MBE Advance Access originally published online on March 31, 2006
Molecular Biology and Evolution 2006 23(6):1286-1292; doi:10.1093/molbev/msk014
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Research Article |
The Stepwise Evolution of Early Life Driven by Energy Conservation
* Department of Biochemistry and Molecular Biology and Pennsylvania State Astrobiology Research Center, 205 South Frear Laboratory, Pennsylvania State University; and Department of Geosciences and Pennsylvania State Astrobiology Research Center, 220 Deike Building, Pennsylvania State University
E-mail: jgf3{at}psu.edu.
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Abstract |
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Two main theories have emerged for the origin and early evolution of life based on heterotrophic versus chemoautotrophic metabolisms. With the exception of a role for CO, the theories have little common ground. Here we propose an alternative theory for the early evolution of the cell which combines principal features of the widely disparate theories. The theory is based on the extant pathway for conversion of CO to methane and acetate, largely deduced from the genomic analysis of the archaeon Methanosarcina acetivorans. In contrast to current paradigms, we propose that an energy-conservation pathway was the major force which powered and directed the early evolution of the cell. We envision the proposed primitive energy-conservation pathway to have developed sometime after a period of chemical evolution but prior to the establishment of diverse protein-based anaerobic metabolisms. We further propose that energy conservation played the predominant role in the later evolution of anaerobic metabolisms which explains the origin and evolution of extant methanogenic pathways.
Key Words: Methanosarcina acetivorans • energy conservation • methanogenesis • acetate kinase • phosphotransacetylase
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Introduction |
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TOPAbstractIntroductionMaterials and MethodsResults and DiscussionAcknowledgementsReferences |
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The heterotrophic theory for the origin of life (Lazcano and Miller 1999
; Bada and Lazcano 2002) purports that life arose from an "organic soup" of diverse preexisting compounds. The theory is supported experimentally by the abiotic synthesis of diverse biologically important compounds starting from reduced gases (Miller 1998), including CO (Pinto, Gladstone, and Yung 1980; Chameides and Walker 1981; Miyakawa et al. 2002), and the view that the earth's atmosphere at the time of the origin of life could have contained significant amounts of CO (Holland 1984; Kasting 1990; Kharecha, Kasting, and Siefert 2005), especially, if the hydrogen escape rates were low (Tian et al. 2005; Pavlov, Toon, and Feng 2006). The heterotrophic theory is also derived from the metabolism of extant fermentative organisms which metabolize reduced organic compounds for the synthesis of adenosine triphosphate (ATP) by substrate-level phosphorylation (SLP) (Lazcano and Miller 1999). A widely accepted challenge to this theory is that life had a chemoautotrophic origin (Russell et al. 1988; Wachtershauser 1988; Russell and Hall 1997) in which the primary prebiotic initiation reaction for carbon fixation was the surface-catalyzed synthesis of an acetate thioester from CO and H2S driven by a geochemical energy source. Central to the chemoautotrophic theory is the evolution of biological CO2 fixation pathways in primitive cells for which there are two views. One view is that a variation of the extant reduced citric acid cycle evolved first (Wachtershauser 1990), whereas the other view suggests a primitive form of the extant Wood-Ljungdahl pathway (Wachtershauser 1997; Pereto et al. 1999; Martin and Russell 2003; Russell and Martin 2004) in which 2CO2 molecules are reduced to acetyl-coenzyme A (CoA).
With the exception of a role for CO, the heterotrophic and chemoautotrophic theories have little common ground. Proponents of each theory continue to argue steadfastly for the principles which separate them (Wachtershauser 2002). In the debate, far less attention has been given to the role that energy conservation could have played in the early stages for the evolution of life and metabolic pathways. Although inherent to the heterotrophic theory, a major role for SLP in the chemoautotrophic theory has not been advanced. It has been suggested that the earliest chemoautotrophic organisms conserved energy by a chemiosmotic mechanism in which ATP synthesis was driven by a naturally occurring geochemical pH gradient (Russell and Hall 1997). Here we propose a novel cyclic SLP energy-conserving pathway that functioned in primitive cells. Further, the cells feature a combination of principles that have separated the two main contrasting theories for the origin of life (Lazcano and Miller 1999; Martin and Russell 2003; Russell and Martin 2004). Although our primitive cell requires the abiotic synthesis of diverse organic compounds for biosynthesis of cell material that is a tenet of the heterotrophic theory (Miller and Bada 1988), the "primary" energy source is geochemical that is also a feature of the chemoautotrophic hypothesis (Wachtershauser 1988). Moreover, we propose that the cyclic SLP energy-conserving pathway was the main driving force directing the evolution of primitive metabolisms and extant energy-yielding pathways, reshaping current theories for the early evolution of life.
