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Home , Emile Zuckerkandl, Ford Doolittle, Tree of life, Tree of life (biology)

About 10 years ago scientists finally worked out Uprooting the basic outline of how the modern life-forms evolved. Now parts of their tidy scheme are unraveling by W.Ford Doolittle Instead of looking just at anatomy or physiology, they asked, why not base family trees on differences in the order of the building blocks in selected or proteins? harles Darwin contended more than a century Their approach, known as molecular phylogeny, is emi- ago that all modern species diverged from a nently logical. Individual genes, composed of unique se- more limited set of ancestral groups, which quences of nucleotides, typically serve as the blueprints for themselves evolved from still fewer progeni- making specific proteins, which consist of particular strings tors and so on back to the beginning of life. In of amino acids. All genes, however, mutate (change in se- C principle, then, the relationships among all liv- quence), sometimes altering the encoded protein. Genetic mu- ing and extinct could be represented as a single ge- tations that have no effect on protein function or that im- nealogical tree. prove it will inevitably accumulate over time. Thus, as two Most contemporary researchers agree. Many would even species diverge from an ancestor, the sequences of the genes argue that the general features of this tree are already known, they share will also diverge. And as time passes, the genetic all the way down to the root—a solitary cell, termed life’s last divergence will increase. Investigators can therefore recon- universal common ancestor, that lived roughly 3.5 to 3.8 bil- lion years ago. The consensus view did not come easily but has been widely accepted for more than a decade. Yet ill winds are blowing. To everyone’s surprise, discover- Other bacteria ies made in the past few years have begun to cast serious doubt on some aspects of the tree, especially on the depiction of the relationships near the root.

The First Sketches

cientists could not even begin to contemplate constructing Sa universal tree until about 35 years ago. From the time of Aristotle to the 1960s, researchers deduced the relatedness of organisms by comparing their anatomy or physiology, or both. For complex organisms, they were frequently able to draw reasonable genealogical inferences in this way. Detailed analyses of innumerable traits suggested, for instance, that hominids shared a common ancestor with apes, that this common ancestor shared an earlier one with monkeys, and that that precursor shared an even earlier forebear with prosimians, and so forth. Microscopic single-celled organisms, however, often pro- vided too little information for defining relationships. That Hyperthermophilic paucity was disturbing because microbes were the only in- bacteria habitants of the for the first half to two thirds of the planet’s history; the absence of a clear phylogeny (family tree) for microorganisms left scientists unsure about the sequence in which some of the most radical innovations in cellular struc- ture and function occurred. For example, between the birth CONSENSUS VIEW of the universal tree of life holds that the of the first cell and the appearance of multicellular fungi, early descendants of life’s last universal common ancestor—a plants and animals, cells grew bigger and more complex, small cell with no nucleus—divided into two prokaryotic (non- gained a nucleus and a cytoskeleton (internal scaffolding), nucleated) groups: the bacteria and the . Later, the ar- chaea gave rise to organisms having complex cells containing a and found a way to eat other cells. nucleus: the . Eukaryotes gained valuable energy-gen- In the mid-1960s Emile Zuckerkandl and of erating organelles—mitochondria and, in the case of plants, the Institute of Technology conceived of a revolu- —by taking up, and retaining, certain bacteria. tionary strategy that could supply the missing information.

