Inn Sagan

J. Theoret. Biol. (1967) 14, 225-274

On the Origin of Mitosing C dls
L Y N N SAGAN

Department of Biology, Boston University
Boston, Massachusetts, U.S.A.
(Received 8 June 1966)
A theory of the origin of eukaryotic cells ("higher" cells which divide by
classical mitosis) is presented. By hypothesis, three fundamental organelles:
the mitochondria, the photosynthetic plastids and the (9+2) basalbodies
of flagella were themselves once free-living (prokaryotic) cells. The evolution of photosynthesis under the anaerobic conditions of the early atmosphere to form anaerobic bacteria, photosynthetic bacteria and eventually
blue-green algae (and protoplastids) is described. The subsequent evolution
of aerobic metabolism in prokaryotes to form aerobic bacteria (protoflagella andprotomitochondria) presumably occurred during the transition
to the oxidizing atmosphere. Classical mitosis evolved in protozoan-type
cells millions of years after the evolution of photosynthesis. A plausible
scheme for the origin of classical mitosis in primitive amoeboflagellates is
presented. During the course of the evolution of mitosis, photosynthetic
plastids (themselves derived from prokaryotes) weresymbiotically
acquired by some of these protozoans to form the eukaryotie algae and the
green plants.
The cytological, biochemical and paleontological evidence for this theory
is presented, along with suggestions for further possible experimental
verification. The implications of this scheme for the systematics of the
lower organisms is discussed.
1. Introduction
A ll free-living organisms are cells orare made of cells. There are two basic cell
types: prokaryotic a nd eukaryotic. P rokaryotic cells include the eubacteria,
the blue-green algae, the gliding bacteria, the budding bacteria, the pleuropneumonia-like organisms, the spirochaetes and rickettsias, etc. Eukaryotic
cells, of course, are the familiar components of plants and animals, molds and
protozoans, and all other "higher" organisms.They contain subcellular
organelles such as mitochondria and membrane-bounded nuclei and have
many other features in common.
"The numerous and fundamental differences between the eukaryotic and
prokaryotic cell which have been described in this chapter have been
fully recognized only in the past few years. In fact, this basic divergence
in cellular structure which separates the bacteria andblue-green algae
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L. SAGAN
from all other cellular organisms, probably represents the greatest single
evolutionary discontinuity to be found in the present-day living world"
(Stanier, Douderoff & Adelberg, 1963).

This paper presents a theory of the origin of this discontinuity between
eukaryotic (mitosing or "higher") and prokaryotic cells. Specifically, the
mitochondria, the (9 +2) basal bodies of the flagella, and the photosynthetic
plastids can all be considered to have derived from free-living cells, and the
eukaryotic cell is the result of the evolution of ancient symbioses. Although
these ideas are not new [Merechowsky (1910) & Minchin (1915)in Wilson
(1925), WaUin (1927), Lederberg (1952), Haldane (1954), Ris & Plaut (1962)], t
in this paper they have beensynthesized in such a way as to be consistent with
recent data on the biochemistry and cytology of subcellular organeUes. In
accord with both the fossil record and this theory, the lower eukaryotes
(protozoans, eukaryotic algae and fungi) can now be included on a single
phylogenetic tree (Fig. 1). In contrast to previous thought on the subject
(Cronquist, 1960; Dougherty & Allen, 1960; Fritsch, 1935), manyaspects of
this theory are verifiable by modern techniques of molecular biology.
In defending the idea that the eukaryotic cell arose by a specific series of
endosymbioses, a plausible scheme for the origin of mitosis itself emerges.
("Mitosis" is meant only in the classical sense; the analogous equal distribution of genes to daughter cells in prokaryotes is not relevant here.)
The paper is...