when that it was given over 80 years ago and is we discuss the origin and evolution of endo- still in active use in some biological disci- membranes, we are discussing another seme. plines, such as protistology: the mastigont. Recognizing where one seme ends and In parabasalids and other protists, as well as another begins can be a difficult problem, mammalian sperm cells, the nucleus is at-

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Figure 1. Karyomastigont Structure A) Diagram of the flagellar/cytoskeletal system forming one karyomastigont in a mastigameboid type: Mastigina. From a microtubule organizaing centre (mC) associated with the basal body (bB) of the unique flagellum (F) arises a cone of microtubules that caps and attaches to the nucleus (N). A surface root (mR)is also differentiated. B) Electron micrograph of the Mastigamoeba karyomastogont. The cone of microtubules (mt) arises from a center (MC) at the base of a short basal body (bB) and is associated with the nuclear envelope. The large endosomal structure is remarkable in the pear-shape nucleus (N). The flagellar axoneme (F) appears normal (b), but a helix-like structure is apparent in the basal region (arrow). (Figures and captions from Brugerolle 1991, Figures 1 and 5a, respectively; reproduced with permission from Springer-Verlag Wien). tached to the basal body (or bodies) via a can perform double duty as part of the mitotic nuclear connector made of centrin protein. MTOC, enabling simultaneous flagellar repli- With the nucleus added, this karyomastigont cation and mitosis. In basal eukaryotes, which (Janicki 1915) often also includes Golgi ele- have not yet evolved a diverse suite of targeting ments that function in sorting and targeting and recognition proteins, the karyomastigont proteins to the flagellar compartment. Re- would have been not merely a valuable seme, gardless of terminology, the karyomastigont but an essential one. The nucleus is dependent is a ubiquitous signature system and seme of on the microtubule-based motility system that eukaryotic cells well known in some fields forms the mitotic spindle. Likewise, the micro- (Figure 1). tubule-based motility system depends on ex- The karyomastigont insures physical associa- pression of nuclear genes that encode its more tion of the nucleus with the basal bodies, which than 360 known proteins.

