Physiology, phylogeny, early evolution, and GAPDH

Protoplasma, Mar 2017

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.

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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 - 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)


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William F. Martin, Rüdiger Cerff. Physiology, phylogeny, early evolution, and GAPDH, Protoplasma, 2017, pp. 1-12, DOI: 10.1007/s00709-017-1095-y