The Invasion Begins!

: Serial Endosymbiosis Theory

Supporting Document: Viral Eukaryogenes is http://www.geocities .com/jjmohn/endos ymbios is .htm

The Serial Endosymbiosis Theory of Eukaryotic Evolution

by Jeremy Mohn The trans ition between eukaryotes , cells with nuclei, and prokaryotes , cells which lack nuclei, is cons idered by many biologis ts to be the mos t profound change in evolutionary his tory. In an attempt to des cribe the way in which this gap was bridged, s cientis ts have propos ed the s erial endos ymbios is theory (SET). The term endos ymbios is s pecifies the relations hip between organis ms which live one within another (s ymbiont within hos t) in a mutually beneficial relations hip. The SET s tates that the evolution of eukaryotes from prokaryotes involved the s ymbiotic union of s everal previous ly independent ances tors . According to the theory, thes e ances tors included a hos t cell, an ances tor of mitochondria, an ances tor of chloroplas ts , and, more controvers ially, a prokaryote that brought with it the s tructures that today provide cellular motion. The idea that the eukaryotic cell is actually a colony of microbes was firs t s ugges ted in the 1920s by American biologis t Ivan Wallin (Faus to-Sterling 1993). The originator of the modern vers ion of the SET is biologis t Lynn Margulis . In 1981, Margulis publis hed the firs t edition of her book entitled Symbios is in Cell Evolution in which s he propos ed that eukaryotic cells originated as communities of interacting entities that joined together in a s pecific order. With time, the members of this union became the organelles of a s ingle hos t (Margulis 1993). The organelle progenitors could have gained entry into a hos t cell as undiges ted prey or as an internal paras ite after which the combination became mutually beneficial to both organis ms . As the organis ms became more interdependent, an obligatory s ymbios is evolved. The SET pos tulates that the ances tors of mitochondria were free-living bacteria, s imilar to todays Daptobacter and Bdellovibrio, that developed the ability to efficiently res pire oxygen (Margulis and Sagan 1987). The ances tors of chloroplas ts , todays cyanobacteria, were originally independent photos ynthetic organis ms . In addition, the whiplike cilia that are common in eukaryotes but are not found in prokaryotes are thought to have derived from s till another group of free-living bacteria, the modern s pirochetes . According to the SET, the original prokaryotic hos t cell was an archaebacterium, s imilar to todays Thermoplas ma, that could withs tand high temperatures and acidic conditions (Margulis and Sagan 1987). This hos t cell was neither photos ynthetic nor capable of effectively us ing oxygen. Throughout her writings , Margulis contends that s ymbios is is a major driving force behind evolution. In her opinion, cooperation, interaction, and mutual dependence among life forms allowed for lifes eventual global dominance. As a res ult, Darwins notion of evolution as the s urvival of the fittes t, a continual competition among individuals and s pecies , is incomplete. According to Margulis and Sagan (1986), Life did not take over the globe by combat, but by networking. Rather than focus s olely on the elimination of competitors , Margulis view of evolution downplays competition its elf on the bas is of s ymbiotic relations hips . One early and important dis covery in s upport of the SET occurred in the laboratory of Kwang W. Jeon, a biologis t at the Univers ity of Tennes s ee. Jeon witnes s ed the es tablis hment of an amoeba-bacteria s ymbios is in which new bacterial s ymbionts became integrated in the hos t amoeba (Jeon 1991). In 1966, when the bacteria firs t infected the amoebas , they were lethal to their hos ts . However, as time progres s ed, s ome of the infected amoebas s urvived and became dependent on their newly acquired endos ymbionts within a few years . Jeon was able to prove this dependency by performing nuclei trans plants between infected amoebas and amoebas lacking the bacteria. If left alone, the hybrid amoebas died in a matter of days . Yet if he reinfected thes e hybrids with the once-lethal bacteria, the amoebas recovered and once again began to grow (Margulis and Sagan 1987). This dis covery s erved to demons trate that endos ymbios is could provide a major mechanis m for cellular evolution and explain the introduction of new s pecies (Jeon 1991). Although s ome of Margulis ideas remain controvers ial, there is mounting evidence in s upport of the SET (Faus to-Sterling 1993). The bulk of this evidence s erves to defend the notion of an endos ymbiotic origin of mitochondria and chloroplas ts . The recognition that new mitochondria and chloroplas ts can aris e only from preexis ting mitochondria and chloroplas ts was one of the firs t clues . Scientis ts found that mitochondria and chloroplas ts cannot be formed in a cell that lacks them becaus e nuclear genes only code for s ome of the proteins of which they are made. Als o, both mitochondria and chloroplas ts have their own s ets of genes that are more s imilar to thos e of prokaryotes than thos e of eukaryotes . They both contain a circular molecule of DNA, jus t like that found in prokaryotes . Finally, both mitochondria and chloroplas ts have their own protein-