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The mastigont and its components—the in establishing the taxonomy of the termite- basal body plus associated structures such symbiotic calonymphid protists (for example, as the cilium or flagellum (undulipodium) Calonympha, Coronympha, Metacoronympha, and and, in some cases, the parabasal body (Go- Stephanonympha; Figure 2) noted that karyo- lgi)—is well-studied under this name in many mastigonts increase in number with increasing protist groups, including ciliates (Tetrahymena, cell size (Kirby and Margulis 1994). Under se- Paramecium), dinoflagellates (Gonyaulax, Gym- lection for larger cell size and/or faster swim- nodinium), and trichomonads (Trichomonas). ming, cells such as Calonympha (Figure 2A) By definition, the mastigont is present in all evolved multiple karyomastigonts per cell (e.g., ciliated or flagellated eukaryotes. However, vi- Coronympha, Figure 2B). Large numbers sualization of the mastigont as a unit can be of intact karyomastigonts, however, create dif- complicated by changing morphologies dur- ficulties with mitosis, so in giant cells such as ing the life cycle of a single organism so that Stephanonympha (Figure 2D), which may be sometimes its full presence is obvious, and at hundreds of microns in length, the hundreds other times parts may be translocated or tem- of nuclei become detached from the basal bod- porarily disassembled or incorporated into ies creating akaryomastigonts. An intermediate other modules. An example of such dynamics stage in this evolutionary process is repre- in a well-known model organism is the unicel- sented by Metacoronympha (Figure 2C) some of lular alga, Chlamydomonas (Johnson and Porter whose nuclei are detached and others at- 1968). For most of the Chlamydomonas life cycle tached—components of intact karyomas- two roughly equivalent mastigonts are present tigonts (Kirby and Margulis 1994). (thus the designation as isokont). During cell Organelle multiplicity is of basic impor- division, however, the flagella are disassem- tance in evolution. This holds true for the bled, and the basal bodies (kinetosomes) rep- karyomastigont. Kirby introduced a new tax- licate, then move to the anterior end of the onomic perspective based upon mastigont dividing cell to lie next to the cleavage furrow. multiplicity in his classification of the calonym- As originally theorized by Henneguy (1898) phids. Prior to his treatise, calonymphid taxa and Lenhosse´k (1898), in many cells, mitotic were organized into classes according to num- centrioles replicate and move to the plasma ber of mastigonts. Kirby proposed that rela- membrane to function as basal bodies (i.e., tionships defining descent within a group centrioles and basal bodies are not only struc- should be based on mastigont composition turally equivalent, but in some cells are virtually and morphology rather than mastigont num- the same organelle). ber. That is, protists bearing different numbers Chlamydomonas mastigonts, because they of mastigonts, but with similar karyomas- are linked to the nucleus, also serve to illus- tigont morphology, were related by descent. trate the next level of organization in this Kirby utilized the entire unit, the seme, to system—the karyomastigont. The complex- more accurately describe evolutionary taxo- ity of the karyomastigont system is multiplied nomic relationships in the Calonymphidae by several permutations that may exist, in and other classes of protists. Use of the seme that the ratio of mastigonts to nuclei can vary for taxonomic analysis incorporated more in- depending upon both the number of mas- formation than simple mastigont counts, tigonts and the number of nuclei in a given which could vary according to nutritional states cell. In Chlamydomonas, there are two mas- and other factors. tigonts associated with a single nucleus. In mammalian sperm, the ratio is 1:1. Other selective advantages of the cells such as Metacoronympha may have mul- karyomastigont tiple mastigonts, some of which are associ- Attempts to model the principal events of ated with a nucleus, and some of which are eukaryogenesis have historically suffered from not (akaryomastigonts; see Figure 2C). the reductionist tendency in science to focus As the karyomastigont may change during on individual parts of the system, rather than the life cycle of a single organism, so it varies the whole. Focusing on two components of, through evolutionary descent. Harold Kirby, say, nucleolar physiology separately, can yield

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Figure 2. Stages of Mastigont Multiplicity Leading to Evolution of Detached Nucleus A) Generic trichomonad (this order of anaerobic protists includes the genera Trichomonas, Mixotricha, and Histomonas, among others) with one quadriflagellate karyomastigont; B) Coronympha octonaria with ring of eight karyomastigonts, each with four flagella; C) Calonympha with karyomastigonts and akaryomastigonts; and D) Snyderella with akaryomastigonts and free nuclei. two very different models of evolutionary ori- considered in toto. In this respect, all functional gin (Je´kely 2008; Ohyanagi et al. 2008). In- attributes of the karyomastigont—genetic reor- deed, two nearly opposite theories of nucleolar ganization from genophore to chromosomes, origins have been drawn from the analysis of the origin of introns, microtubule-based cell the very same protein set (Moreira et al. 2004; motility, and membranous fusion both be- Staub et al. 2004). Although gene- or protein- tween cells (as in fertilization) and within cells based molecular clocks are often powerful (as in vesicular transport)—must be consid- tools for phylogenetic analysis, an overreliance ered together in order to reach a coherent on such criteria at the expense of classical evo- evolutionary hypothesis. In terms of genetic lutionary focus on shared characters can be structure, the most striking eukaryotic innova- dangerous. Molecular clocks derived from fo- tion over prokaryotes is reorganization of the raminiferan cytochrome c, for example, place genome into multiple discrete, yet interdepen- the origin of that well-studied group 300–500 dent, units (chromosomes) as opposed to a million years prior to the earliest known fossil unitary genophore, sometimes accompanied evidence of life on Earth (S. Bowser, personal by plasmids. Proper distribution of a com- communication). pound, multiple chromosome-based genome In terms of function then, a seme must be is highly dependent upon spindle-based mito-

