Download The Serial Endosymbiosis Theory of Eukaryotic

The Serial Endosymbiosis Theory of Eukaryotic Evolution
by Jeremy Mohn
The transition between eukaryotes, cells with nuclei, and prokaryotes, cells which lack nuclei, is
considered by many biologists to be the most profound change in evolutionary history. In an
attempt to describe the way in which this gap was bridged, scientists have proposed the serial
endosymbiosis theory (SET). The term “endosymbiosis” specifies the relationship between
organisms which live one within another (symbiont within host) in a mutually beneficial
relationship. The SET states that the evolution of eukaryotes from prokaryotes involved the
symbiotic union of several previously independent ancestors. According to the theory, these
ancestors included a host cell, an ancestor of mitochondria, an ancestor of chloroplasts, and,
more controversially, a prokaryote that brought with it the structures that today provide cellular
motion.
The idea that the eukaryotic cell is actually a colony of microbes was first suggested in the
1920s by American biologist Ivan Wallin (Fausto-Sterling 1993). The originator of the modern
version of the SET is biologist Lynn Margulis. In 1981, Margulis published the first edition of her
book entitled Symbiosis in Cell Evolution in which she proposed that eukaryotic cells originated as
communities of interacting entities that joined together in a specific order. With time, the
members of this union became the organelles of a single host (Margulis 1993). The organelle
progenitors could have gained entry into a host cell as undigested prey or as an internal parasite
after which the combination became mutually beneficial to both organisms. As the organisms
became more interdependent, an obligatory symbiosis evolved.
The SET postulates that the ancestors of mitochondria were free-living bacteria, similar to
today’s Daptobacter and Bdellovibrio, that developed the ability to efficiently respire oxygen
(Margulis and Sagan 1987). The ancestors of chloroplasts, today’s cyanobacteria, were originally
independent photosynthetic organisms. In addition, the whiplike cilia that are common in
eukaryotes but are not found in prokaryotes are thought to have derived from still another group
of free-living bacteria, the modern spirochetes. According to the SET, the original prokaryotic
host cell was an archaebacterium, similar to today’s Thermoplasma, that could withstand high
temperatures and acidic conditions (Margulis and Sagan 1987). This host cell was neither
photosynthetic nor capable of effectively using oxygen.
Throughout her writings, Margulis contends that symbiosis is a major driving force behind
evolution. In her opinion, cooperation, interaction, and mutual dependence among life forms
allowed for life’s eventual global dominance. As a result, Darwin’s notion of evolution as the
“survival of the fittest,” a continual competition among individuals and species, is incomplete.
According to Margulis and Sagan (1986), “Life did not take over the globe by combat, but by
networking.” Rather than focus solely on the elimination of competitors, Margulis’ view of
evolution downplays competition itself on the basis of symbiotic relationships.
One early and important discovery in support of the SET occurred in the laboratory of Kwang W.
Jeon, a biologist at the University of Tennessee. Jeon witnessed the establishment of an amoebabacteria symbiosis in which new bacterial symbionts became integrated in the host amoeba (Jeon
1991). In 1966, when the bacteria first infected the amoebas, they were lethal to their hosts.
However, as time progressed, some of the infected amoebas survived and became dependent on
their newly acquired endosymbionts within a few years. Jeon was able to prove this dependency
by performing nuclei transplants between infected amoebas and amoebas lacking the bacteria. If
left alone, the hybrid amoebas died in a matter of days. Yet if he reinfected these hybrids with
the once-lethal bacteria, the amoebas recovered and once again began to grow (Margulis and
Sagan 1987). This discovery served to demonstrate that endosymbiosis could provide a major
mechanism for cellular evolution and explain the introduction of new species (Jeon 1991).
Although some of Margulis’ ideas remain controversial, there is mounting evidence in support of
the SET (Fausto-Sterling 1993). The bulk of this evidence serves to defend the notion of an
endosymbiotic origin of mitochondria and chloroplasts. The recognition that new mitochondria
and chloroplasts can arise only from preexisting mitochondria and chloroplasts was one of the
first clues. Scientists found that mitochondria and chloroplasts cannot be formed in a cell that
lacks them because nuclear genes only code for some of the proteins of which they are made.
