How did LUCA make a living? Chemiosmosis in the origin of life

Lane, Nick; Allen, John F.; Martin, William

doi:10.1002/bies.200900131

Cited by 326 publications

(282 citation statements)

References 77 publications

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“…An entry in the literature of this debate is in [11]. In recent years the opposition between the two approaches has been overstepped by more unitary experimental and theoretical frames, taking into account energetic, evolutionary, proto-metabolic and ur-environmental aspects [12][13][14][15][16][17][18][19][20][21][22]. The productive interaction between vesicles and RNA replication was reported [23].…”

Section: The Need For a Unitary Physical-chemical Framementioning

confidence: 99%

“…Whether autocatalytic cycles have been able to establish themselves is matter of open debate [8,16,17,21,90,133,134]. In particular, the onset of metabolic cycles on the prebiotic Earth has been dubbed as implausible [134], mostly on the basis of kinetic considerations and on the difficulty of justifying both thermodynamically and kinetically the exclusion of side reactions that would disrupt the cycle.…”

Section: Synthesis Of Pre-metabolic Componentsmentioning

confidence: 99%

“…In particular, the onset of metabolic cycles on the prebiotic Earth has been dubbed as implausible [134], mostly on the basis of kinetic considerations and on the difficulty of justifying both thermodynamically and kinetically the exclusion of side reactions that would disrupt the cycle. This opinion is not generally shared [8,12,14,16,17,21,[84][85][86]132,134,135]. The similarity of spontaneous cycles with metabolic ones has been established for the formose reaction [136][137][138], which converts formaldehyde to various sugars and other products, and has been suggested for the triose-ammonia reaction [139] and for the acceleration of the HCN oligomerization [140].…”

Section: Synthesis Of Pre-metabolic Componentsmentioning

confidence: 99%

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Formamide and the origin of life

Saladino

Crestini

Pino

et al. 2012

Physics of Life Reviews

262

234

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The complexity of life boils down to the definition: "self-sustained chemical system capable of undergoing Darwinian evolution" (Joyce, 1994) [1]. The term "self-sustained" implies a set of chemical reactions capable of harnessing energy from the environment, using it to carry out programmed anabolic and catabolic functions. We briefly present our opinion on the general validity of this definition.Running anabolic and catabolic functions entails complex chemical information whose stability, reproducibility and evolution constitute the core of what is dubbed genetics.Life as-we-know-it is made of the intimate interaction of metabolism and genetics, both built around the chemistry of the most common elements of the Universe (hydrogen, oxygen, nitrogen, carbon). Other elements like phosphorus and sulphur play important but ancillary and potentially replaceable roles.The reproducible interaction of metabolic and genetic cycles results in the hypercycles of organization and de-organization of chemical information that we consider living entities. In order to approach the problem of the origin of life it is therefore reasonable to start from the assumption that both metabolism and genetics had a common origin, shared a common chemical frame, were embedded in physical-chemical conditions favourable for the onset of both.The most abundant three-atoms organic compound in interstellar environment is hydrogen cyanide HCN, the most abundant three-atoms inorganic compound is water H 2 O. The combination of the two results in the formation of formamide H 2 NCOH. We have explored the chemistry of formamide in conditions compatible with the synthesis and the stability of compounds of potential pre-genetic and pre-metabolic interest. We discuss evidence showing (i) that all the compounds necessary for the build-up of nucleic acids are easily obtained abiotically, (ii) that essentially all the steps leading to the spontaneous generation of RNA are abiotically possible, (iii) that the key compounds of extant metabolic cycles are obtained in the same chemical frame, often in the same test tube.How close are these observations to a plausible scenario for the origin of life?