This content downloaded on Tue, 1 Jan 2013 20:03:14 PM All use subject to JSTOR Terms and Conditions December 2012THE KARYOMASTIGONT AS AN EVOLUTIONARY SEME 321 sis. Flagellar motility, cell fusion, and vesicular leading to mitosis, meiosis, and sexual fusion. transport are equally dependent on microtu- The foregoing explanation of the selective ad- bules and motor proteins. vantage of the karyomastigont does not consti- The MTOC, in whatever form it takes in a tute an argument for the spirochete model of given cell, therefore, is the central component eukaryogenesis (Margulis 1993), nor for a sym- or linchpin of the karyomastigont, as essent- biotic origin of the seme, although the selective ial to the eukaryotic condition as the nucleus advantages would be the same. Indeed, almost itself. As shown by Henneguy-Lenhosse´k the- diametrically opposed theories of eukaryogen- ory (Chapman 1998), cells produce a spin- esis may still begin with the critical karyomas- dle only after retraction of their axonemes. tigont (e.g., Bornens and Asimzadeh 2007; The physical connection between nucleus Margulis et al. 2007). and kinetosomes (basal bodies) is most ap- parent in anaerobic protists (parabasalids, the karyomastigont perspective oxymonads, pyrsonymphids), but also per- sists in derived protists (green algae, chryso- Reluctance to use the term karyomastigont phytes). Plants and animals have retained the may be due in part to its reputation in some karyomastigont in their flagellated sperm cells. circles as outdated. Perhaps a more descriptive Even the fungi, which like amoebae and fora- name can be devised. Regardless of nomencla- miniferans have discarded their flagella in fa- ture, there are advantages to considering the vor of cell (hyphal) elongation over the course karyomastigont as a unitary organelle rather of evolution, retain a physical connection be- than as separate entities associated by physi- tween nucleus and MTOC in the form of their cal proximity and broad functional overlap. nuclear membrane-associated spindle pole Also, the tangible connections between these bodies. seemingly distinct organelles may not yet Taken together, the suite of shared charac- be discovered, or at least obvious, but may ters involving the karyomastigont suggests that nevertheless exist. The karyomastigont per- the physical connection between nucleus and spective seamlessly incorporates a number of MTOC was a crucial selective innovation that observations, including some very recent and conferred an advantage over symbiotic associ- surprising findings. The data may only be ations such as the spirochete-Thermoplasma bac- correlative at present, but when viewed from terial symbiosis, Thiodendron (Surkov et al. the karyomastigont perspective, they are no 2001). As shown by stratigraphic correlation longer surprising. It was quite unexpected, between acritarchs (early eukaryotic fossils) for example, to find that the Golgi can func- and stromatolites (cyanobacterial fossils), the tion as a MTOC (Efimov et al. 2007). Yet it is predominant environmental stress on early eu- not so surprising when, as pointed out earlier karyotes was increasing oxygen in the atmo- in this discussion, the Golgi (parabasal body) sphere due to cyanobacterial photosynthesis has long been considered a karyomastigont (Margulis 1993). A permanent physical con- component. From this perspective, the obser- nection between the nucleus and motility or- ganelle, incorporating the motility system vation that a component of a unitary micro- within the cell membrane, would have con- tubule-based motility organelle could nucleate ferred the advantage of better motility through microtubules is no revelation. The karyomas- high-oxygen or low-sulfur environmental zones tigont perspective also addresses reports of and consequent improved chances of reaching MTOC components in the nucleus of some greener pastures. The simple Thiodendron asso- cells (Tanaka 1973; Laane and Haugli 1974; ciation, by contrast, with its oxygen-sensitive Alliegro et al. 2010, 2012). Viewed in light of spirochete partner and sulfide-requiring ar- the unitary karyomastigont, the relationship chaean partner, would tend to break down in between the microtubule-based motility system stress environments. Moreover, through incor- and the nucleus is not simply one devised to poration of the motility system within the cell segregate genetic material, but a much more membrane, the karyomastigont system con- integrated, reciprocal relationship with shared ferred intra- as well as extracellular motility, and exchanged elements.

