The Impact of Oxygen on Metabolic Evolution: A Chemoinformatic Investigation

Ying, Jiang; Kong, De-Xin; Qin, Tao; Li, Xiao; Caetano‐Anollés, Gustavo; Zhang, Hong Yu

doi:10.1371/journal.pcbi.1002426

Cited by 25 publications

(29 citation statements)

References 39 publications

Supporting

Mentioning

Contrasting

Unclassified

Order By: Relevance

“…In contrast, FFs are generally unambiguously linked to molecular functions and are more powerful in their ability to uncover the history of early biochemistry [17]. This power has been made evident in the study of the most ancient proteins [18], the rise of translation [19], the protein repertoire of the last universal common ancestor [9], the first amino acid biosynthetic pathways and the origin of aerobic metabolism and planet oxygenation [20], [21]. We therefore assigned ages to the FF domains of the purine metabolic subnetwork using phylogenomic trees reconstructed from an analysis of domain abundance in the proteomes of 989 organisms that have been completely sequenced (A989) [20] and a subset of 420 that are free-living (FL420) [19].…”

Section: Resultsmentioning

confidence: 99%

Structural Phylogenomics Reveals Gradual Evolutionary Replacement of Abiotic Chemistries by Protein Enzymes in Purine Metabolism

Caetano-Anollés

Caetano‐Anollés

2013

PLoS ONE

Self Cite

View full text Add to dashboard Cite

The origin of metabolism has been linked to abiotic chemistries that existed in our planet at the beginning of life. While plausible chemical pathways have been proposed, including the synthesis of nucleobases, ribose and ribonucleotides, the cooption of these reactions by modern enzymes remains shrouded in mystery. Here we study the emergence of purine metabolism. The ages of protein domains derived from a census of fold family structure in hundreds of genomes were mapped onto enzymes in metabolic diagrams. We find that the origin of the nucleotide interconversion pathway benefited most parsimoniously from the prebiotic formation of adenine nucleosides. In turn, pathways of nucleotide biosynthesis, catabolism and salvage originated ∼300 million years later by concerted enzymatic recruitments and gradual replacement of abiotic chemistries. Remarkably, this process led to the emergence of the fully enzymatic biosynthetic pathway ∼3 billion years ago, concurrently with the appearance of a functional ribosome. The simultaneous appearance of purine biosynthesis and the ribosome probably fulfilled the expanding matter-energy and processing needs of genomic information.

show abstract

Section: Resultsmentioning

confidence: 99%

Structural Phylogenomics Reveals Gradual Evolutionary Replacement of Abiotic Chemistries by Protein Enzymes in Purine Metabolism

Caetano-Anollés

Caetano‐Anollés

2013

PLoS ONE

Self Cite

View full text Add to dashboard Cite

show abstract

“…Discriminative oxic metabolites are reported to be secondary metabolites and hormones [19]. However, these metabolites are expected to appear to be characteristically observed in higher organisms, suggesting strongly biased evaluation.…”

Section: Introductionmentioning

confidence: 99%

Limited Influence of Oxygen on the Evolution of Chemical Diversity in Metabolic Networks

Takemoto

Yoshitake

2013

Metabolites

View full text Add to dashboard Cite

Oxygen is thought to promote species and biomolecule diversity. Previous studies have suggested that oxygen expands metabolic networks by acquiring metabolites with different chemical properties (higher hydrophobicity, for example). However, such conclusions are typically based on biased evaluation, and are therefore non-conclusive. Thus, we re-investigated the effect of oxygen on metabolic evolution using a phylogenetic comparative method and metadata analysis to reduce the bias as much as possible. Notably, we found no difference in metabolic network expansion between aerobes and anaerobes when evaluating phylogenetic relationships. Furthermore, we showed that previous studies have overestimated or underestimated the degrees of differences in the chemical properties (e.g., hydrophobicity) between oxic and anoxic metabolites in metabolic networks of unicellular organisms; however, such overestimation was not observed when considering the metabolic networks of multicellular organisms. These findings indicate that the contribution of oxygen to increased chemical diversity in metabolic networks is lower than previously thought; rather, phylogenetic signals and cell-cell communication result in increased chemical diversity. However, this conclusion does not contradict the effect of oxygen on metabolic evolution; instead, it provides a deeper understanding of how oxygen contributes to metabolic evolution despite several limitations in data analysis methods.

show abstract

“…This cooperation might have resulted in the internalization of aerobic bacteria (the ancestors of mitochondria) by anaerobic archaea, resulting in the emergence of eukaryotes [212][213][214]. However, as mitochondria, subsequently, generated intracellular toxicity by producing intracellular ROS, this detoxification would have favored the biogenesis of new cellular compounds [215,216]. In this setting, biogenesis of sterols that requires oxygen-dependent enzymes could have first played a role in oxygen detoxification [216][217][218].…”

Section: From Molecular Innovations To Emergence Of New Properties Atmentioning

confidence: 99%

Physicochemical Foundations of Life that Direct Evolution: Chance and Natural Selection are not Evolutionary Driving Forces

Auboeuf

2020

Life

View full text Add to dashboard Cite

The current framework of evolutionary theory postulates that evolution relies on random mutations generating a diversity of phenotypes on which natural selection acts. This framework was established using a top-down approach as it originated from Darwinism, which is based on observations made of complex multicellular organisms and, then, modified to fit a DNA-centric view. In this article, it is argued that based on a bottom-up approach starting from the physicochemical properties of nucleic and amino acid polymers, we should reject the facts that (i) natural selection plays a dominant role in evolution and (ii) the probability of mutations is independent of the generated phenotype. It is shown that the adaptation of a phenotype to an environment does not correspond to organism fitness, but rather corresponds to maintaining the genome stability and integrity. In a stable environment, the phenotype maintains the stability of its originating genome and both (genome and phenotype) are reproduced identically. In an unstable environment (i.e., corresponding to variations in physicochemical parameters above a physiological range), the phenotype no longer maintains the stability of its originating genome, but instead influences its variations. Indeed, environment- and cellular-dependent physicochemical parameters define the probability of mutations in terms of frequency, nature, and location in a genome. Evolution is non-deterministic because it relies on probabilistic physicochemical rules, and evolution is driven by a bidirectional interplay between genome and phenotype in which the phenotype ensures the stability of its originating genome in a cellular and environmental physicochemical parameter-depending manner.

show abstract

The Impact of Oxygen on Metabolic Evolution: A Chemoinformatic Investigation

Cited by 25 publications

References 39 publications

Structural Phylogenomics Reveals Gradual Evolutionary Replacement of Abiotic Chemistries by Protein Enzymes in Purine Metabolism

Structural Phylogenomics Reveals Gradual Evolutionary Replacement of Abiotic Chemistries by Protein Enzymes in Purine Metabolism

Limited Influence of Oxygen on the Evolution of Chemical Diversity in Metabolic Networks

Physicochemical Foundations of Life that Direct Evolution: Chance and Natural Selection are not Evolutionary Driving Forces

Contact Info

Product

Resources

About