90 Scientific American February 2000 Copyright 2000 Scientific American, Inc. struct the evolutionary past of living species—can construct data to draw some important inferences. Since then, phyloge- their phylogenetic trees—by assessing the sequence diver- neticists studying microbial , as well as investigators gence of genes or proteins isolated from those organisms. concerned with higher sections of the universal tree, have Thirty-five years ago scientists were just becoming profi- based many of their branching patterns on sequence analyses cient at identifying the order of amino acids in proteins and of SSU rRNA genes. This accumulation of rRNA data helped could not yet sequence genes. Protein studies completed in the greatly to foster consensus about the universal tree in the late 1960s and 1970s demonstrated the general utility of molecu- 1980s. Today investigators have rRNA sequences for several lar phylogeny by confirming and then extending the family thousands of species. trees of well-studied groups such as the vertebrates. They also From the start, the rRNA results corroborated some already lent support to some hypotheses about the links among cer- accepted ideas, but they also produced an astonishing surprise. tain bacteria—showing, for instance, that bacteria capable of By the 1960s microscopists had determined that the world of producing oxygen during photosynthesis form a group of living things could be divided into two separate groups, eukary- their own (cyanobacteria). otes and , depending on the structure of the cells As this protein work was progressing, Carl R. Woese of the that composed them. Eukaryotic organisms (animals, plants, University of Illinois was turning his attention to a powerful fungi and many unicellular life-forms) were defined as those new yardstick of evolutionary distances: small subunit riboso- composed of cells that contained a true nucleus—a membrane- mal RNA (SSU rRNA). This genetically specified molecule is a bound organelle housing the chromosomes. Eukaryotic cells key constituent of ribosomes, the “factories” that construct proteins in cells, and cells throughout time have needed it to survive. These features suggested to Woese in the late 1960s EUKARYOTES that variations in SSU rRNA (or more precisely in the genes encoding it) would reliably indicate the relatedness among Animals Fungi Plants any life-forms, from the plainest bacteria to the most complex animals. Small subunit ribosomal RNA could thus serve, in Woese’s words, as a “universal molecular chronometer.” Initially the methods available for the project were indirect and laborious. By the late 1970s, though, Woese had enough

ARCHAEA Algae Crenarchaeota Euryarchaeota

Proteobacteria

Ciliates loroplasts Bacteria that gave rise to ch Other single- }cell eukaryotes t gave rise to mitochondria Bacteria tha

Korarchaeota G N I N N E R B

A N

Last Universal Common Ancestor A J (single cell) Scientific American February 2000 91 Copyright 2000 Scientific American, Inc. HYPOTHESIS proposes that mitochondria formed after a MITOCHONDRION that had evolved into an early en- gulfed (a) and then kept (b) one or more al- pha-proteobacteria cells. Eventually, the d Cell acquires second symbiont, bacterium gave up its ability to live on which becomes the chloroplast its own and transferred some of its genes to the nucleus of the host CYANOBACTERIAL (c), becoming a mitochondri- FOOD on. Later, some mitochondri- SYMBIONT on-bearing eukaryote ingest- c Symbiont loses many ed a cyanobacterium that genes, and some genes became the chloroplast (d). transfer to nucleus H C