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Conclusion parts perhaps necessitated physical linkage in The physical linkage between parts of the the early, simplified versions of the karyo- karyomastigont in basal organisms consid- matigont; i.e., the nucleus maintained a physi- ered together with the interdependence and cal association with the basal body because that exchangeability of these components in so organelle became a spindle pole during mito- many derived taxa lacking an intact karyo- sis; and similarly, maintained an axostyle of mastigont is thought-provoking. So, too, is nonephemeral microtubules running caudally the observation that karyomatigont compo- down the length of the cell. In its ancestral nents are all individually considered eukary- state, these two bundles of microtubules—the otic signature structures: the Golgi (Dacks flagellar and axostylar—conferred intrinsic et al. 2003; Mironov 2007), flagellum, and motility during interphase on the flagellum centriole/basal body/centrosome (Satir et and cell body, respectively, then formed the al. 2007; Marshall 2009) are found across two lobes of the spindle during mitosis. The basal body replicated to generate spindle all taxonomic groups universally, or nearly poles during mitosis, then resumed its role in so. In cases where they are absent, it is nucleation of the new flagellum in inter- considered due to a secondary loss (Dacks phase in the offspring cell. The ancestral et al. 2003; Mironov et al. 2007; Marshall Golgi, probably a modified series of cisternae 2009). The nucleus, of course, is presently derived from the endoplasmic reticulum considered definitional for eukaryotes by (Staehelin and Kang 2008), was closely ap- itself. We can therefore state with some con- posed to the nucleus and nuclear connector fidence that, if not in its composite form, the because of its function. Highly complex in building blocks of the karyomastigont are as structure and subject to intense physical close to the irreducible minimum for eukary- stress in its function, the flagellum needs otic life as has yet been deliberated. concerted effort by the cell for its assembly Constructing a testable hypothesis of origin and maintenance. This is the province of the for the karyomastigont is difficult, given the IFT (intraflagellar transport) proteins, which lack of data prerequisite for a reasonable shuttle components of the axoneme and fla- model. Perhaps the only applicable test to fal- gellar membrane from the base to the tip sify any immediate hypothesis would be docu- and back again. Because one would expect mentation of a derived organism with an intact ancestral IFT proteins to have been far fewer karyomastigont, and of its ancestor or ances- in number and less specialized than the 18 tors lacking karyomastigonts. Still, we can spec- that are known today, close physical proxim- ulate. To do so, we begin by allowing that the ity might have been necessary between the nucleus was derived symbiogenetically, as most ancestral Golgi and the basal body. The same modern theories of eukaryogenesis posit. If the is true of the centrin nuclear connector, unitary karyomastigont is truly the archaic whose component proteins had not yet di- form, it can only follow that the entire com- versified into the centrin family of proteins plex—nucleus, connector, MTOC (centriole/ we know today. Perhaps in order to regulate basal body/centrosome), and Golgi—was de- the cell cycle, this ancestral centrin needed rived symbiogenetically. The moment of its physical contact with both the nucleus and incorporation into a host cell represents cre- one of the spindle poles. ation of the eukaryotic lineage and the ele- Meanwhile, it is tempting to choose individ- ments of the karyomastigont are thenceforth ual molecules, or small groups of molecules conserved across virtually all eukaryotic taxa. that one or another investigator considers We will not go so far as to speculate on whether “core” to any given structure, and construct an the karyomastigont was, prior to this point, de- evolutionary narrative for the seme or entire rived from a single organism or was itself a organism based on limited molecular phylog- composite. However, from this point forward, eny. This is perhaps a more likely trap when we can borrow on Kirby’s model for the tran- the chimeric eukaryotic cell, with its admixture sition from karyomastigont to the akaryomas- of archaean and eubacterial proteins and its tigont of derived taxa. The interdependence of composite, yet unitary karyomastigont, is over-

