Oxygen and hydrogen peroxide in the early evolution of life on earth: in silico comparative analysis of biochemical pathways

Abstract

In the Universe, oxygen is the third most widespread element, while on Earth it is the most abundant one. Moreover, oxygen is a major constituent of all biopolymers fundamental to living organisms. Besides O(2), reactive oxygen species (ROS), among them hydrogen peroxide (H(2)O(2)), are also important reactants in the present aerobic metabolism. According to a widely accepted hypothesis, aerobic metabolism and many other reactions/pathways involving O(2) appeared after the evolution of oxygenic photosynthesis. In this study, the hypothesis was formulated that the Last Universal Common Ancestor (LUCA) was at least able to tolerate O(2) and detoxify ROS in a primordial environment. A comparative analysis was carried out of a number of the O(2)-and H(2)O(2)-involving metabolic reactions that occur in strict anaerobes, facultative anaerobes, and aerobes. The results indicate that the most likely LUCA possessed O(2)-and H(2)O(2)-involving pathways, mainly reactions to remove ROS, and had, at least in part, the components of aerobic respiration. Based on this, the presence of a low, but significant, quantity of H(2)O(2) and O(2) should be taken into account in theoretical models of the early Archean atmosphere and oceans and the evolution of life. It is suggested that the early metabolism involving O(2)/H(2)O(2) was a key adaptation of LUCA to already existing weakly oxic zones in Earth's primordial environment.

FIG. 1.

Two schemes (a, b) of searching algorithms in which BioCyc (http://biocyc.org) was used as the primary database. ^aSecondary databases: AraCyc (www.arabidopsis.org/biocyc/index.jsp), CalbiCyc (http://pathway.candidagenome.org/), DictyCyc (http://dictybase.org/Dicty_Info/dictycyc_info.html), FungiCyc (http://fungicyc.broadinstitute.org:1555/), MedicCyc (http://mediccyc.noble.org/), MouseCyc (http://mousecyc.jax.org/), RiceCyc (http://www.gramene.org/pathway/), SolCyc (http://solcyc.solgenomics.net/), Yeast Biochemical Pathways (http://pathway.yeastgenome.org/biocyc/). ^bExcluding the following compounds, which are extremely common in all organisms: H₂O, H⁺, ATP, ADP, AMP, phosphate, diphosphate, NAD⁺, NADH, NADP⁺, NADPH, an oxidized electron acceptor, a reduced electron acceptor.

FIG. 2.

Reactions involving O₂/H₂O₂. (a) the mean number of O₂-involving reactions, (b) the percent of O₂-involving reactions, (c) total mean number of H₂O₂-involving reactions, (d) the percent of H₂O₂-involving reactions. The values were calculated according to Eqs. 1 and 2 (Materials and Methods). Values represent means±SD; n=number of species, obligate anaerobes: n=40, facultative anaerobes: n=31, aerobes: n=34; see also Table 1. The same letters above bars indicate no significant differences between means, at least at the level of P<0.05 (Kruskal-Wallis test and Dunn's test as a post test).

FIG. 3.

Reactions involving O₂/H₂O₂ in organisms belonging to the three domains of life, Bacteria, Archaea, and Eukarya. (a), (b), (c), (d) description is the same as in Fig. 2. The values were calculated according to Eqs. 1 and 2 (Materials and Methods). Values represent means±SD; n=number of species, obligate anaerobes: n=27 (Bacteria), n=13 (Archaea), facultative anaerobes: n=24 (Bacteria), n=3 (Archaea), n=4 (Eukarya), aerobes: n=15 (Bacteria), n=3 (Archaea), n=16 (Eukarya) The same letters above bars indicate no significant differences between means, at least at the level of P<0.05 (Kruskal-Wallis test and Dunn's test as a post test).

FIG. 4.

Reactions involving O₂/H₂O₂ in organisms performing anoxygenic photosynthesis (Bacteria), oxygenic photosynthesis (cyanobacteria and plants), and in nonphotosynthesizing organisms (animals and fungi). (a), (b), (c), (d) description is the same as in Fig. 2; o. an—obligate anaerobes, f. an—facultative anaerobes. The values were calculated according to Eqs. 1 and 2 (Materials and Methods). Values represent means±SD; n=number of species, obligate anaerobes: n=3 (Bacteria), facultative anaerobes: n=3 (Bacteria), aerobes: n=6 (cyanobacteria), n=9 (plants), n=7 (animals and fungi). The same letters above bars indicate no significant differences between means, at least at the level of P<0.05 (Kruskal-Wallis test and Dunn's test as a post test).

FIG. 5.

The presence of reactions/pathways representative of aerobes in obligate anaerobes and facultative anaerobes. (a) the percentage of organisms performing aerobic respiration, (b) the percentage of organisms performing ROS removal reactions, (c) the percentage of organisms where both aerobic respiration and ROS removal reactions are present. The values were calculated according to Eq. 7 (Materials and Methods). The dashed lines represent a reference value for aerobes=100%; n=number of species, n=40 (obligate anaerobes), n=31 (facultative anaerobes).