R ubisco: still the most abundant protein of Earth?
2013; Wiley; Volume: 198; Issue: 1 Linguagem: Inglês
10.1111/nph.12197
ISSN1469-8137
Autores Tópico(s)Marine and coastal ecosystems
Resumo'How can leaf Rubisco N values for vascular plants best be compared with whole organism (whole cell) Rubisco protein values for cyanobacteria and algae?' Ellis (1979) suggested that Rubisco was the most globally abundant protein in land biota, based on the enzyme from C3 land plants. However, work on organisms with Rubiscos with different kinetics and CO2 supply mechanisms, specifically CO2 concentrating mechanisms (CCMs), suggests that less Rubisco is needed in some organisms to catalyse a given rate of CO2 assimilation. In this issue of New Phytologist, Losh et al. provide a very important data set which measures the Rubisco content in cultures of eight species of microalgae, and also in natural populations of marine phytoplankton. A very important finding is that the protein content of the algal cells, as a fraction of total cell protein, is only about a fifth of that in the leaves of C3 plants, and is the minimum Rubisco content needed to support the observed maximum growth rate of the algae. The highest values of Rubisco per unit nitrogen (N) among the flowering plants (Table 1) are found in C3 plants relying on diffusive entry of CO2 to Rubisco from the bulk atmosphere. All the other organisms listed have CCMs; for the terrestrial vascular plants these are all C4 plants, and they have lower Rubisco values on a leaf blade N basis (Table 1), based on the measurements on seven NADme (using NAD malic enzyme as the C4 decarboxylase) grasses, as well as for seven NADPme (using NADP malic enzyme as the C4 decarboxylase) grasses. There seem to be no comparable values for Rubisco N as a fraction of total leaf protein in plants with the PEPck (PEP carboxykians as the C4 decarboxylase) variants of C4 metabolism, or those with the other kind of CCM, that is, Crassulacean Acid Metabolism (CAM), although Niewiadomska et al. (2011) examined the CAM and C3 phenotypes of a facultative CAM plant and found that the CAM phenotype had a lower Rubisco content than did the C3 phenotype. The other category of oxygenic phototrophs with CCMs in Table 1 is that found in the cyanobacteria and microalgae. The values in Table 1 are Rubisco as a fraction of total protein in the cells. The very careful work of Losh et al. is all based on Rubisco protein as a fraction of total protein, and the values for nutrient-replete culture show much less variation than those cited in Raven (1991). Losh et al. also give values for phytoplankton from the marine environment; the values are near or below the values found for nutrient-replete cultures. How can the leaf Rubisco N as a fraction of the total leaf N values for the vascular plants in Table 1 best be compared with whole organism (whole cell) Rubisco protein as a fraction of total protein values for cyanobacteria and algae? Rubisco N on a leaf-blade-N basis is less than Rubisco N as a fraction of leaf protein N since some leaf N is in nucleic acids, free amino acids and other intermediary metabolites, and stored N; possibly outweighing this is the protein occurring in the rest of the plant where the fraction contributed to Rubisco is much less than in leaf blades. However, a more detailed analysis is needed before it can be concluded that the Rubisco N : leaf N ratios needs downward correction for comparison with the Rubisco : total organism protein ratios in Table 1. Returning to the global quantitative significance of Rubisco relative to other proteins, the lower fraction of Rubisco in algae and vascular plants with CCMs can be considered in relation to the contribution of these organisms to global primary productivity. The contributions of marine and continental primary productivity are given by Field et al. (1998) and Raven (2009). Essentially all of the marine planktonic net primary productivity (47.5 Pg C yr−1; Field et al., 1998) involved organisms with CCMs, and CCMs also occur in many of the organisms contributing to coastal benthic net primary productivity (c. 1 Pg C yr−1: Field et al., 1998). It is important to note that CCMs seem to be as prevalent in polar as in warmer waters (Tortell et al., 2006); even though the arguments as to the smaller, or absent, competitive advantage of CCMs at low temperatures used for terrestrial C4 plants (Long, 1999) also apply to marine primary producers (Raven et al., 2002). On land, Field et al. (1998) suggest a global net primary productivity of 56 Pg C yr−1; from global values for natural abundance stable C isotope discrimination, 21% of this is due to C4 plants (Lloyd & Farquhar, 1994). These values suggest that at least half of global primary productivity involves CCMs, and the organisms with CCMs have less Rubisco per unit biomass, and a smaller fraction of total protein allocated to Rubisco, than in C3 terrestrial plants. The values in Table 1 suggest that the organisms with CCMs have less than half of the Rubisco content of terrestrial C3 plants. The global quantity of Rubisco is, then, less than three quarters, and possibly less than five-eighths, of what would be the case if all primary producers using Rubisco had the quantity of Rubisco found in C3 terrestrial plants. The smaller quantity of Rubisco in photolithotrophs using CCMs is often reflected in a greater N use efficiency (NUE; rate of biomass gain per unit N in the organism), in C4 plants (Long, 1999), and predicted for algae with CCMs (Raven, 1991; Raven et al., 2012). This greater NUE means that the decreased content of Rubisco, and of the machinery used in the photorespiratory C oxidation cycle(s) in organisms with CCMs than in C3 terrestrial plants, is not quantitatively offset by the need for additional N in the catalysts and structures required by CCMs. Are there any other autotrophic CO2 assimilation pathways which could function in oxygenic photosynthetic organisms in the present atmosphere with a lower requirement for protein in the CO2 assimilation pathway per unit CO2 fixation rate than for Rubisco-based systems? Of the five well-characterized alternatives to Rubisco and the Benson–Calvin cycle, all have a lower running cost (mol ATP and mol NADPH per mol CO2 assimilated) than the Rubisco-based systems in the present atmosphere, but some are ruled out by irreversible inhibition by O2 or low inorganic C affinity (Raven, 2009; Bar-Even et al., 2012; Raven et al., 2012). However, lower energy inputs mean that the overall reaction sequence is closer to thermodynamic equilibrium, with a greater extent of back-reactions and so a requirement for enzyme protein than for a reaction sequence further from equilibrium (Bar-Even et al., 2012). Bar-Even et al. (2012) also point out that the enzymes with the lowest specific reaction sequence in the pathway are typically carboxylases, so non-Rubisco-based pathways can also have a high protein allocation to carboxylases. The most plausible alternative to the Rubisco-based systems is the 3-hydroxypropionate bi-cycle (Bar-Even et al., 2012), although even this pathway only represents a protein saving, for a given rate of CO2 assimilation, of 0.33 relative to a Rubisco-based system with the PCOC (Bar-Even et al., 2012) and a smaller factor for Rubisco-based systems with CCMs (Raven, 1991; Long, 1999). What now of the suggestion by Ellis (1979) that Rubisco is the commonest protein in the (terrestrial) world? The allocation of 20% of terrestrial primary productivity to C4 plants decreases the quantity of Rubisco on land to 85–90% of the value calculated by Ellis (1979); this would probably still allow Rubisco to be the most abundant protein on land, with actin (quantity unspecified) suggested by Ellis as the next most abundant protein. Even with the global quantity of Rubisco in the ocean suggested by the work of Losh et al., it could be the most abundant protein in marine biota.
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