Perspectives

MICROBIOLOGY:

Autotrophs are organisms that can grow using carbon dioxide (CO₂) as their sole source of carbon. Among them are plants, algae, cyanobacteria, purple and green bacteria, and also some bacteria and archaea that do not obtain energy from light. Autotrophs generate the biomass on which all other organisms--including humans--thrive. They also play an important role in Earth's nitrogen and sulfur cycles. Four mechanisms are known by which autotrophic organisms fix carbon (see the figure). On page 1782 of this issue, Berg et al. (1) describe a fifth autotrophic CO₂ fixation pathway in archaea that may have been used by some of the earliest organisms on Earth.

In 1966, Evans et al. proposed that the green sulfur bacterium Chlorobium uses a second cycle for autotrophic CO₂ fixation (4). It took until 1990 until all the details of this reductive citric acid cycle were worked out (5). The cycle also operates in several other groups of bacteria and archaea. Because it involves enzymes that are sensitive to oxygen, this cycle is only found in anaerobes or in organisms that tolerate oxygen only at levels below those found in air (microaerophiles). At the beginning of the 1980s, a third pathway of autotrophic CO₂ fixation was found in certain Gram-positive bacteria and methane-forming archaea. In these organisms, one CO₂ molecule is reduced to CO and one to methanol (bound to a carrier); subsequently, acetyl-coenzyme A (CoA) is synthesized from CO and methanol (6). This reductive acetyl-CoA pathway is also found in several other bacteria and archaea. It involves one of the most oxygen-sensitive enzymes known and is thus only found in strict anaerobes.

The fourth pathway was discovered in the green nonsulfur bacterium Chloroflexus. Here, CO₂ fixation starts with the carboxylation of acetyl-CoA; the CO₂ acceptor is then regenerated in a cyclic process, with 3-hydroxypropionate and malyl-CoA as characteristic intermediates (7). The 3-hydroxypropionate/malyl-CoA cycle appears to be restricted to Chloroflexus species. None of the enzymes involved in this cycle are inherently sensitive toward oxygen; one of them is sensitive to ultraviolet-A light, which, however, does not reach the ecological niches in which the green bacteria thrive.

The novel autotrophic CO₂ fixation pathway described by Berg et al. has some of the same intermediates as the 3-hydroxypropionate/malyl-CoA cycle. Succinyl-CoA is also formed from acetate and 2 CO₂ molecules via 3-hydroxypropionate. However, the enzymes involved appear not to be phylogenetically related, indicating convergent evolution. From succinyl-CoA on, the two pathways are different.

Berg et al. show that the novel cycle is operative in Metallosphaera growing on H₂ and O₂ as the energy source. The genes for this cycle are also present in other archaea. All these organisms are either microaerophiles or, as in the case of Archaeoglobus, strict anaerobes. The cycle involves 4-hydroxybutyryl-CoA dehydratase, a radical enzyme sensitive to oxygen (8).

Why do different autotrophs use different pathways of CO₂ fixation? According to one hypothesis, the first organisms on Earth were strict anaerobes and autotrophs that used a reductive acetyl-CoA pathway very similar to that found today in some strictly anaerobic archaea and bacteria (9, 10). After the emergence of oxygenic photosynthesis, the atmospheric oxygen concentration increased slowly and the reductive acetyl-CoA pathway could no longer operate in most organisms due to the extreme oxygen sensitivity of one of its key enzymes. Autotrophy thus had to be reinvented after the major phyla had already evolved, leading to different pathways of autotrophic CO₂ fixation in different organisms dependent on their genetic outfit and living conditions.

Lateral gene transfer helped to spread the new inventions. Some were lost again. The reductive citric acid cycle and the 3-hydroxypropionate/4-hydroxybutyrate cycle could only survive in organisms that live under anaerobic or microaerophilic conditions due to the inherent oxygen sensitivity of the enzymes involved. Only the Calvin cycle made it into the aerobic world of plants, one reason being that it does not use enzymes that are inactivated by O₂ or by light.

References

1. I. A. Berg et al., Science 318, 1782 (2007).
2. M. Calvin, Nature 192, 799 (1961).
3. RuBisCO stands for ribulose-1,5-bisphosphate carboxylase-oxygenase.
4. M. C. W. Evans, B. B. Buchanan, D. I. Arnon, Proc. Natl. Acad. Sci. U.S.A. 55, 928 (1966).
5. B. B. Buchanan, D. I. Arnon, Photosynth. Res. 24, 47 (1990).
6. S. W. Ragsdale, Crit. Rev. Biochem. Mol. Biol. 26, 261 (1991).
7. S. Herter et al., J. Biol. Chem. 277, 20277 (2002).
8. B. M. Martin et al., Proc. Natl. Acad. Sci. U.S.A. 44, 15645 (2004).
9. G. Wächtershäuser, Chem. Biodivers. 4, 584 (2007).
10. W. Martin, M. J. Russel, Philos. Trans. R. Soc. B 362, 1887 (2007).

10.1126/science.1152209