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Materials and Methods |
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Analysis of the Methanosarcina acetivorans strain C2A genome (Galagan et al. 2002
) was performed with the sequence available at The Institute for Genomic Research (TIGR) Web site (http://pathema.tigr.org/tigr-scripts/CMR/CmrHomePage.cgi) using the Comprehensive Microbial Resource bioinformatics tools previously described (Peterson et al. 2001). All annotations reported were the primary annotations listed on the TIGR Web site. |
Results and Discussion |
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The Pathway for CO Utilization by M. acetivorans C2A
A popular approach for development of theories for the origins of metabolisms is the conceptual reconstruction from extant pathways. Extant CO metabolisms of ancient microbial lineages have the potential to reveal characteristics of primitive metabolic pathways. Strictly anaerobic methane-producing Archaea (methanoarchaea) are particularly attractive for predicting ancient pathways. Phylogenetic analysis indicates that methanogenic Archaea are ancient (Bapteste, Brochier, and Boucher 2005
), appearing prominent among the deepest branching chemoautotrophs on the tree of life (Kandler 1993) and dating to perhaps 3.8–4.1 billion years ago (Battistuzzi, Feijao, and Hedges 2004). The phylogenetic analyses are supported by recent evidence for biologically produced methane in 3.5 billion-year-old hydrothermal precipitates (Ueno et al. 2006). Further, a few species of methanoarchaea utilize CO as a growth substrate. It was recently reported that M. acetivorans C2A has a highly unusual energy-yielding metabolism producing methane, acetate, and formate during CO-dependent chemoautotrophic growth (Rother and Metcalf 2004).
Figure 1 shows the pathway proposed for conversion of CO to acetate and methane based on the genomic analysis of M. acetivorans C2A and experimental results. Step 1 involves oxidation of CO to CO2 providing electrons for the reduction of CO2 to CH3-tetrahydromethanopterin (THMPT) (steps 2–6) in analogy to the well-characterized pathway for CO2 reduction to methane with electrons derived from the oxidation of H2 in species other than M. acetivorans C2A (Ferry 1999). Methane is produced from CH3-THMPT in steps 7–9, steps common to all known pathways for methanogenesis (Ferry 1999). The genomic sequence of M. acetivorans C2A is annotated for genes encoding enzymes catalyzing steps 2–9 (table 1), supporting the proposed pathway. Genes annotated to encode both the molybdenum and tungsten forms of the formyl-methanofuran (MF) dehydrogenase were identified in the genome. However, genes encoding the H2-dependent methylene-THMPT reductase were not found, consistent with the inability of M. acetivorans to reduce CO2 to methane with H2. Further, proteomic analyses of CO-grown M. acetivorans C2A (in preparation) has provided experimental evidence for abundant synthesis of enzymes catalyzing steps 2–9. The genome is also annotated with genes encoding CooS (table 1), a CO dehydrogenase with the potential to catalyze step 1; however, the CO dehydrogenase/acetyl-CoA synthetase proposed to catalyze step 10 (see below) could also function in step 1.
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Acetate is produced from CH3-THMPT in the proposed pathway (steps 10–12, fig. 1) by reversal of the first three steps in the well-characterized pathway for methane formation from acetate in other Methanosarcina species (Ferry 2003
). In the acetate pathway, the five-subunit CO dehydrogenase/acetyl-CoA synthetase (CdhABCDE) reversibly cleaves acetyl-CoA producing CH3-THMPT, a carbonyl group, and CoA. Indeed, it has been proposed (Rother and Metcalf 2004) that the CdhABCDE complex condenses the methyl group of CH3-THMPT with CO and CoA to synthesize acetyl-CoA in step 10 (fig. 1). The reported synthesis of acetyl-CoA from CO, CH3I, and CoA by CdhABCDE from Methanosarcina thermophila (Abbanat and Ferry 1990) further supports a role for this complex in the proposed pathway (fig. 1). The acetyl-CoA is converted to acetate by phosphotransacetylase (Pta) in step 11 and acetate kinase (Ack) in step 12 with the synthesis of ATP by SLP. The genome is annotated with pta, ack, and duplicate cdhABCDE operons (MA1011–MA1016 and MA3860–MA3865, table 1). Further, proteomic analyses identify Pta, Ack, and subunits of both CdhABCDE complexes in CO-grown M. acetivorans C2A (in preparation). Finally, M. acetivorans C2A variants with the ack and pta genes disrupted are unable to grow with CO (Rother and Metcalf 2004), a result that further supports a role for these enzymes in the proposed pathway (fig. 1). Thus, the results suggest that Ack plays a prominent role in the energy metabolism of CO-grown M. acetivorans. Indeed, the energy available for ATP synthesis during conversion of CO to acetate (eq. 1) is comparable to that for conversion of CO to methane (eq. 2).
