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REVIEW
One Plus One Equals One:
Symbiosis and the Evolution of Complex Life
by John Archibald
Oxford: Oxford University Press, 2014. 224 pages
reviewed by Susan Spath
The eukaryotic cell originated more than a billion years ago (Knoll and others 2006). It was
a fundamental event in the history of life. As microbiologist John Archibald writes in One
Plus One Equals One, without eukaryotes, “There would be no plants or animals of any
kind. And we wouldn’t be here to ponder our existence” (page 10).
In the last sixty years, scientists have learned a lot about the emergence of cells that contain distinct organelles and a membrane-bound nucleus. In his lively, engaging account,
Archibald relates what is now known about the origin of eukaryotes and presents the
questions that remain. The centerpiece of his book is the endosymbiont theory, which
holds that the eukaryotic cell evolved in whole or in part through symbiotic associations
of prokaryotes. Archibald recounts the changing fortunes of this idea from its beginnings
through its neglect to its revival, refinement, contestation, and eventual acceptance. Archibald interweaves explanations of current biological knowledge with historical sketches
of how it was obtained as he describes the strong personalities, bold ideas, sharp controversies, experimental techniques and diverse organisms that have contributed to understanding the evolutionary significance of endosymbiosis.
Archibald begins by introducing chloroplasts and mitochondria, the organelles in which
photosynthesis and cellular respiration occur, respectively. He writes vividly about the crucial role that these organelles and their bacterial relatives play in the flow of energy and
matter through the biosphere. Foreshadowing later chapters, he explains that cyanobacteria are photosynthetic prokaryotes now known to be the closest relatives of the chloroplast. The reader senses that Archibald sees bioenergetics as a powerful force in evolution,
but he doesn’t fully develop this view here.
In the second chapter, Archibald makes a valiant attempt to summarize the history of molecular biology as it developed from the 1940s to the 1960s. His main point is to explain
that visionary scientists like Francis Crick, Linus Pauling, Margaret Dayhoff, and Emile
Zuckerkandl recognized that comparing sequences of subunits in proteins and nucleic acids could yield invaluable phylogenetic information. As we later learn, molecular evidence
was crucial for confirming the endosymbiont theory for chloroplasts and mitochondria.
Archibald then jumps back in time and gives a brief overview of symbiosis research in the
late nineteenth and early twentieth centuries. Here he relies (with attribution) largely on
Jan Sapp’s detailed monograph Evolution by Association (1994), as well as on the scientific
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literature. We learn that some biologists thought that symbiosis provided a more powerful
source of innovation for evolution than small heritable variations. Constantin Mereschkowsky in Russia, Paul Portier in France, and Ivan Wallin in the United States all suggested
that symbionts were key players in evolutionary change. Portier’s claims in the 1920s that
he had isolated mitochondria and cultured them, however, raised skepticism and discredited research in endosymbiosis. Further, the concept did not fit well within the framework
of the “evolutionary synthesis” as put forward in the 1940s and 1950s. Endosymbiosis was
largely ignored for decades.
The situation began to change in the late 1950s and early 1960s, however, when images
from the new technology of electron microscopy showed that chloroplasts and mitochondria appeared to contain DNA and even ribosomes. A few scientists began to reconsider
endosymbiosis, notably Lynn Margulis, who developed the idea into a provocative and encompassing hypothesis. We learn that Margulis was indeed the most prominent champion
of the endosymbiont hypothesis, but we also come to understand that she was not alone;
we are introduced to other early proponents including Hans Ris, Walter Plaut, FJR “Max”
Taylor, and Roger Stanier.
It’s instructive to learn (or be reminded) that even as the endosymbiont hypothesis gained
credibility in the 1970s, staunch opposition continued. A cadre of prominent biologists
adhered to the view that mitochondria and chloroplasts arose endogenously within the
cytoplasm, and had never been free-living organisms. Archibald gives an exciting account
of how molecular data came to settle the issue once and for all, first for chloroplasts and
later for mitochondria.
Archibald covers the well-known work of Carl Woese who pioneered the use of ribosomal RNA (rRNA) as a probe of phylogenetic relationships. Initially, Woese and colleagues
chopped samples of rRNA into pieces with an enzyme and then displayed the fragments on
a gel. As Woese predicted, the pattern of fragments proved to be characteristic for different
groups of organisms. Distinguishing prokaryotic from eukaryotic rRNA turned out to be
easy. Once complete rRNA sequences were available, it became possible to build universal
phylogenetic trees, yielding the famous “Three Domain” model (now under serious challenge: see, for example, Williams and Embley 2014).