s ynthes izing machinery. Their ribos omal s tructures and their ribos omal RNA (rRNA) more clos ely res emble thos e of prokaryotes . Thes e three lines of evidence have been cited to firmly es tablis h the theory of the origin of mitochondria and chloroplas ts through the proces s of endos ymbios is . The leas t accepted and mos t ques tionable as pect of the SET is the hypothes is that eukaryotic undulipodia originated from s pirochete bacteria (Margulis 1993). The term undulipodia is us ed to des cribe the eukaryotic motility organelles , flagella and cilia. Undulipodia are compos ed of microtubules in a s pecific configuration. Microtubules are compris ed of s everal clos ely related proteins called tubulins . Thes e s tructures are far larger and more complex than bacterial flagella, which are made of flagellin proteins . The SET pos tulates that undulipodia may be derived from bacteria through motility s ymbios es (Bermudes , Margulis , and Tzertzinis 1987). This idea is referred to as the exogenous hypothes is . The details of the argument are complex, but the s upporters of the SET point to s everal lines of circums tantial evidence. Their argument emphas izes the biology of the organelles thems elves , their dis tribution, and the occurrence of related and analogous s tructures . Opponents of this view, s upporters of the endogenous hypothes is , s ugges t that undulipodia originated internally as an extens ion of the microtubules utilized in mitos is . This hypothes is is als o referred to as direct filiation, which is the nons ymbiotic view of evolution that emphas izes the role of various kinds of mutations in the evolutionary s eparation of eukaryotic cells from prokaryotic cells . The main controvers y between the endogenous and exogenous hypothes es for the origin of undulipodia res ts upon a ques tion of chronology. Proponents of the endogenous hypothes is claim that microtubules preceded the origin of undulipodia, which eventually aros e endogenous ly. In contras t, the exogenous hypothes is s tates that motility s ymbios es gave ris e to cells with undulipodia, and this acquis ition s ubs equently led to the internal s tructures involved in mitos is (Bermudes , Margulis , and Tzertzinis 1987). Although the s ymbiotic origin of undulipodia is gaining s upport, the controvers y is yet to be s olved. According to Bermudes and Margulis (1985), there is ins ufficient evidence to prove either direct filiation or the s ymbiotic hypothes is for the origin of undulipodia. An important dis tinctive element of the SET is the overall chronology of s ymbiotic acquis itions in the origin of the eukaryotic cell. In order to fully unders tand the theorys implications for the clas s ification of all life forms , a brief s ummary of the current interpretation of endos ymbiotic events is neces s ary. According to the theory, eukaryotes evolved when archaeal and eubacterial cells merged in anaerobic s ymbios is . The archaeal cell provided the cytoplas m while the eubacterial cell (a s pirochete) allowed for mobility and, eventually, mitos is . Some of thes e anaerobic cells then incorporated oxygen-res piring eubacteria (s imilar to Daptobacter or Bdellovibrio) to become mitochondria-containing aerobes from which mos t protoctis ts , animals , and fungi evolved. Finally, s ome of thes e aerobes went on to incorporate photos ynthes izing cyanobacteria to become chloroplas t-containing algae and plants . The divis ions or domains implied by this des cription (Archaea, (true)Bacteria, and Eukarya) are cons is tent with the widely acknowledged clas s ification s ys tem des cribed by Ols en, Woes e, and Overbeek (1994). Although the nucleus is the defining characteris tic of the eukaryotic cell, the origin of this organelle and its relation to s ymbios is is uncertain. Margulis tends to favor a proces s involving the combination of direct filiation and s ymbios is as the s ource of the nucleated cell. She believes that s ome prokaryotic cells evolved primitive nuclei through direct filiation but remained prokaryotic. Others evolved thes e s ame s tructures but als o acquired other s ymbiotic genes and cons equently became eukaryotes (Margulis 1993). Overall, the traditional view of the origin of the nucleus s tates that the nuclear genome originated through direct evolution from an archaebacterial ances tor. A 1996 paper by Golding and Gupta dis putes the traditional view of the origin of the nucleus and s ugges ts an alternative called the chimeric model. The term chimeric refers to an organis m containing tis s ues from at leas t two genetically dis tinct parents . The chimeric model propos es that the firs t eukaryotic cell aros e as the res ult of a unus ual fus ion event between a Gram-negative eubacterium (hos t) without a cell wall and an archaebacterium (s ymbiont) in which both parents made major contributions to the cells nuclear genome. The nucleus appeared as the res ult of the folding in of the hos ts membrane around the engulfed cell. Such fus ion events are generally rejected by s upporters of the SET becaus e of the inability of pres ent-day bacteria to envelope prey. The chimeric model is bas ed on genetic and biochemical evidence. One piece of genetic evidence that s upports the model is the fact that prokaryotic cells are homogenomic (having genetic material from one parent only), whereas eukaryotic cells are heterogenomic (having genetic material from more than one parent). Biochemical evidence in s upport of the chimeric model involved the phylogenetic, or evolutionary, analys is of s equence data from proteins . This analys is demons trated a clos e relations hip between Gram-negative bacteria and eukaryotes on one hand and Gram-pos itive bacteria and archaebacteria on the other (Golding and Gupta 1996). Even more protein s equence data s ugges ted a relations hip between eukaryotes and archaebacteria. Thes e data imply that a s ymbiotic relations hip between Gram-negative bacteria and archaebacteria as the

