The Effect of Oxygen on Biochemical Networks and the Evolution of Complex Life

Raymond, Jason; Segrè, Daniel

doi:10.1126/science.1118439

Cited by 440 publications

(371 citation statements)

References 16 publications

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“…Two derived energy-linked subnetworks stand out in the list, oxygenic mitochondrial ATP synthesis (NRG 00193) and oxygenic photosynthesis (NRG 00195), suggesting these important functions appeared late in evolution, well after discovery of most enzymatic activities. This is consistent with molecular and geological records that suggest life achieved considerable complexity before the appearance of oxygen in the atmosphere, and with enzyme distribution in aerobic pathways that suggests adaptation to oxygen occurred after major prokaryotic divergences in the tree of life (21). Subnetworks with many ancient folds belonging to the remaining mesonetworks, amino acid metabolism (AAC), carbohydrate metabolism (CAR), lipid metabolism (LIP) and nucleotide metabolism (NUC), were clearly ancestral and part of the early enzymatic burst.…”

Section: Most Enzymatic Functions Were Discovered At the Start Of Thesupporting

confidence: 71%

The origin of modern metabolic networks inferred from phylogenomic analysis of protein architecture

Caetano‐Anollés¹,

Kim²,

Mittenthal

2007

Proc. Natl. Acad. Sci. U.S.A.

157

171

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Metabolism represents a complex collection of enzymatic reactions and transport processes that convert metabolites into molecules capable of supporting cellular life. Here we explore the origins and evolution of modern metabolism. Using phylogenomic information linked to the structure of metabolic enzymes, we sort out recruitment processes and discover that most enzymatic activities were associated with the nine most ancient and widely distributed protein fold architectures. An analysis of newly discovered functions showed enzymatic diversification occurred early, during the onset of the modern protein world. Most importantly, phylogenetic reconstruction exercises and other evidence suggest strongly that metabolism originated in enzymes with the P-loop hydrolase fold in nucleotide metabolism, probably in pathways linked to the purine metabolic subnetwork. Consequently, the first enzymatic takeover of an ancient biochemistry or prebiotic chemistry was related to the synthesis of nucleotides for the RNA world.enzyme activity ͉ evolution ͉ metabolism ͉ nucleotide metabolism T here is current interest in the processes underlying the biology of network because these offer insight into the organization and evolution of life (1). Cellular metabolism, one of the greatest achievements of science, is clearly the best-studied biological network. It represents a complex collection of enzymatic reactions and transport processes that convert metabolites into molecules capable of supporting cells and organisms. However, our knowledge of how modern metabolism originated and evolved is limited (2). One widely accepted hypothesis is that promiscuous catalytic activities in proteins provide a selective advantage and are recruited to perform new metabolic functions (3, 4). Considerable evidence supports a patchwork recruitment scenario in which recruited homologous enzymes are scattered over diverse pathways (2). For example, enzymes with ␣/␤ barrel fold structure that catalyze similar reactions occur across metabolic subnetworks (5, 6) and a small set of structural families dominates the small-molecule metabolism in Escherichia coli (7-10). The recruitment hypothesis assumes there is already an active enzymatic core with multifunctional enzymes from which proteins are drawn for metabolic innovation. Because history restricts the interplay between structure and function of metabolic enzymes, we here use evolutionary patterns in protein structure advantageously to study recruitment processes and metabolic network evolution.The protein world has a hierarchical and redundant organization specified in terms of evolutionary units of molecular structure, the protein domains (11). Domains are generally unified into a comparatively small set of folding architectures, protein superfamilies, and these are further grouped into protein folds (12). Domain structure is generally maintained for long periods of evolutionary time. Consequently, the discovery of an architectural design constitutes an important and rare event in evolutionary history....

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Section: Most Enzymatic Functions Were Discovered At the Start Of Thesupporting

confidence: 71%

The origin of modern metabolic networks inferred from phylogenomic analysis of protein architecture

Caetano‐Anollés¹,

Kim²,

Mittenthal

2007

Proc. Natl. Acad. Sci. U.S.A.