Comparing rRNA fragment patterns yielded exciting results even before complete sequences were available. In 1975, researchers found that chloroplast rRNA is of the prokaryote
type and very different from cytoplasmic rRNA. A year later, researchers found that rRNA
from cyanobacteria and from chloroplasts are highly homologous. By 1980, there was no
longer any doubt that chloroplasts evolved from endosymbiotic cyanobacterial ancestors.
Within a few more years, it was shown that mitochondria derive from the alpha-proteobacterial group of bacteria. It was finally clear that endosymbiosis has been a key process in
the evolution of the eukaryotic cell.
At a few points, Archibald brings in the human side of scientific research. It’s delightful to
read that in 1978, for example, when the first complete sequence of small subunit rRNA
was published, W Ford Doolittle read the entire list of 1542 nucleotides over the phone to
Woese, whose copy of the journal had not yet arrived in the mail.
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Archibald devotes a full chapter to endosymbiosis and the evolution of photosynthetic organisms. We learn that free-living cyanobacteria, a diverse and widely-distributed group,
account for 20–30% of the photosynthetic output on the planet and, as chloroplasts in algae
and plants, they essentially account for the rest as well. Molecular data has shown that
chloroplasts in the three main lineages of algae are very closely related, suggesting that
the chloroplast evolved only once. At the same time, it is fascinating to learn that some
eukaryotes have acquired chloroplasts, not by ingesting cyanobacteria, but by ingesting
other eukaryotes that already contained chloroplasts, a process called secondary symbiosis. It is now clear that the capacity for photosynthesis has been spread widely across the
eukaryotic tree through secondary symbiosis. (This section of the book could have been
called “One Plus N Equals One.”) One of the few relevant topics not covered in this book
is research on cytoplasmic inheritance by researchers such as Ruth Sager, who studied the
genetics of the chloroplast in green algae in the 1950s and 1960s. It would be interesting
to know how much this research area contributed to the revival and acceptance of the endosymbiont theory.
Once the bacterial nature of mitochondria and chloroplasts was understood, researchers
began to dig even deeper into eukaryotic evolution. What kind of cell incorporated the ancestral mitochondria? Was it another type of prokaryote or some kind of proto-eukaryote?
Why and how did that symbiotic relationship get started? How do symbionts become fully
integrated into the host cell? These questions have not been easy to answer and are still under active investigation. Archibald recounts the rise and fall of the once promising “archezoan hypothesis,” proposed in the 1980s by Thomas Cavalier-Smith, a scientist famous for
his long, complex, and provocative papers on cellular evolution. If a relatively complex cell
ingested the mitochondrial ancestor, Cavalier-Smith reasoned, then eukaryotic descendants
of that cell, still lacking mitochondria, could still exist. He called these hypothetical cells
“archezoa” and identified protozoa that looked like good candidates. Ultimately, however, it
was found that the candidate organisms were not closely related to one another and that, in
fact, they contain remnants of mitochondria. As Archibald puts it, “The archezoa hypothesis is dead” (page 105), but he also explains that testing it was fruitful in unexpected ways.
Archibald’s account makes clear that evolutionary change has proceeded not only by the
divergence of lineages but also by the unification and integration of genetically distinct
organisms. Thus the research it describes contributes to a more comprehensive picture of
evolution than is obtained by looking exclusively at multicellular organisms. Packed with
information, his book is not easy for a non-specialist to read, but it is enjoyable and rewarding. It would be most useful to readers with reasonably strong science backgrounds
who want to learn about the origins of the endosymbiont theory and understand where
it stands today. However, One Plus One Equals One will leave any reader with a good understanding of the profound role that endosymbiosis has played in evolution and with a
deeper appreciation of the prokaryotic ancestry of all eukaryotic cells, including our own.
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References
Knoll AH, Javaux EJ, Hewitt D, Cohen P. 2006. Eukaryotic organisms in Proterozoic oceans. Philosophical Transactions of the Royal Society B: Biological Sciences 361:1023–1038.
Sapp J. 2004. Evolution by Association: A History of Symbiosis. New York: Oxford University Press.
Williams TA, Embley TM. 2014. Archaeal “dark matter” and the origin of eukaryotes. Genome Biology and Evolution 6(3):474–481.
About th e author
Susan Spath was on the staff of NCSE from 2004 to 2009 and has a PhD in the history of science.
Author’s address
Susan Spath
c/o NCSE
PO Box 9477
Berkeley CA 94709-0477
[email protected]
Copyright 2015 by Susan Spath; licensed under a Creative Commons Attribution-Non-CommercialNoDerivs 3.0 Unported License. http://creativecommons.org/licenses/by-nc-nd/3.0/
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