 | (1) |
 | (2) |
). The finding that Ack and Pta function in SLP pathways of chemolithoautotrophic methanoarchaea is consistent with a role for SLP in a chemoautotrophic origin of life.
A Primitive Cyclic SLP Pathway for an Early Cell
The pathway in figure 1 provides a unique perspective for proposing an alternative to primitive metabolisms predicted by either of the two leading theories for the origin of life (Martin and Russell 2003; Russell and Martin 2004). We propose that a cyclic SLP pathway (fig. 2A), with combined features of the heterotrophic and chemoautotrophic theories, evolved early and had a prominent role in the evolution of diverse metabolisms. We envision that this pathway evolved sometime after a period of chemical evolution (possibly including an "RNA World"; Joyce 2002) but before the establishment of diverse protein-based biochemistries. The pathway features the catalysis of steps B and C (fig. 2A) by ancestors of extant Pta and Ack wherein ATP is synthesized by SLP, although ATP could have been replaced with pyrophosphate (de Duve 1991; de Zwart, Meade, and Pratt 2004). Further, a one-step conversion of CH3COSR to acetate and ATP catalyzed by an ancestor of acetate thiokinase cannot be ruled out; nonetheless, the major implications of the pathway are unchanged. We suggest that the SLP pathway was operative in primitive lipid-encapsulated cells (fig. 2A), closely associated with sulfide minerals. The acetic acid and R-SH excreted by the cell is converted back to the CH3COSR thioester in an abiotic reaction outside the lipid membrane (step A; fig. 2A). The synthesis of CH3COSR from CO, R-SH, and CH3SH (broken arrow, fig. 2A) is not part of the cyclic energy-conserving pathway (steps A–C) and functions only to prime the pathway and supply acetyl groups for biosynthesis. Step A and the priming reaction (broken arrow, fig. 2) are grounded in the previously proposed geochemical-driven surface-catalyzed synthesis of acetate thioesters from CO and CH3SH, a primary tenet of the chemoautotrophic theory (Heinen and Lauwers 1996; Huber and Wachtershauser 1997; Martin and Russell 2003). Thus, Step A is proposed to occur adjacent to the cell membrane on the surface of FeS/NiS minerals analogous to the Fe-S-Ni active site of the CdhABCDE complex (step 10, fig. 1) where an acetyl group is condensed with CoA-SH to form CH3COSCoA (Drennan, Doukov, and Ragsdale 2004). Our model also uses geochemical energy, consistent with previously proposed abiotic acetate thioester synthesis driven by an exergonic "pyrite-pulled" reaction in which FeS and H2S are converted to FeS2 and H2 (Wachtershauser 1988, 1992). Thus, the pathway in figure 2A (steps A–C) is a biogeochemical cycle in which the primary energy source is geochemical (step A), and primitive enzymes conserve this energy by SLP (steps B and C). The cyclic pathway would have circumvented the previously discussed problem of instability of the CH3COSR thioester (Huber and Wachtershauser 1997; Russell and Martin 2004) by the ensuing enzyme-catalyzed conversion to acetyl-phosphate and acetate (steps B and C). Further, the cyclic pathway ensures a steady supply of substrates for pyrite-pulled abiotic synthesis of the thioester immediately outside the cell. Support for this externally driven cycle can be found in the extant archaeon Pyrodictium occultum that accumulates pyrite outside the cell during growth by sulfur respiration (Stetter, Konig, and Stackebrandt 1983). One explanation previously offered is that P. occultum forms pyrite outside the cell by reaction of Fe2+ in the medium with the excreted metabolic end product H2S to obtain additional energy for growth (Stetter, Konig, and Stackebrandt 1983).