progenitors of the eukaryotic cell is feas ible. Overall, the s equence data s upport the chimeric model. Recent res earch by Martin and Mller (1998) into the origin of the mitochondrion has led to a new theory of endos ymbios is called the hydrogen hypothes is . In the current picture of the origin of the eukaryotic cell, the mitochondrion was a lucky accident (Vogel 1998). The ances tral hos t cell s imply engulfed the mitochondrion ances tor, did not fully inges t it, and an even more s ucces s ful cell res ulted. According to the hydrogen hypothes is , however, the firs t eukaryotic cell did not form s imply by accident. Ins tead, it was the res ult of a purpos eful union between an archaebacterial hos t cell, a methanogen that cons umed hydrogen and carbon dioxide to produce methane, and a future mitochondrion s ymbiont that made hydrogen and carbon dioxide as was te products of anaerobic metabolis m. Thus , although the s ymbiont was probably capable of aerobic res piration, the s ymbios is began as a res ult of the products of anaerobic metabolis m. The hos ts dependence upon hydrogen produced by the s ymbiont is identified as the s elective principle that cons olidated the common ances tor of eukaryotic cells (Martin and Mller 1998). The hydrogen hypothes is has s ome important implications that contradict the current view of the relations hip between eukaryotes and archaebacteria. In the current view, the eukaryotes branched off from the archaebacteria long before the archaebacteria had divided into their pres ent-day groups . The hydrogen hypothes is implies that the firs t eukaryotes appeared much later in the evolutionary picture, meaning they are more clos ely tied to the archaebacteria. In order for the hydrogen hypothes is to be confirmed, an analys is of the complete s equences of eukaryotic and archaebacterial genomes mus t be completed (Vogel 1998). Another recent explanation of the origin of eukaryotes called the s yntrophic hypothes is was pres ented by Lpez-Garca and Moreira (1998). Though they were independently propos ed, the s yntrophic hypothes is is complementary in s everal as pects to the hydrogen hypothes is . Both hypothes es agree in the s ugges tion of an anaerobic metabolis m for the origin of mitochondrial s ymbios is . They are als o s trikingly s imilar in s ome metabolic details of the s ymbios is and archaeal molecular features (Lpez-Garcia and Moreira 1998). The major difference between the two hypothes es is in the nature of the original bacterial partners hip. As previous ly s tated, in the hydrogen hypothes is , the original s ymbios is is thought to have taken place between a methanogenic archaebacterium and a eubacterial ances tor to the mitochondrion. In the s yntrophic hypothes is , the original s ymbios is is conceived to have taken place between a methanogenic archaebacterium and an ances tral s ulfate-res piring delta-proteobacterium. The former provided the central genetic material and nucleic acid metabolis m while the latter provided mos t metabolic characteris tics (Lpez-Garcia and Moreira 1998). Mitochondria are thought to have derived from a later, independent s ymbiotic event. As with the hydrogen hypothes is , further genetic s equencing analys es are neces s ary in order for the claims of the s yntrophic hypothes is to be upheld. It has been nearly thirty years s ince Lynn Margulis firs t publis hed a book on the origin of eukaryotic cells . Since that time, biology has undergone extraordinary changes . The mos t noticeable change is the extens ive accumulation of s equence data for both nucleic acids and proteins . The collection of new data will undoubtedly lead to continuous revis ion of the s erial endos ymbios is theory of the origin of the eukaryotic cell. Des pite the uncertain future, the crucial foundation has been laid. Symbios is is now accepted by the s cientific community as an important factor in generating evolutionary change. The next s teps include the development of more elaborate methods to interpret genetic and molecular s equence data and the undertaking of a fres h look at the fos s il record. Thes e tactics might reveal s ignificant information concerning one of the mos t challenging and fas cinating problems in evolutionary biology, the origin of the eukaryotes .

