Physiology, phylogeny, early evolution, and GAPDH
Physiology, phylogeny, early evolution, and GAPDH
William F. Martin 0 1 2
Rüdiger Cerff 0 1 2
Handling Editor: Uli Kutschera
0 Institute of Molecular Evolution, University of Düsseldorf , Universitätsstr. 1, 40225 Düsseldorf , Germany
1 Institute of Genetics, Technical University of Braunschweig , Spielmannstr. 7, 38106 Braunschweig , Germany
2 Physiology , phylogeny, early evolution, and GAPDH
The chloroplast and cytosol of plant cells harbor a number of parallel biochemical reactions germane to the Calvin cycle and glycolysis, respectively. These reactions are catalyzed by nuclear encoded, compartment-specific isoenzymes that differ in their physiochemical properties. The chloroplast cytosol isoenzymes of D-glyceraldehyde-3-phosphate dehydrogenase (GAPDH) harbor evidence of major events in the history of life: the origin of the first genes, the bacterial-archaeal split, the origin of eukaryotes, the evolution of protein compartmentation during eukaryote evolution, the origin of plastids, and the secondary endosymbiosis among the algae with complex plastids. The reaction mechanism of GAPDH entails phosphorolysis of a thioester to yield an energy-rich acyl phosphate bond, a chemistry that points to primitive pathways of energy conservation that existed even before the origin of the first free-living cells. Here, we recount the main insights that chloroplast and cytosolic GAPDH provided into endosymbiosis and physiological evolution.
Endosymbiosis; Plastids; Mitochondria; Cell evolution; Peter Sitte
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Peter Sitte was a virtuoso in the art of electron microscopy. He
devoted his scientific career to understanding the nature and
evolutionary basis of compartmentation in eukaryotic cells
and the role that endosymbiosis played therein (Sitte 2007).
Thanks mainly to electron microscopic studies in the 1960s
and 1970s, scientists in 2016 recognize two kinds of cells: the
prokaryotic type and the eukaryotic type. The main difference
that distinguishes the two cell types is the nature of internal
compartmentation in eukaryotes. The chromosomes in
eukaryotic cells are separated from the cytoplasm by membrane
surrounding the cell nucleus, while chromosomes in
prokaryotes are freely dispersed throughout in the cytoplasm.
Eukaryotes typically possess a complex endomembrane
system, and mitochondria, plant, and algal cells possess
chloroplasts in addition. By the measure of compartmentation, the
most complex cells in nature are found among the algae that
possess plastids surrounded by three or four membranes,
plastids that are remnants of evolutionarily reduced eukaryotic
cells residing within the cytosol of another nucleus-bearing
cell (Stoebe and Maier 2002; Gould et al. 2008). Though it
was not always the case, today, biologists recognize that
complexity in eukaryotic cells stems from endosymbiosis
(Archibald 2014).
Endosymbiotic theory takes root in Mereschkowsky’s
classical essay on the origin of plastids (Mereschkowsky 1905). It
has a long and turbulent history, as recently summarized
elsewhere (Martin et al. 2015). The elder of us first learned about
endosymbiosis in the 1960s in Peter Sitte’s cell biology
lectures at the University of Freiburg. Endosymbiotic theory—
the prospect that mitochondria and chloroplasts descended
from free living prokaryotes that entered into a symbiotic
relationship with their respective host cell early in eukaryotic
history—was a very exciting, almost revolutionary, prospect
in cell evolution that opened up fundamentally new avenues
of pursuit to investigate and understand eukaryotic
intracellular compartmentation. One aspect in particular was important
for endosymbiotic theory: the compartmentation of
metabolism in eukaryotes. Early on, endosymbiotic theory had it that
the core metabolic functions of mitochondria (respiration) and
chloroplasts (photosynthesis) were direct inheritances from
the bacterial ancestors of organelles. It was also clear from
electron microscopy that organelles possessed DNA
(Kowallik and Haberkorn 1971), and that organelle genomes
were much too small to encode all of the proteins that
underpin respiration and photosynthesis (Herrmann et al. 1975). As
a consequence, most of the proteins that support the
physiological function of chloroplasts and mitochondria had to be
encoded in nuclear chromosomes, which meant that there had
to have been some form of gene transfer going on from
endosymbionts to the host, or as Wallin put it with regard to
mitochondria, B...bacterial organisms may develop an absolute
symbiosis with a higher organism and in some way or another
impress a new character on the factors of heredity. The
simplest and most readily conceivable mechanism by which the
alteration takes place would be the addition of new genes to
the chromosomes from the bacterial symbiont.^ (Wallin 1925;
p. 144).
Chloroplast cytosol isoenzymes provided unique
opportunities to test crucial predictions of endosymbiotic theory with
molecular evolutionary studies. I (...truncated)