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The cyclic energy-conserving pathway (steps A–C, fig. 2A) is not dependent on oxidation of a preexisting reduced organic compound to generate ATP that is central to extant fermentations and a precept of the heterotrophic theory for the origin of life. The pathway is also not dependent on redox chemistry and chemiosmosis for energy conservation that has been suggested for the chemoautotrophic theory (Martin and Russell 2003
). Thus, the pathway incorporates SLP and surface-catalyzed reactions that are, respectively, prominent features of the widely disparate heterotrophic and chemoautotrophic theories.
In our view, the proposed cyclic SLP pathway (fig. 2A) was of major importance in evolution of the cell, and evolved prior to autotrophic carbon fixation pathways, which contrasts with currently proposed chemoautotrophic theories (Wachtershauser 1990; Martin and Russell 2003; Russell and Martin 2004). We suggest that the pathway necessarily evolved early to supply an energy "currency" that drove and directed coevolution of primitive energy-dependent biosynthetic pathways utilizing the previously proposed diversity of precursor compounds synthesized in prebiotic reactions. We further suggest that the SLP pathway was the first protein-based energy-conserving metabolic cycle and was an early event in the evolution of diverse primitive metabolisms. This view is supported by the simplicity of the pathway involving only two enzymes which is in contrast to the more complicated membrane-bound electron transport chain and multisubunit ATPase complex inherent in the chemiosmotic mechanism previously proposed to have evolved in primitive cells (Martin and Russell 2003). Recent crystal structures establish that Ack and Pta are simple homodimers with no prosthetic groups (Buss et al. 2001; Iyer et al. 2004). Further, the secondary structure of Ack suggests an ancient origin and the founding member of the ASKHA superfamily of phosphotransferases (Buss et al. 2001). Thus, the pathway could have been necessary for the early establishment of phosphoryl group transfer that is essential for diverse metabolic processes fundamental to all extant life. It has been proposed that acetyl phosphate served as the first metabolic handle for activated phosphate (de Duve 1991). Indeed, Ack from Escherichia coli also transfers phosphate from acetyl phosphate to enzyme I of the bacterial phosphotransferase system (Fox, Meadow, and Roseman 1986). Thus, Pta and Ack could have been among the first enzymes to have evolved. In fact, it has been demonstrated that steps B and C occur without enzymes (Weber 1981, 1982) that may have preceded de novo evolution of primitive ancestors to Pta and Ack. Finally, de Duve (1991) also has postulated a nonenzymatic phosphorolysis of the thioester bond leading to formation of acetyl phosphate.
A Central Role for the Primitive SLP Pathway in Evolution of Early Metabolic Pathways
The proposed early evolution of the SLP energy-conserving pathway (fig. 2A) reshapes current proposals for the continuing evolution of life and early metabolic pathways (Martin and Russell 2003; Russell and Martin 2004). Key to this reshaping is the transition to a cell (fig. 2A) independent of abiotic surface-catalyzed reactions. The initial event in this transition is the evolution of a primitive ancestor to the extant CdhABCDE complex that evolved catalysis of C-S bond formation to accelerate the geochemical-driven synthesis of CH3COSR from acetic acid and R-SH (step A, fig. 2A) as an energy source. It has been proposed (Huber and Wachtershauser 1997) that CdhABCDE evolved to catalyze the synthesis of CH3COSCH3 from CO and CH3SH for cell carbon, analogous to the priming reaction (broken arrow, fig. 2A) in which both a C-C and C-S bond is formed. Here we modify this concept to propose instead that a primitive Cdh at first evolved only catalysis of C-S bond formation to assist the condensation of acetic acid and R-SH to provide CH3COSR as an energy source (step A, fig. 2A). Further evolution of additional subunits permitted the Cdh to catalyze both C-C and C-S bond formation required for the priming reaction (broken arrow, fig. 2A) characteristic of the extant CdhABCDE complex. However, at this juncture, the primitive cell is still dependent on geochemistry as the sole source of energy (step A, fig. 2A). Thus, the next proposed event is the evolution of enzymes catalyzing steps 1–6 in the extant pathway (fig. 1) which grafted onto the CdhABCDE complex and completely released the primitive cell from dependence on geochemical energy and the surface-catalyzed abiotic synthesis of CH3COSR (fig. 2B). These events coincided with the evolution of enzymes for the synthesis of compounds starting from CH3COSR, feeding the biosynthetic pathways that coevolved earlier with the SLP pathway proposed in figure 2A. In the scenario presented here, this early cell (fig. 2B) was chemoautotrophic which is in fundamental agreement with the chemoautotrophic theory, albeit with four important exceptions. First, the driving force for evolution of the Wood-Ljungdahl pathway was to supply an energy source and only later became essential to supply CH3COSR for chemoautotrophic growth that is a tenet of the chemoautotrophic theory. Further, although H2 has been proposed as the first electron donor in the Wood-Ljungdahl pathway (Russell and Martin 2004), CO is preferred based on the unfavorable thermodynamics (eqs. 3 and 4) with H2 for step 2 in the pathway (fig. 1).