SSU rRNA. Hence, once the I R M

right tools became available in the mid- U L B

H

1970s, investigators decided to see if P O T S those RNA genes were inherited from I R H alpha-proteobacteria and cyanobacteria, C b Eukaryote retains bacterium PRIMITIVE as a symbiont respectively—as the endosymbiont hy- EUKARYOTE pothesis would predict. They were. CHROMOSOME One deduction, however, introduced NUCLEUS a discordant note into all this harmony. INTERNAL MEMBRANE In the late 1970s Woese asserted that CYTOSKELETON BACTERIAL FOOD (ALPHA-PROTEOBACTERIUM) the two- view of life, dividing the world into bacteria and eukaryotes, was no longer tenable; a three-domain construct had to take its place. PROKARYOTE a Cell loses wall, grows, acquires other eukaryotic features and ingests a bacterium Certain prokaryotes classified as bac- DNA RIBOSOME teria might look like bacteria but, he in- MEMBRANE sisted, were genetically much different. CELL WALL In fact, their rRNA supported an early cient anaerobic prokaryote (unable to separation. Many of these species had use oxygen for energy) lost its cell wall. already been noted for displaying unusu- also displayed other prominent features, The more flexible membrane under- al behavior, such as favoring extreme en- among them a cytoskeleton, an intricate neath then began to grow and fold in vironments, but no one had disputed system of internal membranes and, usu- on itself. This change, in turn, led to their status as bacteria. Now Woese ally, mitochondria (organelles that per- formation of a nucleus and other inter- claimed that they formed a third primary form respiration, using oxygen to ex- nal membranes and also enabled the group—the archaea—as different from tract energy from nutrients). In the case cell to engulf and digest neighboring bacteria as bacteria are from eukaryotes. of algae and higher plants, the cells also prokaryotes, instead of gaining nour- contained chloroplasts (photosynthetic ishment entirely by absorbing small Acrimony, Then Consensus organelles). molecules from its environment. Prokaryotes, thought at the time to be At some point, one of the descen- t first, the claim met enormous resis- synonymous with bacteria, were noted to dants of this primitive eukaryote took Atance. Yet eventually most scientists consist of smaller and simpler nonnucle- up bacterial cells of the type known as became convinced, in part because the ated cells. They are usually enclosed by alpha-proteobacteria, which are profi- overall structures of certain molecules both a membrane and a rigid outer wall. cient at respiration. But instead of di- in archaeal species corroborated the Woese’s early data supported the dis- gesting this “food,” the eukaryote set- three-group arrangement. For instance, tinction between prokaryotes and eu- tled into a mutually beneficial (symbiot- the cell membranes of all archaea are karyotes, by establishing that the SSU ic) relationship with it. The eukaryote made up of unique lipids (fatty sub- rRNAs in typical bacteria were more sheltered the internalized cells, and the stances) that are quite distinct—in their similar in sequence to one another than “” provided extra ener- physical properties, chemical constituents to the rRNA of eukaryotes. The initial gy to the host through respiration. Fi- and linkages—from the lipids of bacteria. rRNA findings also lent credence to nally, the endosymbionts lost the genes Similarly, the archaeal proteins respon- one of the most interesting notions in they formerly used for independent sible for several crucial cellular processes evolutionary cell biology: the endosym- growth and transferred others to the have a distinct structure from the pro- biont hypothesis. This conception aims host’s nucleus—becoming mitochon- teins that perform the same tasks in bac- to explain how eukaryotic cells first dria in the process. Likewise, chloro- teria. transcription and translation came to possess mitochondria and plasts derive from cyanobacteria that an are two of those processes. To make a chloroplasts [see “The Birth of Com- early, mitochondria-bearing eukaryote protein, a cell first copies, or transcribes, plex Cells,” by Christian de Duve, Sci- took up and kept. the corresponding gene into a strand of entific American, April 1996]. Mitochondria and chloroplasts in messenger RNA. Then ribosomes trans- On the way to becoming a eukary- modern eukaryotes still retain a small late the messenger RNA codes into a ote, the hypothesis proposes, some an- number of genes, including those that specific string of amino acids. Bio-