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Section: The Need For a Unitary Physical-chemical Framementioning

confidence: 99%

Section: Synthesis Of Pre-metabolic Componentsmentioning

confidence: 99%

Section: Synthesis Of Pre-metabolic Componentsmentioning

confidence: 99%

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Formamide and the origin of life

Saladino

Crestini

Pino

et al. 2012

Physics of Life Reviews

262

234

View full text Add to dashboard Cite

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“…It is increasingly recognised that H 2 metabolism is important for a wide range of microorganisms: lithotrophs and phototrophs, respirers and fermenters and aerobes and anaerobes alike (Vignais and Billoud, 2007;Schwartz et al, 2013;Peters et al, 2014). Furthermore, it is widely hypothesised that H 2 was the primordial electron donor, suggesting early and sustained evolutionary importance (Lane et al, 2010).…”

Section: Introductionmentioning

confidence: 99%

Genomic and metagenomic surveys of hydrogenase distribution indicate H2 is a widely utilised energy source for microbial growth and survival

et al. 2015

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Recent physiological and ecological studies have challenged the long-held belief that microbial metabolism of molecular hydrogen (H 2 ) is a niche process. To gain a broader insight into the importance of microbial H 2 metabolism, we comprehensively surveyed the genomic and metagenomic distribution of hydrogenases, the reversible enzymes that catalyse the oxidation and evolution of H 2 . The protein sequences of 3286 non-redundant putative hydrogenases were curated from publicly available databases. These metalloenzymes were classified into multiple groups based on (1) amino acid sequence phylogeny, (2) metal-binding motifs, (3) predicted genetic organisation and (4) reported biochemical characteristics. Four groups (22 subgroups) of [NiFe]-hydrogenase, three groups (6 subtypes) of [FeFe]-hydrogenases and a small group of [Fe]-hydrogenases were identified. We predict that this hydrogenase diversity supports H 2 -based respiration, fermentation and carbon fixation processes in both oxic and anoxic environments, in addition to various H 2 -sensing, electron-bifurcation and energy-conversion mechanisms. Hydrogenase-encoding genes were identified in 51 bacterial and archaeal phyla, suggesting strong pressure for both vertical and lateral acquisition. Furthermore, hydrogenase genes could be recovered from diverse terrestrial, aquatic and host-associated metagenomes in varying proportions, indicating a broad ecological distribution and utilisation. Oxygen content (pO 2 ) appears to be a central factor driving the phylum-and ecosystem-level distribution of these genes. In addition to compounding evidence that H 2 was the first electron donor for life, our analysis suggests that the great diversification of hydrogenases has enabled H 2 metabolism to sustain the growth or survival of microorganisms in a wide range of ecosystems to the present day. This work also provides a comprehensive expanded system for classifying hydrogenases and identifies new prospects for investigating H 2 metabolism.

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“…Membrane barriers also permit the building of barrages to accumulate potential energy and become less dependent on the uncertain free energy provision from the surrounding soup. The evolutionary onset of proton-motive forces is analyzed in (Lane et al, 2010).…”

Section: Ratchet Mechanisms Shortening the Life's Emergence Timementioning

confidence: 99%

Basic statistical recipes for the emergence of biochemical discernment

Michel

2011

Progress in Biophysics and Molecular Biology

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An essential step towards understanding life would be to identify the very basic mechanisms responsible for the discerning behaviour of living biochemical systems, absent from randomly reacting chemical soups. One intuitively feels that this question goes beyond the particular nature of the biological molecules and should relate to general physical principles. The preeminent physicist Ludwig Boltzmann early envisioned life as a struggle for entropy, in concordance with the subsequent principle of self-organization out of equilibrium. Reexamination of elementary steady state biochemical systems from a statistical perspective supports this view and shows that sigmoidal responses arising from microstates elimination, are sufficient to explain innermost characteristics of life, including its capacity to convert random molecular interactions into accurate biological reactions. A primary operating strategy to achieve this goal is the introduction of time-irreversible transitions in molecular state conversion cycles by injection of free energy, which confers decisional capacity to single macromolecules. Selected examples from various fields of molecular biology such as enzymology and gene expression, are provided to show that these non-equilibrium steady state mechanisms remain important in contemporary biochemical systems. But in addition, information archiving allowed the emergence of the time-reversible counterparts of these mechanisms, mediated by evolutionary preorganized macromolecular complexes capable of increasing discernment in a non-dissipative manner.

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How did LUCA make a living? Chemiosmosis in the origin of life

Cited by 326 publications

References 77 publications

Formamide and the origin of life

Formamide and the origin of life

Genomic and metagenomic surveys of hydrogenase distribution indicate H2 is a widely utilised energy source for microbial growth and survival

Basic statistical recipes for the emergence of biochemical discernment

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