Ecological Aspects of the Distribution of Different Autotrophic CO ₂ Fixation Pathways

Abstract

Autotrophic CO 2 fixation represents the most important biosynthetic process in biology. Besides the wellknown Calvin-Benson cycle, five other totally different autotrophic mechanisms are known today. This minireview discusses the factors determining their distribution. As will be made clear, the observed diversity reflects the variety of the organisms and the ecological niches existing in nature.Autotrophic CO 2 fixation represents the most important biosynthetic process in nature, being responsible for the net fixation of 7 ϫ 10 16 g carbon annually, corresponding to the conservation of 2.8 ϫ 1018 kJ of energy (107). The photosynthetic path of carbon in algae and plants was elucidated in the laboratory of Melvin Calvin in the 1940s and 1950s; the discovered reductive pentose phosphate (Calvin-Benson [CB]) cycle was immediately proposed to be the universal autotrophic carbon dioxide assimilation pathway, and the presence of its key enzyme, ribulose-1,5-bisphosphate carboxylase, was regarded as a synonym for autotrophy. This idea fit perfectly with the central biological dogma of that time, the biochemical unity of life (74). However, already in 1966 the second autotrophic CO 2 fixation cycle (the reductive citric acid cycle) had been discovered in the laboratory of Daniel Arnon (33). Today, six autotrophic CO 2 fixation mechanisms are known, raising the question of why so many pathways are necessary. In this review, the factors determining their distribution are discussed. As will be made clear, the observed diversity reflects the variety of the organisms and the ecological niches existing in nature. First, the general aspects of autotrophic CO 2 fixation will be discussed; then the known pathways will be introduced in the order of their discovery, highlighting their main characteristic features; finally, the main factors determining their distribution will be summarized. For those interested in a more detailed discussion of different aspects of autotrophy, several highly valuable reviews published in the last few years can be recommended, covering the function, structure, and evolution of ribulose-1,5-bisphosphate carboxylase (7,(101)(102)(103)111) and carboxysomes (61, 126); the reductive acetyl coenzyme A (acetyl-CoA) pathway (25,78,80) and the reductive citric acid cycle (2); CO 2 fixation in Archaea (14) and in deep-sea vent chemoautotrophs (73); and autotrophy in various oceanic ecosystems (47). GENERAL ASPECTS OF AUTOTROPHIC CO 2 FIXATIONIn general terms, the assimilation of CO 2 (oxidation state of ϩ4) into cellular carbon (average oxidation state of 0, as in carbohydrates) requires four reducing equivalents. An input of energy is also required for the reductive conversion of CO 2 to cell carbon and is provided by ATP hydrolysis. Anaerobes often use low-potential electron donors like reduced ferredoxin for CO 2 fixation, whereas aerobes usually rely on NAD(P)H as a reductant. Since reduced ferredoxin bears more energy than NADPH (ferredoxin, E 0 Ј Ϸ Ϫ400 mV; NADPH, E 0 Ј ϭ Ϫ320 mV), aerobic pathways usu...

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