Cooperation and Competition in the Evolution of ATP-Producing Pathways

Heterotrophic organisms generally face a trade-off between rate and yield of adenosine triphosphate (ATP) production. This trade-off may result in an evolutionary dilemma, because cells with a higher rate but lower yield of ATP production may gain a selective advantage when competing for shared energy resources. Using an analysis of model simulations and biochemical observations, we show that ATP production with a low rate and high yield can be viewed as a form of cooperative resource use and may evolve in spatially structured environments. Furthermore, we argue that the high ATP yield of respiration may have facilitated the evolutionary transition from unicellular to undifferentiated multicellular organisms.

[1]  H G Crabtree,et al.  Observations on the carbohydrate metabolism of tumours. , 1929, The Biochemical journal.

[2]  O. Warburg [Origin of cancer cells]. , 1956, Oncologia.

[3]  T. Bauchop,et al.  The growth of micro-organisms in relation to their energy supply. , 1960, Journal of general microbiology.

[4]  T. Ohnishi,et al.  Preparation and some properties of yeast mitochondria. , 1966, The Journal of biological chemistry.

[5]  G. Hardin,et al.  The Tragedy of the Commons , 1968, Green Planet Blues.

[6]  G. Kraepelin,et al.  Factors affecting dimorphism in Mycotypha (Mucorales): a correlation with the fermentation-respiration equilibrium. , 1974, Journal of general microbiology.

[7]  G. Clark-Walker,et al.  Effects of Oxygen and Glucose on Energy Metabolism and Dimorphism of Mucor genevensis Grown in Continuous Culture: Reversibility of Yeast-Mycelium Conversion , 1974, Journal of bacteriology.

[8]  C. Inderlied,et al.  Glucose metabolism and dimorphism in Mucor , 1978, Journal of bacteriology.

[9]  J. Stucki The optimal efficiency and the economic degrees of coupling of oxidative phosphorylation. , 1980, European journal of biochemistry.

[10]  L. Chao,et al.  Structured habitats and the evolution of anticompetitor toxins in bacteria. , 1981, Proceedings of the National Academy of Sciences of the United States of America.

[11]  T. Swain,et al.  Symbiosis in Cell Evolution: by L. Margulis. W. H. Freeman, San Francisco, 1981. xix + 419 pp. , 1983 .

[12]  A. Lehninger,et al.  The upper and lower limits of the mechanistic stoichiometry of mitochondrial oxidative phosphorylation. Stoichiometry of oxidative phosphorylation. , 1986, European journal of biochemistry.

[13]  W. A. Scheffers,et al.  Enzymic analysis of the crabtree effect in glucose-limited chemostat cultures of Saccharomyces cerevisiae , 1989, Applied and environmental microbiology.

[14]  A. Fiechter,et al.  Metabolic control of glucose degradation in yeast and tumor cells. , 1989, Advances in biochemical engineering/biotechnology.

[15]  D. L. Harris,et al.  Mechanistic stoichiometry of mitochondrial oxidative phosphorylation. , 1991, Biochemistry.

[16]  M. Nowak,et al.  Evolutionary games and spatial chaos , 1992, Nature.

[17]  B. Poolman,et al.  Energy transduction in lactic acid bacteria. , 1993, FEMS microbiology reviews.

[18]  R. Gennis,et al.  Energetic efficiency of Escherichia coli: effects of mutations in components of the aerobic respiratory chain , 1993, Journal of bacteriology.

[19]  O. Neijssel,et al.  The energetics of bacterial growth: a reassessment , 1994, Molecular microbiology.

[20]  M Rigoulet,et al.  Mechanistic stoichiometry of yeast mitochondrial oxidative phosphorylation. , 1994, Biochemistry.

[21]  R. Mitchell,et al.  P/O ratios reassessed: Mitochondrial P/O ratios consistently exceed 1.5 with succinate and 2.5 with NAD‐linked substrates , 1996, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[22]  R. Heinrich,et al.  The Regulation of Cellular Systems , 1996, Springer US.

[23]  Tibor Vellai,et al.  A New Aspect to the Origin and Evolution of Eukaryotes , 1998, Journal of Molecular Evolution.

[24]  Francisco Montero,et al.  Optimization of glycolysis: new discussions , 1999 .