The origin and evolution of modern metabolism

Caetano‐Anollés, Gustavo; Yafremava, Liudmila S.; Gee, Hannah; Caetano-Anollés, Derek; Kim, Hee Shin; Mittenthal, Jay E.

doi:10.1016/j.biocel.2008.08.022

Cited by 106 publications

(99 citation statements)

References 81 publications

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“…Cambialistic metal-binding protein architectures capable of binding multiple metals appeared earlier than metal-specific counterparts, and the trend from promiscuity to specificity in metal-binding parallels general patterns observed in evolution of modern metabolism (27). The hypothesis that a functional metal homeostasis system would be necessary for the first steps in akaryotic evolution has been argued using transitional arguments (3), and the concomitant appearances of structures involved in metal homeostasis, metal-specific architectures, and the diversification of the akaryotic lineages provides the first genomic evidence of this.…”

Section: Emergence Of the Akaryotes Metal Homeostasis And Biogeochementioning

confidence: 65%

History of biological metal utilization inferred through phylogenomic analysis of protein structures

Dupont

Butcher

Valas³

et al. 2010

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

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The fundamental chemistry of trace elements dictates the molecular speciation and reactivity both within cells and the environment at large. Using protein structure and comparative genomics, we elucidate several major influences this chemistry has had upon biology. All of life exhibits the same proteome size-dependent scaling for the number of metal-binding proteins within a proteome. This fundamental evolutionary constant shows that the selection of one element occurs at the exclusion of another, with the eschewal of Fe for Zn and Ca being a defining feature of eukaryotic proteomes. Early life lacked both the structures required to control intracellular metal concentrations and the metal-binding proteins that catalyze electron transport and redox transformations. The development of protein structures for metal homeostasis coincided with the emergence of metal-specific structures, which predominantly bound metals abundant in the Archean ocean. Potentially, this promoted the diversification of emerging lineages of Archaea and Bacteria through the establishment of biogeochemical cycles. In contrast, structures binding Cu and Zn evolved much later, providing further evidence that environmental availability influenced the selection of the elements. The late evolving Zn-binding proteins are fundamental to eukaryotic cellular biology, and Zn bioavailability may have been a limiting factor in eukaryotic evolution. The results presented here provide an evolutionary timeline based on genomic characteristics, and key hypotheses can be tested by alternative geochemical methods.Archean-Proterozoic | biogeochemistry | bioinorganic chemistry | evolution | metal homeostasis M etalloproteins contain one or more ions of an inorganic element in their 3D structure and are said to comprise 30% of all proteins (1). Many biological pathways contain at least one metalloenzyme (2) and consequently require Mg, K, Ca, Fe, Mn, and Zn to sustain life (3). Other elements, like Cu, Mo, Ni, Se, and Co, are required by many-though not all-organismal lineages, and the utilization of trace elements varies greatly between species (3). The different elements have a range of affinities for most coordinating environments in the order Mg +2 /Ca +2 < Mn +2 < Fe +2 < Co +2 < Ni +2 < Cu +2 ∼Zn +2 , an equilibrium series known as the Irving-Williams Series (4). This array of outer-sphere chemistry provides significant catalytic diversity, yet has consequences for both biological and environmental chemistry. Within the cell, metals compete for protein binding sites; hence, extensive protein networks involving transporters and metalsensing regulatory proteins are required to maintain the proper subcellular concentrations of each element, and in some cases directly shuttle each metal to its requisite metalloprotein in the proper cellular compartment (1, 5, 6). It has been hypothesized that the establishment of a metal homeostasis system is required for distinct phylotypes of cells to develop (7).Environmentally, for similar fundamental chemical reasons, the...

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Section: Emergence Of the Akaryotes Metal Homeostasis And Biogeochementioning

confidence: 65%

History of biological metal utilization inferred through phylogenomic analysis of protein structures

Dupont

Butcher

Valas³

et al. 2010

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

Self Cite

274

245

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“…With the appearance of complex catalysts (ribonucleic acid-or protein-based enzymes), these cycles gained complexity, and evolved in their effectiveness and robustness [1]. These metabolic pathways now form the basis for life.…”

