Inorganic Pyrophosphate and the Evolution of Biological Energy Transformation.

Baltscheffsky, Herrick; Hofsten, Bengt von; Svensson, Sigfrid; Norin, Torbjörn; Eriksson, G.; Blinc, R.; Paušak, S.; Ehrenberg, L.; Dumanović, J.

doi:10.3891/acta.chem.scand.21-1973

Cited by 36 publications

(22 citation statements)

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“…It is the only known alternative to ATP synthases for the production of energy-rich phosphoanhydride bonds and is the only primary pump that is preserved in all three domains of life (42,51). Given mounting evidence that the earliest forms of life were chemoautotrophic (52), the apparent pervasiveness of energy-conserving H + -PPase pathways in chemoautotrophs adds further weight to the hypothesis that PPi preceded ATP as the central energy carrier in the early evolution of life (51,53,54).…”

Section: Resultsmentioning

confidence: 99%

Metaproteomics of a gutless marine worm and its symbiotic microbial community reveal unusual pathways for carbon and energy use

Kleiner

Wentrup

Lott

et al. 2012

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

184

251

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Low nutrient and energy availability has led to the evolution of numerous strategies for overcoming these limitations, of which symbiotic associations represent a key mechanism. Particularly striking are the associations between chemosynthetic bacteria and marine animals that thrive in nutrient-poor environments such as the deep sea because the symbionts allow their hosts to grow on inorganic energy and carbon sources such as sulfide and CO 2 . Remarkably little is known about the physiological strategies that enable chemosynthetic symbioses to colonize oligotrophic environments. In this study, we used metaproteomics and metabolomics to investigate the intricate network of metabolic interactions in the chemosynthetic association between Olavius algarvensis, a gutless marine worm, and its bacterial symbionts. We propose previously undescribed pathways for coping with energy and nutrient limitation, some of which may be widespread in both freeliving and symbiotic bacteria. These pathways include (i) a pathway for symbiont assimilation of the host waste products acetate, propionate, succinate and malate; (ii) the potential use of carbon monoxide as an energy source, a substrate previously not known to play a role in marine invertebrate symbioses; (iii) the potential use of hydrogen as an energy source; (iv) the strong expression of high-affinity uptake transporters; and (v) as yet undescribed energy-efficient steps in CO 2 fixation and sulfate reduction. The high expression of proteins involved in pathways for energy and carbon uptake and conservation in the O. algarvensis symbiosis indicates that the oligotrophic nature of its environment exerted a strong selective pressure in shaping these associations.3-hydroxypropionate bi-cycle | Calvin cycle | proton-translocating pyrophosphatase | pyrophosphate dependent phosphofructokinase | metagenomics G rowth in nutrient-limited environments presents numerous challenges to organisms. Symbiotic and syntrophic relationships have evolved as particularly successful strategies for coping with these challenges. Such nutritional symbioses are widespread in nature and, for example, have enabled plants to colonize nitrogen-poor soils and animals to thrive on food sources that lack essential amino acids and vitamins (1). Chemosynthetic symbioses, discovered only 35 years ago at hydrothermal vents in the deep sea, revolutionized our understanding of nutritional associations, because these symbioses enable animals to live on inorganic energy and carbon sources such as sulfide and CO 2 (2, 3). The chemosynthetic symbionts use the energy obtained from oxidizing reduced inorganic compounds such as sulfide to fix CO 2 , ultimately providing their hosts with organic carbon compounds. Chemosynthetic symbioses thus are able to thrive in habitats where organic carbon sources are rare, such as the deep sea, and the symbionts often are so efficient at providing nutrition that many hosts have reduced their digestive systems (4).The marine oligochaete Olavius algarvensis is a particularly extre...

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Section: Resultsmentioning

confidence: 99%

Metaproteomics of a gutless marine worm and its symbiotic microbial community reveal unusual pathways for carbon and energy use

Kleiner

Wentrup

Lott

et al. 2012

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

184

251

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“…An example of exergonic redox reactions would be the formation of pyrite by reaction (4.1), either at the outside of the membrane (Koch & Schmidt 1991) or at the inside of the membrane (Wächtershäuser 1997). Next, membrane-bound pyrophosphate formation (Baltscheffsky et al 1966;Baltscheffsky 1967Baltscheffsky , 1971 would become established, now causing the proton potential to mediate energy coupling between redox energy and group activation energy. Finally, membrane-bound pyrophosphate formation would be first supplemented and later substituted by an emerging rotary ATPase.…”