92 Scientific American February 2000 Uprooting the Tree of Life Copyright 2000 Scientific American, Inc. chemists found that archaeal RNA tions that many genes involved in tran- or cyanobacterial precursors of these polymerase, the enzyme that carries out scription and translation are much the organelles. The transferred genes, more- gene transcription, more resembles its same in eukaryotes and archaea and over, would be ones involved in respira- eukaryotic than its bacterial counter- that these processes are performed very tion or photosynthesis, not in cellular parts in complexity and in the nature of similarly in the two domains. Further, processes that would already be han- its interactions with DNA. The protein although archaea do not have nuclei, dled by genes inherited from the ances- components of the ribosomes that under certain experimental conditions tral archaean. translate archaeal messenger RNAs are their chromosomes resemble those of Those expectations have been violat- also more like the ones in eukaryotes eukaryotes: the DNA appears to be as- ed. Nuclear genes in eukaryotes often than those in bacteria. sociated with eukaryote-type proteins derive from bacteria, not solely from Once scientists accepted the idea of called histones, and the chromosomes archaea. A good number of those bac- three domains of life instead of two, they can adopt a eukaryotic “beads-on-a- terial genes serve nonrespiratory and naturally wanted to know which of the string” structure. These chromosomes nonphotosynthetic processes that are two structurally primitive groups—bacte- are replicated by a suite of proteins, arguably as critical to cell survival as ria or archaea—gave rise to the first eu- most of which are found in some form are transcription and translation. karyotic cell. The studies that showed a in eukaryotes but not in bacteria. The classic tree also indicates that kinship between the transcription and bacterial genes migrated only to a eu- translation machinery in archaea and eu- Nevertheless, Doubts karyote, not to any archaea. Yet we are karyotes implied that eukaryotes diverged seeing signs that many archaea possess a from the archaeans. he accumulation of all these won- substantial store of bacterial genes. One This deduction gained added credibil- Tderfully consistent data was grati- example among many is Archaeoglobus ity in 1989, when groups led by J. Peter fying and gave rise to the now accepted fulgidus. This meets all the Gogarten of the University of Connecti- arrangement of the universal genealogi- criteria for an archaean (it has all the cut and Takashi Miyata, then at Kyushu cal tree. This phylogeny indicates that proper lipids in its cell membrane and University in Japan, used sequence in- life diverged first into bacteria and ar- the right transcriptional and translation- formation from genes for other cellular chaea. Eukaryotes then evolved from al machinery), but it uses a bacterial components to “root” the universal tree. an archaealike precursor. Subsequently, form of the enzyme HMGCoA reduc- Comparisons of SSU rRNA can indicate eukaryotes took up genes from bacteria tase for synthesizing membrane lipids. It which organisms are closely related to twice, obtaining mitochondria from al- also has numerous bacterial genes that one another but, for technical reasons, pha-proteobacteria and chloroplasts help it to gain energy and nutrients in one cannot by themselves indicate which from cyanobacteria. of its favorite habitats: undersea oil wells. groups are oldest and therefore closest to Still, as DNA sequences of complete The most reasonable explanation for the root of the tree. The DNA sequences have become increasingly avail- these various contrarian results is that encoding two essential cellular proteins able, my group and others have noted the pattern of evolution is not as linear agreed that the last common ancestor patterns that are disturbingly at odds and treelike as Darwin imagined it. Al- spawned both the bacteria and the ar- with the prevailing beliefs. chaea; then the eukaryotes branched If the consensus tree were from the archaea. correct, researchers would Metamonads Since 1989 a host of discoveries have expect the only bacterial Nematodes supported that depiction. In the past genes in eukaryotes to be five years, sequences of the full those in mitochondrial or (the total complement of genes) in half a chloroplast DNA or to be dozen archaea and more than 15 bacte- those that were trans- EUKARYOTES ria have become available. Comparisons ferred to the nucleus from of such genomes confirm earlier sugges- the alpha-proteobacterial Maize

Root BACTERIA (based on other data) y t i s r e v i

n Rickettsia U

Trypanosomes e i s u o h l a D

Parabasalids R

E Mitochondria C ; N H E C I P R S . F M

U D

L Methanococcus I B V

A Cyanobacteria H D P

: Aquifex O E T C S R I R U Sulfolobus

H ARCHAEA O C S Chloroplasts

RELATIONSHIPS among ribosomal RNAs (rRNAs) from almost or mitochondrial genes. The mitochondrial lines are relatively long 600 species are depicted. A single line represents the rRNA sequence because mitochondrial genes evolve rapidly. Trees derived from in one species or a group; many of the lines reflect rRNAs encoded rRNA data are rootless; other data put the root at the colored dot, by nuclear genes, but others reflect rRNAs encoded by chloroplast corresponding to the lowest part of the tree on pages 90 and 91.