Bibliography
Bermudes , D., L. Margulis , and G. Tzertzinis . 1987. Prokaryotic Origin of Undulipodia. In: Endocytobiology III (eds . John J. Lee and Jerome F. Fredrick). The New York Academy of Sciences , New York, pp. 187-197. Bermudes , D., and L. Margulis . 1985. Symbios is as a Mechanis m of Evolution: Status of the Symbios is Theory. Symbios is 1: 101-124. Faus to-Sterling, A. 1993. Is Nature Really Red in Tooth and Claw? Dis cover 14: 24-27. Jeon, K.W. 1991. Amoeba and x-Bacteria: Symbiont Acquis ition and Pos s ible Species Change. In: Symbios is as a Source of Evolutionary Innovation (eds . L. Margulis and R. Fes ter). The MIT Pres s , Cambridge, Mas s ., pp. 118-131. Lpez-Garca, P., and D. Moreira. 1998. Symbios is Between Methanogenic Archaea and delta-Proteobacteria as the Origin of Eukaryotes : The Syntrophic Hypothes is . Journal of Molecular Evolution 47: 517-530. Margulis , L. 1981. Symbios is in Cell Evolution, 1s t Edition. Freeman, New York. Margulis , L. 1993. Symbios is in Cell Evolution, 2nd Edition. Freeman, New York. Margulis , L., and D. Sagan. 1986. Microcos mos . Summit Books , New York. Margulis , L., and D. Sagan. 1987. Bacterial Bedfellows . Natural His tory 96(3): 26-33.

Martin, W., and M. Mller. 1998. The Hydrogen Hypothes is for the Firs t Eukaryote. Nature 392: 37-41. Ols en, G.J., C.R. Woes e, and R. Overbeek. 1994. The Winds of (Evolutionary) Change: Breathing Life into Microbiology. Journal of Bacteriology 176(1): 1-6. Vogel, G. Did the Firs t Complex Cell Eat Hydrogen? Science 279: 1633-1634.