This content downloaded on Tue, 1 Jan 2013 20:03:14 PM All use subject to JSTOR Terms and Conditions December 2012THE KARYOMASTIGONT AS AN EVOLUTIONARY SEME 323 looked and analyses are performed on a se- tures—nucleus, basal body, flagellum, and lected set from the basal body, flagellum, Golgi—have shared components, physical centrosome, or nucleus, each alone. Decisions linkage, and concerted function in basal pro- on which members comprise the set of mole- tists, it would be improvident to overlook the cules chosen for analysis are always based on strong possibility of a shared evolutionary operational (functional/physiological) consid- history. Viewed as a seme, the karyomas- erations, yet operational genes can be and are tigont offers fresh evolutionary insights on all exchanged between organelles and organisms. components of the system, and may ulti- The targets for analysis may therefore be ratio- mately shed light on the origin of eukaryotic nally chosen, but are still arbitrary. Rather, we cells. propose that the proteomes and transcrip- tomes of karyomastigont components should acknowledgments be assembled in their entirety and analyzed Mark C. Alliegro is supported by grants from the using a shotgun approach. This will let the core National Institutes of Health (NIGMS) and National components and their origins reveal them- Science Foundation. The authors thank Mary Anne selves to us, without bias. Alliegro for reading and commenting on the manu- In conclusion, given that all of these struc- script.

REFERENCES

Allen R. D. 1951. The role of the nucleolus in spindle Maia A. R. R., McLeod I. X., Yates J. R., III, Maiato formation. Biological Bulletin 101:214. H., Khodjakov A., Akhmanova A., Kaverina I. Allen R. D. 1953. Fertilization and artificial activation 2007. Asymmetric CLASP-dependent nucleation in the egg of the surf-clam, Spisula solidissima. Bi- of noncentrosomal microtubules at the trans-Golgi ological Bulletin 105:213–239. network. Developmental Cell 12:917–930. Alliegro M. A., Henry J. J., Alliegro M. C. 2010. Re- Hanson E. D. 1976. Major evolutionary trends in an- discovery of the nucleolinus, a dynamic RNA-rich imal protists. Journal of Protozoology 23:4–12. organelle associated with the nucleolus, spindle, Hanson E. D. 1977. The Origin and Early Evolution of Ani- and centrosomes. Proceedings of the National Acad- mals. Middletown (Connecticut): Wesleyan University emy of Sciences of the United States of America 107: Press. 13718–13723. Henneguy L.-F. 1898. Sur le rapports des cils vibratiles avec Alliegro M. C., Hartson S., Alliegro M. A. 2012. Com- les centrosomes. Archives d’Anatomie Microscopique et de position and dynamics of the nucleolinus, a link Morphologie Expe´rimentale 1:481–486. between the nucleolus and cell division apparatus Janicki C. 1915. Untersuchungen an parasitischen in surf clam (Spisula) oocytes. Journal of Biological Flagellaten. II. Teil: Die Gattungen Devescovina, Chemistry 287:6702–6713. Parajoenia, Stephanonympha, Calonympha.–U¨ ber Bermudes D., Hinkle G., Margulis L. 1994. Do pro- den Parabasalapparat. – U¨ ber Kernkonstitution und karyotes contain microtubules? Microbiology and Kernteilung. Zeitschreft fu¨r Wissenschaftliche Zoologie 112: Molecular Biology Reviews 58:387–400. 573–691. Bornens M., Azimzadeh J. 2007. Origin and evolution Je´kely G. 2008. Origin of the nucleus and Ran- of the centrosome. Advances in Experimental Medi- dependent transport to safeguard ribosome bio- cine and Biology 607:119–129. genesis in a chimeric cell. Biology Direct 3:31. Brugerolle G. 1991. Flagellar and cytoskeletal systems Johnson U. G., Porter K. R. 1968. Fine structure of in amitochondrial flagellates: Archamoeba, Meta- cell division in Chlamydomonas reinhardi: basal bod- monada and Parabasala. Protoplasma 164:70–90. ies and microtubules. Journal of Cell Biology 38:403– Chapman M. J. 1998. One hundred years of centri- 425. oles: the Henneguy-Lenhosse´k Theory, meeting Kirby H., Margulis L. 1994. Harold Kirby’s symbionts report. International Microbiology 1:233–236. of termites: karyomastigont reproduction and Dacks J. B., Davis L. A. M., Sjögren Å. M., Andersson calonymphid taxonomy. Symbiosis 16:7–63. J. O., Roger A. J., Doolittle W. F. 2003. Evidence Kutschera U. 2009. Symbiogenesis, natural selection, for Golgi bodies in proposed “Golgi-lacking” lin- and the dynamic Earth. Theory in Biosciences 128: eages. Proceedings of the Royal Society, Series B: Biolog- 191–203. ical Sciences 270:S168–S171. Kutschera U. 2011. From the scala naturae to the Efimov A., Kharitonov A., Efimova N., Loncarek J., symbiogenetic and dynamic tree of life. Biology Miller P. M., Andreyeva N., Gleeson P., Galjart N., Direct 6:33.