Uprooting the Tree of Life Scientific American February 2000 93 Copyright 2000 Scientific American, Inc. though genes are passed vertically from slipped those surprising genes into the too pat as well. A host of genes and bio- generation to generation, this vertical eukaryotic nuclear genome horizontally. chemical features do unite the prokary- inheritance is not the only important In truth, microbiologists have long otes that biologists now call archaea process that has affected the evolution known that bacteria exchange genes and distinguish those organisms from of cells. Rampant operation of a differ- horizontally. Gene swapping is clearly the prokaryotes we call bacteria, but ent process—lateral, or horizontal, gene how some disease-causing bacteria give bacteria and archaea (as well as species transfer—has also affected the course of the gift of antibiotic resistance to other within each group) have clearly en- that evolution profoundly. Such transfer species of infectious bacteria. But few gaged in extensive gene swapping. involves the delivery of single genes, or researchers suspected that genes essen- Researchers might choose to define whole suites of them, not from a parent tial to the very survival of cells traded evolutionary relationships within the cell to its offspring but across species hands frequently or that lateral transfer prokaryotes on the basis of genes that barriers. exerted great influence on the early his- seem least likely to be transferred. In- Lateral gene transfer would explain tory of microbial life. Apparently, we deed, many investigators still assume how eukaryotes that supposedly evolved were mistaken. that genes for SSU rRNA and the pro- from an archaeal cell obtained so many teins involved in transcription and trans- bacterial genes important to metabolism: Can the Tree Survive? lation are unlikely to be moveable and the eukaryotes picked up the genes from that the based on them bacteria and kept those that proved use- hat do the new findings say about thus remains valid. But this nontrans- ful. It would likewise explain how vari- Wthe structure of the universal tree ferability is largely an untested assump- ous archaea came to possess genes usu- of life? One lesson is that the neat pro- tion, and in any case, we must now ad- ally found in bacteria. gression from archaea to eukaryote in mit that any tree is at best a description Some molecular phylogenetic theo- the consensus tree is oversimplified or of the evolutionary history of only part rists—among them, Mitchell L. Sogin of wrong. Plausibly, eukaryotes emerged of an organism’s genome. The consen- the Marine Biological Laboratory in not from an archaean but from some sus tree is an overly simplified depiction. Woods Hole, Mass., and Russell F. precursor cell that was the product of What would a truer model look like? Doolittle (my very distant relative) of the any number of horizontal gene trans- At the top, treelike branching would University of California at San Diego— fers—events that left it part bacterial continue to be apt [see illustration on have also invoked lateral gene transfer to and part archaean and maybe part oth- opposite page] for multicellular animals, explain a long-standing mystery. Many er things. plants and fungi. And gene transfers in- eukaryotic genes turn out to be unlike The weight of evidence still supports volved in the formation of bacteria-de- those of any known archaea or bacteria; the likelihood that mitochondria in eu- rived mitochondria and chloroplasts in they seem to have come from nowhere. karyotes derived from alpha-proteobac- eukaryotes would still appear as fusions Notable in this regard are the genes for terial cells and that chloroplasts came of major branches. Below these transfer the components of two defining eukary- from ingested cyanobacteria, but it is no points (and continuing up into the mod- otic features, the cytoskeleton and the longer safe to assume that those were ern bacterial and archaeal domains), we system of internal membranes. Sogin the only lateral gene transfers that oc- would, however, see a great many addi- and Doolittle suppose that some fourth curred after the first eukaryotes arose. tional branch fusions. Deep in the realm domain of organisms, now extinct, Only in later, multicellular eukaryotes do of the prokaryotes and perhaps at the we know of definite restrictions on hori- base of the eukaryotic domain, designa- Borrelia zontal gene exchange, such as the advent tion of any trunk as the main one would of separated (and protected) germ cells. be arbitrary. The standard depiction of the rela- Though complicated, even this revised tionships within the prokaryotes seems BACTERIA picture would actually be misleadingly simple, a sort of shorthand cartoon, be- cause the fusing of branches usually Archaean having Archaeoglobus a bacterial EUKARYOTES would not represent the joining of whole reductase gene [ fulgidus genomes, only the transfers of single or Animals multiple genes. The full picture would Pseudomonas Dictyostelium have to display simultaneously the super- Streptococcus Streptococcus imposed genealogical patterns of thou- pyogenes pneumoniae Fungi sands of different families of genes (the rRNA genes form just one such family). Sulfolobus Plants If there had never been any lateral MINI PHYLOGENETIC TREE transfer, all these individual gene trees groups species according to differ- Haloferax Trypanosoma would have the same topology (the ences in a gene coding for the en- same branching order), and the ances- zyme HMGCoA reductase. It shows Methanobacterium Methanococcus that the reductase gene in Archaeo- tral genes at the root of each tree would globus fulgidus, a definite archaean, came ARCHAEA have all been present in the genome of