Also, both mitochondria and chloroplasts have their own sets of genes that are more similar to
those of prokaryotes than those of eukaryotes. They both contain a circular molecule of DNA,
just like that found in prokaryotes. Finally, both mitochondria and chloroplasts have their own
protein-synthesizing machinery. Their ribosomal structures and their ribosomal RNA (rRNA) more
closely resemble those of prokaryotes. These three lines of evidence have been cited to firmly
establish the theory of the origin of mitochondria and chloroplasts through the process of
endosymbiosis.
The least accepted and most questionable aspect of the SET is the hypothesis that eukaryotic
undulipodia originated from spirochete bacteria (Margulis 1993). The term “undulipodia” is used
to describe the eukaryotic motility organelles, flagella and cilia. Undulipodia are composed of
microtubules in a specific configuration. Microtubules are comprised of several closely related
proteins called tubulins. These structures are far larger and more complex than bacterial flagella,
which are made of flagellin proteins. The SET postulates that undulipodia may be derived from
bacteria through motility symbioses (Bermudes, Margulis, and Tzertzinis 1987). This idea is
referred to as the exogenous hypothesis. The details of the argument are complex, but the
supporters of the SET point to several lines of circumstantial evidence. Their argument
emphasizes the biology of the organelles themselves, their distribution, and the occurrence of
related and analogous structures. Opponents of this view, supporters of the endogenous
hypothesis, suggest that undulipodia originated internally as an extension of the microtubules
utilized in mitosis. This hypothesis is also referred to as direct filiation, which is the nonsymbiotic
view of evolution that emphasizes the role of various kinds of mutations in the evolutionary
separation of eukaryotic cells from prokaryotic cells.
The main controversy between the endogenous and exogenous hypotheses for the origin of
undulipodia rests upon a question of chronology. Proponents of the endogenous hypothesis claim
that microtubules preceded the origin of undulipodia, which eventually arose endogenously. In
contrast, the exogenous hypothesis states that motility symbioses gave rise to cells with
undulipodia, and this acquisition subsequently led to the internal structures involved in mitosis
(Bermudes, Margulis, and Tzertzinis1987). Although the symbiotic origin of undulipodia is gaining
support, the controversy is yet to be solved. According to Bermudes and Margulis (1985), there is
insufficient evidence to prove either direct filiation or the symbiotic hypothesis for the origin of
undulipodia.
An important distinctive element of the SET is the overall chronology of symbiotic acquisitions in
the origin of the eukaryotic cell. In order to fully understand the theory’s implications for the
classification of all life forms, a brief summary of the current interpretation of endosymbiotic
events is necessary. According to the theory, eukaryotes evolved when archaeal and eubacterial
cells merged in anaerobic symbiosis. The archaeal cell provided the cytoplasm while the
eubacterial cell (a spirochete) allowed for mobility and, eventually, mitosis. Some of these
anaerobic cells then incorporated oxygen-respiring eubacteria (similar to Daptobacter or
Bdellovibrio) to become mitochondria-containing aerobes from which most protoctists, animals,
and fungi evolved. Finally, some of these aerobes went on to incorporate photosynthesizing
cyanobacteria to become chloroplast-containing algae and plants. The divisions or domains
implied by this description (Archaea, (true)Bacteria, and Eukarya) are consistent with the widely
acknowledged classification system described by Olsen, Woese, and Overbeek (1994).
Although the nucleus is the defining characteristic of the eukaryotic cell, the origin of this
organelle and its relation to symbiosis is uncertain. Margulis tends to favor a process involving
the combination of direct filiation and symbiosis as the source of the nucleated cell. She believes
that some prokaryotic cells evolved primitive nuclei through direct filiation but remained
prokaryotic. Others evolved these same structures but also acquired other symbiotic genes and
consequently became eukaryotes (Margulis 1993). Overall, the traditional view of the origin of
the nucleus states that the nuclear genome originated through direct evolution from an
archaebacterial ancestor.
A 1996 paper by Golding and Gupta disputes the traditional view of the origin of the nucleus and
suggests an alternative called the chimeric model. The term “chimeric” refers to an organism
containing tissues from at least two genetically distinct parents. The chimeric model proposes
that the first eukaryotic cell arose as the result of a unusual fusion event between a Gramnegative eubacterium (host) without a cell wall and an archaebacterium (symbiont) in which both
parents made major contributions to the cell’s nuclear genome. The nucleus appeared as the
result of the folding in of the host’s membrane around the engulfed cell. Such fusion events are
generally rejected by supporters of the SET because of the inability of present-day bacteria to
envelope prey.