This content downloaded on Tue, 1 Jan 2013 20:03:14 PM All use subject to JSTOR Terms and Conditions 324 THE QUARTERLY REVIEW OF BIOLOGY Volume 87

Laane M. M., Haugli F. B. 1974. Division centers in Satir P., Guerra C., Bell A. J. 2007. Evolution and mitotic nuclei of Physarum polycephalum plasmodia. persistence of the cilium. Cell Motility and the Cyto- Norwegian Journal of Botany 21:309–318. skeleton 64:906–913. Lenhosse´k M. von. 1898. U¨ ber flimmerzellen. Verhand- Staehelin L. A., Kang B.-H. 2008. Nanoscale architec- lungen der Anatomischen Gesellschaft 12:106–128. ture of endoplasmic reticulum export sites and of Margulis L. 1993. Symbiosis in Cell Evolution: Microbial Golgi membranes as determined by electron to- Communities in the Archaean and Proterozoic Eons. mography. Plant Physiology 147:1454–1468. Second Edition. New York: W. H. Freeman and Staub E., Fiziev P., Rosenthal A., Hinzmann B. 2004. Company. Insights into the evolution of the nucleolus by an Margulis L., Chapman M., Dolan M. F. 2007. Semes analysis of its protein domain repertoire. Bioessays for the analysis of evolution: de Duve’s peroxi- 26:567–581. somes and Myer’s hydrogenases in the sulphurous Surkov A. V., Dubinina G. A., Lysenko A. M., Glöckner Proterozoic eon. Nature Reviews Genetics 8:1–2. F. O., Kuever J. 2001. Dethiosulfovibrio russensis sp. Marshall W. F. 2009. Centriole evolution. Current Opin- nov., Dethiosulfovibrio marinus sp. nov. and Dethiosul- ion in Cell Biology 21:14–19. fovibrio acidaminovorans sp. nov., novel anaerobic, Mironov A. A., Banin V. V., Sesorova I. S., Dolgikh thiosulfate- and sulfur-reducing bacteria isolated V. V., Luini A., Beznoussenko G. V. 2007. Evolu- from ‘Thiodendron’ sulfur mats in different saline tion of the endoplasmic reticulum and the Golgi environments. International Journal of Systematic and complex. Advances in Experimental Medicine and Bi- Evolutionary Microbiology 51:327–337. ology 607:61–72. Tanaka K. 1973. Intranuclear microtubule organizing Moreira D., Ranjard L., Lope´z-Garcia P. 2004. The center in early prophase nuclei of the plasmo- nucleolar proteome and the (endosymbiotic) ori- dium of the slime mold, Physarum polycephalum. gin of the nucleolus. Bioessays 26:1144–1145. Journal of Cell Biology 57:220–224. Ohyanagi H., Ikeo K., Gojobori T. 2008. The origin of the nucleus: rebuild from the prokaryotic ances- tors of ribosome export factors. Gene 423:149–152. Handling Editor: Karl J. Niklas

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