H the universal last common ancestor, a

from a bacterium, not from an archaean an- C I R

cestor. This finding is part of growing evidence in- M single ancient cell. But extensive trans- U L B dicating that the evolution of unicellular life has long been influenced H fer means that neither is the case: gene P O

profoundly by lateral gene transfer (occurring between contemporaries). T

S trees will differ (although many will I R

The consensus universal tree does not take that influence into account. H C have regions of similar topology), and

94 Scientific American February 2000 Uprooting the Tree of Life Copyright 2000 Scientific American, Inc. there would never have been a single eukaryotes].” In other words, early confusing and discouraging. It is as if cell that could be called the last univer- cells, each having relatively few genes, we have failed at the task that Darwin sal common ancestor. differed in many ways. By swapping set for us: delineating the unique struc- As Woese has written, “The ancestor genes freely, they shared various of their ture of the tree of life. But in fact, our cannot have been a particular organ- talents with their contemporaries. Even- science is working just as it should. An ism, a single organismal lineage. It was tually this collection of eclectic and attractive hypothesis or model (the sin- communal, a loosely knit, diverse con- changeable cells coalesced into the three gle tree) suggested experiments, in this glomeration of primitive cells that basic domains known today. These do- case the collection of gene sequences evolved as a unit, and it eventually de- mains remain recognizable because and their analysis with the methods of veloped to a stage where it broke into much (though by no means all) of the molecular phylogeny. The data show several distinct communities, which in gene transfer that occurs these days goes the model to be too simple. Now new their turn become the three primary on within domains. hypotheses, having final forms we can- lines of descent [bacteria, archaea and Some biologists find these notions not yet guess, are called for. SA

EUKARYOTES REVISED “TREE” OF LIFE retains a treelike structure at the top of the eukaryotic do- main and acknowledges that eukaryotes obtained mitochondria and chloroplasts from Animals Fungi Plants bacteria. But it also includes an extensive network of untreelike links between branch- es. Those links have been inserted somewhat randomly to symbolize the rampant later- al gene transfer of single or multiple genes that has always occurred between unicellu- lar organisms. This “tree” also lacks a single cell at the root; the three major domains of life probably arose from a population of primitive cells that differed in their genes.

BACTERIA ARCHAEA Algae Other bacteria Cyanobacteria Crenarchaeota Euryarchaeota Proteobacteria

Ciliates t gave rise to chloroplasts eria tha Bact Other single- cell eukaryotes to mitochondria ia that gave rise Bacter }

Korarchaeota

Hyperthermophilic bacteria G N I N N E R B A N A J Common Ancestral Community of Primitive Cells

The Author Further Information

W. FORD DOOLITTLE, who holds de- The Universal Ancestor. in the Proceedings of the National Academy of grees from Harvard and Stanford universi- Sciences, Vol. 95, No. 12, pages 6854–6859; June 9, 1998. ties, is professor of biochemistry and molec- You Are What You Eat: A Gene Transfer Rachet Could Account for Bacterial ular biology at Dalhousie University in Hali- Genes in Eukaryotic Nuclear Genomes. W. Ford Doolittle in Trends in Genetics, Vol. fax, Nova Scotia, and director of the Program 14, No. 8, pages 307–311; August 1998. in of the Canadian In- Phylogenetic Classification and the Universal Tree. W. Ford Doolittle in Science, stitute for Advanced Research. Vol. 284, pages 2124–2128; June 25, 1999.

Uprooting the Tree of Life Scientific American February 2000 95 Copyright 2000 Scientific American, Inc.