The chimeric model is based on genetic and biochemical evidence. One piece of genetic
evidence that supports 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 support of the chimeric
model involved the phylogenetic, or evolutionary, analysis of sequence data from proteins. This
analysis demonstrated a close relationship between Gram-negative bacteria and eukaryotes on
one hand and Gram-positive bacteria and archaebacteria on the other (Golding and Gupta 1996).
Even more protein sequence data suggested a relationship between eukaryotes and
archaebacteria. These data imply that a symbiotic relationship between Gram-negative bacteria
and archaebacteria as the progenitors of the eukaryotic cell is feasible. Overall, the sequence
data support the chimeric model.
Recent research by Martin and Müller (1998) into the origin of the mitochondrion has led to a
new theory of endosymbiosis called the “hydrogen hypothesis.” In the current picture of the
origin of the eukaryotic cell, the mitochondrion was a “lucky accident” (Vogel 1998). The
ancestral host cell simply engulfed the mitochondrion ancestor, did not fully ingest it, and an
even more successful cell resulted. According to the hydrogen hypothesis, however, the first
eukaryotic cell did not form simply by accident. Instead, it was the result of a purposeful union
between an archaebacterial host cell, a methanogen that consumed hydrogen and carbon dioxide
to produce methane, and a future mitochondrion symbiont that made hydrogen and carbon
dioxide as waste products of anaerobic metabolism. Thus, although the symbiont was probably
capable of aerobic respiration, the symbiosis began as a result of the products of anaerobic
metabolism. The host’s dependence upon hydrogen produced by the symbiont is identified as the
selective principle that consolidated the common ancestor of eukaryotic cells (Martin and Müller
1998).
The hydrogen hypothesis has some important implications that contradict the current view of the
relationship between eukaryotes and archaebacteria. In the current view, the eukaryotes
branched off from the archaebacteria long before the archaebacteria had divided into their
present-day groups. The hydrogen hypothesis implies that the first eukaryotes appeared much
later in the evolutionary picture, meaning they are more closely tied to the archaebacteria. In
order for the hydrogen hypothesis to be confirmed, an analysis of the complete sequences of
eukaryotic and archaebacterial genomes must be completed (Vogel 1998).
Another recent explanation of the origin of eukaryotes called the “syntrophic hypothesis” was
presented by López-García and Moreira (1998). Though they were independently proposed, the
syntrophic hypothesis is complementary in several aspects to the hydrogen hypothesis. Both
hypotheses agree in the suggestion of an anaerobic metabolism for the origin of mitochondrial
symbiosis. They are also strikingly similar in some metabolic details of the symbiosis and archaeal
molecular features (López-Garcia and Moreira 1998). The major difference between the two
hypotheses is in the nature of the original bacterial partnership. As previously stated, in the
hydrogen hypothesis, the original symbiosis is thought to have taken place between a
methanogenic archaebacterium and a eubacterial ancestor to the mitochondrion. In the
syntrophic hypothesis, the original symbiosis is conceived to have taken place between a
methanogenic archaebacterium and an ancestral sulfate-respiring delta-proteobacterium. The
former provided the central genetic material and nucleic acid metabolism while the latter
provided most metabolic characteristics (López-Garcia and Moreira 1998). Mitochondria are
thought to have derived from a later, independent symbiotic event. As with the hydrogen
hypothesis, further genetic sequencing analyses are necessary in order for the claims of the
syntrophic hypothesis to be upheld.
It has been nearly thirty years since Lynn Margulis first published a book on the origin of
eukaryotic cells. Since that time, biology has undergone extraordinary changes. The most
noticeable change is the extensive accumulation of sequence data for both nucleic acids and
proteins. The collection of new data will undoubtedly lead to continuous revision of the serial
endosymbiosis theory of the origin of the eukaryotic cell. Despite the uncertain future, the crucial
foundation has been laid. Symbiosis is now accepted by the scientific community as an important
factor in generating evolutionary change. The next steps include the development of more
elaborate methods to interpret genetic and molecular sequence data and the undertaking of a
fresh look at the fossil record. These tactics might reveal significant information concerning one
of the most challenging and fascinating problems in evolutionary biology, the origin of the
eukaryotes.
Bibliography
o
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Fausto-Sterling, A. 1993. Is Nature Really Red in Tooth and Claw? Discover 14: 24-27.
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
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