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confidence: 99%

Regulatory crosstalk of the metabolic network

Grüning

Lehrach

Ralser

2010

Trends in Biochemical Sciences

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The metabolic network has a modular architecture, is robust to perturbations, and responds to biological stimuli and environmental conditions. Through monitoring by metabolite responsive macromolecules, metabolic pathways interact with the transcriptome and proteome. Whereas pathway interconnecting cofactors and substrates report on the overall state of the network, specialised intermediates measure the activity of individual functional units. Transitions in the network affect many of these regulatory metabolites, facilitating the parallel regulation of the timing and control of diverse biological processes. The metabolic network controls its own balance, chromatin structure and the biosynthesis of molecular cofactors; moreover, metabolic shifts are crucial in the response to oxidative stress and play a regulatory role in cancer.Evolution of the metabolic network and its structure Life probably began with the formation of compartmentalised autocatalytic chemical cycles. With the appearance of complex catalysts (ribonucleic acid-or protein-based enzymes), these cycles gained complexity, and evolved in their effectiveness and robustness [1]. These metabolic pathways now form the basis for life.As was the case for the first primitive life forms, the survival of today's complex organisms depends on the robustness and functionality of the metabolic framework [2]. To prevent and counteract perturbations in the flux, many biological control and sensor systems have evolved around the metabolic network. Metabolic pathways provide the cell with energy and supply macromolecular synthesis pathways with their required intermediates. They also balance metabolic systems under a variety of physiological conditions, and act as transducers and sensor systems for environmental conditions and stimuli. In addition, metabolic pathways are essential for crosstalk between metabolic regulatory components and the cellular transcriptome and proteome.As early as the 1960s, the principle that cells alter their gene expression in response to metabolic requirements has been known. The seminal work of Jacob and Monod, investigating the lac operon, uncovered one of the first examples of chemical-genetic regulation, by which bacterial cells adjust their enzyme production to the nutrient supply [3]. However, only recently have the broader implications of this principle emerged. Indeed, changes in the metabolic network not only control the metabolome, but they also have wide-ranging regulatory functions throughout biology.Most of the biochemical mechanisms that link the metabolic network to the transcriptome and proteome are incompletely understood. However, one type of regulation appears to be common: representative network intermediates bind to and modulate sensor function and activity of transcription factors, translational regulators, chromatin, enzymes, RNA molecules, and ion channels. Significant transcriptional changes around these intermediates identified them as reporter metabolites [4,5]. The use of intermediates as activity reporters ne...

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“…Biochemical pathway evolution has been examined extensively, particularly regarding mechanisms by which novel functions can be generated, diversified, and maintained (9,12). Best studied in this regard is the role of gene duplication followed by divergence, resulting in paralog families that, despite sharing a common evolutionary ancestor, possess different functions (10).…”

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confidence: 99%

Pathway Evolution by Horizontal Transfer and Positive Selection Is Accommodated by Relaxed Negative Selection upon Upstream Pathway Genes in Purple Bacterial Carotenoid Biosynthesis

Klassen

2009

J Bacteriol

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Horizontal gene transfer and selection are major forces driving microbial evolution. However, interactions between them are rarely studied. Phylogenetic analyses of purple bacterial carotenoid biosynthesis genes suggest two lineages: one producing spheroidenone and the other producing spirilloxanthin. Of the latter lineage, Rubrivivax gelatinosus S1 and Hoeflea phototrophica DFL-43 also or instead produce spheroidenone. Evolution of the spheroidenone pathway from that producing spirilloxanthin theoretically requires changes in the substrate specificity of upstream pathway enzymes and acquisition of a terminal ketolase (CrtA). In R. gelatinosus and likely also in H. phototrophica, CrtA was acquired from the Bacteroidetes, in which it functions as a hydroxylase. Estimation of nonsynonymous and synonymous mutations using several pairwise methods indicated positive selection upon both genes, consistent with their functional changes from hydroxylases to ketolases. Relaxed negative selection upon all other carotenoid biosynthetic genes in these organisms was also apparent, likely facilitating changes in their substrate specificities. Furthermore, all genes responsible for terminal carotenoid biosynthetic pathway steps were under reduced negative selection compared to those known to govern biosynthetic pathway specificity. Horizontal transfer of crtA into R. gelatinosus and H. phototrophica has therefore likely been promoted by (i) the apparent selective advantage of spheroidenone production relative to spirilloxanthin production, (ii) reduced negative selection upon other carotenoid biosynthetic genes, facilitating changes in their substrate specificities, and (iii) preexisting low enzyme substrate specificities due to relaxed negative selection. These results highlight the importance and complexity of selection acting upon both a horizontally transferred gene and the biochemical network into which it is integrating.

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The origin and evolution of modern metabolism

Cited by 106 publications

References 81 publications

History of biological metal utilization inferred through phylogenomic analysis of protein structures

History of biological metal utilization inferred through phylogenomic analysis of protein structures

Regulatory crosstalk of the metabolic network

Pathway Evolution by Horizontal Transfer and Positive Selection Is Accommodated by Relaxed Negative Selection upon Upstream Pathway Genes in Purple Bacterial Carotenoid Biosynthesis

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