157

171

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“…Many of the microbes have experienced high levels of oxygen relative to their ancestors for several million years, such that the differences we report are a conservative estimate of the extent to which oxygen may have historically limited proteome composition. This work adds to a growing body of literature connecting atmospheric oxygen levels with macroevolutionary changes, most recently with complexity in metabolic networks 28 and cell types 29 . In order to understand the broad role of oxygen levels in major transitions, further investigation and cooperation between the fields of palaeoclimatology, evolutionary biology and bioinformatics are necessary.…”

Section: Discussionmentioning

confidence: 99%

Oxygen content of transmembrane proteins over macroevolutionary time scales

Acquisti

Kleffe

Collins

2006

Nature

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We observe that the time of appearance of cellular compartmentalization correlates with atmospheric oxygen concentration. To explore this correlation, we predict and characterize the topology of all transmembrane proteins in 19 taxa and correlate differences in topology with historical atmospheric oxygen concentrations. Here we show that transmembrane proteins, individually and as a group, were probably selectively excluding oxygen in ancient ancestral taxa, and that this constraint decreased over time when atmospheric oxygen levels rose. As this constraint decreased, the size and number of communication-related transmembrane proteins increased. We suggest the hypothesis that atmospheric oxygen concentrations affected the timing of the evolution of cellular compartmentalization by constraining the size of domains necessary for communication across membranes.One of the major transitions in macroevolution was the appearance of eukaryotic cells between 2.1 and 1.8 billion years ago [1][2][3] . Cellular compartmentalization by membranes that are impermeable to large or charged molecules requires transport and communication across intracellular membranes. Eukaryotes devote more proteins to roles in communication than prokaryotes; this innovation involved a shift in the dominant secondary structures of transmembrane proteins 4 . Protein secondary structure is largely determined by hydrophobicity 5 , where oxygen and nitrogen are vital to forming hydrophilic residues. Transmembrane protein topology is further influenced by charge, where positively charged amino acids are more prevalent in cytoplasmic domains and negatively charged amino acids are more prevalent in extracellular domains [6][7][8] . This implies that changes in protein atomic composition may occur in parallel with changes in protein function. Traditionally, functional changes were thought to be associated with changes in amino acid sequence 9 , but an alternative approach is to consider proteins at the atomic level. This may be appropriate when large fluctuations in the elemental components of proteins occur through changes in absolute abundance, relative abundance, or form. In this case, nutritional constraints, metabolic optimization and chemical properties such as redox state may have important roles in protein evolution.The atomic content of biomolecules has a role in evolution Several examples of stoichiometric constraints on evolutionary and ecological outcomes have been reported recently. For example, variation in the atomic content of proteins in cyanobacterial lightharvesting proteins and microbial sulphur assimilatory enzymes correlates with nutrient availability 10,11 . Similarly, the carbon content of proteomes differs between species and correlates with genomic G1C content, which may reflect carbon availability in natural habitats 12 . The nitrogen content of proteins is lower in plants than in animals and is related to gene expression levels in plants 13 . These studies indicate that physiology, proteomes and genomes may bear detectable eco...

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“…In particular, the study by Raymond and Segrè 38 found that aerobic bacteria have approximately a 1.5 fold increase in the number of reactions and metabolites relative to anaerobic bacteria, resulting in the expansion of metabolic networks evolving in the presence of oxygen, and thus supporting the view of oxygen induced network complexity.…”

Section: Aerobicmentioning

confidence: 82%

Network motif frequency vectors reveal evolving metabolic network organisation

2015

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At the systems level many organisms of interest may be described by their patterns of interaction, and as such, are perhaps best characterised via network or graph models. Metabolic networks, in particular, are fundamental to the proper functioning of many important biological processes, and thus, have been widely studied over the past decade or so. Such investigations have revealed a number of shared topological features, such as a short characteristic path-length, large clustering coefficient and hierarchical modular structure. However, the extent to which evolutionary and functional properties of metabolism manifest via this underlying network architecture remains unclear. In this paper, we employ a novel graph embedding technique, based upon low-order network motifs, to compare metabolic network structure for 383 bacterial species categorised according to a number of biological features. In particular, we introduce a new global significance score which enables us to quantify important evolutionary relationships that exist between organisms and their physical environments. Using this new approach, we demonstrate a number of significant correlations between environmental factors, such as growth conditions and habitat variability, and network motif structure, providing evidence that organism adaptability leads to increased complexities in the resultant metabolic networks.

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The Effect of Oxygen on Biochemical Networks and the Evolution of Complex Life

Cited by 440 publications

References 16 publications

The origin of modern metabolic networks inferred from phylogenomic analysis of protein architecture

The origin of modern metabolic networks inferred from phylogenomic analysis of protein architecture

Oxygen content of transmembrane proteins over macroevolutionary time scales

Network motif frequency vectors reveal evolving metabolic network organisation

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