Biological calorimetry and the thermodynamics of the origination and evolution of life

Hansen, Lee D.; Criddle, Richard S.; Battley, Edwin H.

doi:10.1351/pac-con-08-09-09

Cited by 46 publications

(48 citation statements)

References 84 publications

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“…From the standpoint of energetics, it appears possible that life could have evolved from gases (H 2 , CO 2 , CO, N 2 , H 2 S, SO 2 ) that reacted, with the help of transition metals, at the solid catalyst phase to produce aqueous organic compounds. Current views on the changes in free energy of biological systems, which are necessarily negative [14,29,39], as well as changes in entropy, which are close to zero [245,246], are compatible with that view. The antiquity of anaerobic chemolithoautotrophs seems as evident today as it did 40 years ago [44].…”

Section: Resultsmentioning

confidence: 97%

Early bioenergetic evolution

Sousa

Thiergart

Landan

et al. 2013

Phil. Trans. R. Soc. B

233

256

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Life is the harnessing of chemical energy in such a way that the energy-harnessing device makes a copy of itself. This paper outlines an energetically feasible path from a particular inorganic setting for the origin of life to the first free-living cells. The sources of energy available to early organic synthesis, early evolving systems and early cells stand in the foreground, as do the possible mechanisms of their conversion into harnessable chemical energy for synthetic reactions. With regard to the possible temporal sequence of events, we focus on: (i) alkaline hydrothermal vents as the far-from-equilibrium setting, (ii) the Wood–Ljungdahl (acetyl-CoA) pathway as the route that could have underpinned carbon assimilation for these processes, (iii) biochemical divergence, within the naturally formed inorganic compartments at a hydrothermal mound, of geochemically confined replicating entities with a complexity below that of free-living prokaryotes, and (iv) acetogenesis and methanogenesis as the ancestral forms of carbon and energy metabolism in the first free-living ancestors of the eubacteria and archaebacteria, respectively. In terms of the main evolutionary transitions in early bioenergetic evolution, we focus on: (i) thioester-dependent substrate-level phosphorylations, (ii) harnessing of naturally existing proton gradients at the vent–ocean interface via the ATP synthase, (iii) harnessing of Na+ gradients generated by H+/Na+ antiporters, (iv) flavin-based bifurcation-dependent gradient generation, and finally (v) quinone-based (and Q-cycle-dependent) proton gradient generation. Of those five transitions, the first four are posited to have taken place at the vent. Ultimately, all of these bioenergetic processes depend, even today, upon CO2 reduction with low-potential ferredoxin (Fd), generated either chemosynthetically or photosynthetically, suggesting a reaction of the type ‘reduced iron → reduced carbon’ at the beginning of bioenergetic evolution.

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Section: Resultsmentioning

confidence: 97%

Early bioenergetic evolution

Sousa

Thiergart

Landan

et al. 2013

Phil. Trans. R. Soc. B

233

256

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“…It is this maintenance of internal structure that is the key factor in allowing a return to viability once an increase in environmental temperature drives the resumption of molecular movement and hence metabolism [12]. There is remarkably little difference between vitrified and living cells in terms of bulk structure, composition and thermodynamic state variables [37]. The difference comes in the extent of molecular motion, small-scale variations in entropy within the cell, and the flux of energy.…”

Section: Discussionmentioning

confidence: 99%

A Low Temperature Limit for Life on Earth

et al. 2013

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There is no generally accepted value for the lower temperature limit for life on Earth. We present empirical evidence that free-living microbial cells cooling in the presence of external ice will undergo freeze-induced desiccation and a glass transition (vitrification) at a temperature between −10°C and −26°C. In contrast to intracellular freezing, vitrification does not result in death and cells may survive very low temperatures once vitrified. The high internal viscosity following vitrification means that diffusion of oxygen and metabolites is slowed to such an extent that cellular metabolism ceases. The temperature range for intracellular vitrification makes this a process of fundamental ecological significance for free-living microbes. It is only where extracellular ice is not present that cells can continue to metabolise below these temperatures, and water droplets in clouds provide an important example of such a habitat. In multicellular organisms the cells are isolated from ice in the environment, and the major factor dictating how they respond to low temperature is the physical state of the extracellular fluid. Where this fluid freezes, then the cells will dehydrate and vitrify in a manner analogous to free-living microbes. Where the extracellular fluid undercools then cells can continue to metabolise, albeit slowly, to temperatures below the vitrification temperature of free-living microbes. Evidence suggests that these cells do also eventually vitrify, but at lower temperatures that may be below −50°C. Since cells must return to a fluid state to resume metabolism and complete their life cycle, and ice is almost universally present in environments at sub-zero temperatures, we propose that the vitrification temperature represents a general lower thermal limit to life on Earth, though its precise value differs between unicellular (typically above −20°C) and multicellular organisms (typically below −20°C). Few multicellular organisms can, however, complete their life cycle at temperatures below ∼−2°C.

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“…Indeed the enthalpy of combustion is directly proportional to the amount of oxygen consumed (or to the amount of electron required to reduce O 2 into H 2 O). In this context it is commonly admitted that 455 kJ are liberated for the consumption of 1 mol of O 2 [43,44]; this value is referred to as the oxycaloric equivalent. In closed calorimetric vials the oxygen amount in solution can be measured using oxygen electrodes or approximated using the Weiss equation [45] and thus the heat generated by respiration can be approximated as well [1,46].…”

Section: Isothermal Microcalorimetrymentioning

confidence: 99%