Section: Cellularization (A) Surface Lipophilizationmentioning

confidence: 99%

“…as inorganic substitutes for ATP (Baltscheffsky 1967). Pyrophosphate has been suggested as primordial phosphorylation agent (Baltscheffsky 1971). Extant organisms produce pyrophosphate by photo-phosphorylation (Baltscheffsky et al 1966).…”

Section: Volcanic Origin Of Chemoautotrophic Life G Wächtershäuser 1791mentioning

confidence: 99%

From volcanic origins of chemoautotrophic life to Bacteria, Archaea and Eukarya

Wächtershäuser¹

2006

Phil. Trans. R. Soc. B

245

225

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The theory of a chemoautotrophic origin of life in a volcanic iron-sulphur world postulates a pioneer organism at sites of reducing volcanic exhalations. The pioneer organism is characterized by a composite structure with an inorganic substructure and an organic superstructure. Within the surfaces of the inorganic substructure iron, cobalt, nickel and other transition metal centres with sulphido, carbonyl and other ligands were catalytically active and promoted the growth of the organic superstructure through carbon fixation, driven by the reducing potential of the volcanic exhalations. This pioneer metabolism was reproductive by an autocatalytic feedback mechanism. Some organic products served as ligands for activating catalytic metal centres whence they arose. The unitary structure-function relationship of the pioneer organism later gave rise to two major strands of evolution: cellularization and emergence of the genetic machinery. This early phase of evolution ended with segregation of the domains Bacteria, Archaea and Eukarya from a rapidly evolving population of pre-cells. Thus, life started with an initial, direct, deterministic chemical mechanism of evolution giving rise to a later, indirect, stochastic, genetic mechanism of evolution and the upward evolution of life by increase of complexity is grounded ultimately in the synthetic redox chemistry of the pioneer organism.

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“…of biopolymers (Hulshof and Ponnamperuma 1976;Baltscheffsky et al 1986) such as RNA or RNA-like polymers in the ancient aqueous environments (Joyce 1989). Although solid-phase catalysts lack the flexibility of an enzyme (Erskelens 1990), they might have been useful before polynucleotides, polypeptides, and proteins appeared on primitive Earth.…”

Section: Hypothetical Catalytic Cycle Of a Prebiotic Inorganic "Enzymmentioning

confidence: 99%

“…In addition, PPi is considered to be an evolutionary precursor of ATP and could have acted as an energy-donor compound (Hulshof and Ponnamperuma 1976;Baltscheffsky et al 1986) in the primordial self-replicating soup of nucleotides (Joyce 1989;Hermes-Lima 1990b). Nonenzymatic PPi synthesis has also been studied as a model with which to understand the mechanisms of enzymatically catalyzed phosphorylation reactions (Nelson and Racker 1973;Meyer-Fernandes and Vieyra !988).…”

Section: Introductionmentioning

confidence: 99%

Pyrophosphate synthesis from phospho(enol)pyruvate catalyzed by precipitated magnesium phosphate with ?enzyme-like? activity

Hermes‐Lima

Vieyra

1992

J Mol Evol

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The enzyme-like kinetic properties of precipitated magnesium phosphate as a catalyst for formation of pyrophosphate (PPi) from phospho(enol)pyruvate (PEP) are described. This synthesis occurs at a low temperature (37 degrees C) and represents a model that may help us understand the relevance to chemical evolution of minerals as ancient catalysts whose functions could have been taken over by contemporary enzymes. An insoluble Pi.Mg matrix was formed in a medium with 80% of the water replaced by dimethyl sulfoxide as a way of simulating conditions in a drying pond. Phospho(enol)pyruvate adsorbs onto the Pi.Mg surface according to a Langmuir isotherm, and the PEP concentration dependence of PPi formation follows a Michaelian-like function. A yield of 33% for transformation of the initially adsorbed PEP into PPi was attained after 4 days of incubation with equimolecular concentrations of Pi, MgCl2, and PEP. The magnesium concentration dependence for Pi and Mg precipitation, for adsorption of PEP onto solid Pi.Mg, and for PPi formation showed complex cooperative behavior. These results taken as a whole lead to the conclusion that the Pi.Mg surface not only provides a reactant for PPi formation but also catalyzes the reaction.

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Inorganic Pyrophosphate and the Evolution of Biological Energy Transformation.

Cited by 36 publications

References 0 publications

Metaproteomics of a gutless marine worm and its symbiotic microbial community reveal unusual pathways for carbon and energy use

Metaproteomics of a gutless marine worm and its symbiotic microbial community reveal unusual pathways for carbon and energy use

From volcanic origins of chemoautotrophic life to Bacteria, Archaea and Eukarya

Pyrophosphate synthesis from phospho(enol)pyruvate catalyzed by precipitated magnesium phosphate with ?enzyme-like? activity

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