 | (3) |
 | (4) |
). Third, we propose that the chemoautotrophic cell inherited enzyme-catalyzed biosynthetic pathways, which coevolved earlier with the primitive SLP pathway, for the synthesis of complex cellular constituents. Finally, in contrast to the more complex chemiosmotic mechanism espoused for the chemoautotrophic theory, we propose that the first chemoautotrophic cell conserved energy by SLP that drove biosynthesis. Thus, the early evolution of an SLP energy-conserving pathway is proposed to have played a previously unrecognized major role in early evolution.
At this juncture in the early evolution of life, it is proposed that the chemoautotrophic generation of complex biomass would have provided growth substrates for the evolution of primitive heterotrophic organisms that adopted the conversion of acetyl-CoA to acetate for energy conservation. Indeed, the conversion of acetyl-CoA to acetate and ATP is a staple of energy conservation in extant fermentative species from both the Archaea and Bacteria domains (Gottschalk 1985). The vast majority of extant fermentation pathways oxidize a variety of reduced substrates to acetyl-CoA as the common intermediate, consistent with the SLP pathway of chemoautotrophic cells anchoring the evolution of diverse extant fermentations. Included among these fermentations is homoacetogenesis which employs the bacterial version of the Wood-Ljungdahl pathway. Although similar to the archaeal version, the bacterial version depends on ATP for the first step, employs different cofactors, and functions to dispose of electrons generated by oxidation of the substrate by reducing 2CO2 to acetyl-CoA (Gottschalk 1985). Thus, we propose that the bacterial version of the Wood-Ljungdahl pathway evolved later for a purpose different from the archaeal version. The next proposed event is the evolution of ATPase and membrane-bound electron transport from CO to one or more of the reductive steps of the Wood-Ljungdahl pathway (steps 2, 5, or 6; fig. 1) which lead to a chemiosmotic mechanism for ATP synthesis. The grafting of ancestral enzymes catalyzing steps 7–9 (fig. 1) onto steps 1–6 of the ancestral Wood-Ljungdahl pathway are postulated to have evolved the CO2 reduction pathway for methanogenesis (steps 1–9, fig. 1) that is strictly dependent on chemiosmosis for ATP synthesis (Deppenmeier, Muller, and Gottschalk 1996). No longer dependent on SLP, the addition of hydrogenase and abandonment of Pta and Ack lead to the H2-oxidizing CO2-reducing methanogenesis pathway typical of most extant methanoarchaea. Thus, the branched pathway leading to both acetate and methane in figure 1 may represent a relic of evolution which existed at the time of transition from SLP to chemiosmosis that was preserved in the Methanosarcina. Finally, the simple reversal of steps 10–12 (fig. 1) coupled with steps 7–9 is postulated to have evolved the pathway for methanogenesis from acetate (fig. 3) that was produced by fermentative anaerobes (Ferry 2003). Thus, the SLP energy-conserving pathway directed and powered the early evolution of anaerobic energy-yielding pathways that also provided the foundation for evolution of energy-yielding pathways in extant anaerobic and aerobic organisms from all three domains of life.
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In conclusion, an alternative for the early evolution of life is offered that combines principles of the two most popular albeit widely disparate theories. Further, in contrast to both popular theories, it is proposed that the early evolution of a primitive energy-conserving cycle drove and directed the early evolution of fundamental metabolic pathways. The alternative theory reshapes features of the first chemoautotrophic cell predicted by popular theory and explains the origin and evolution of extant methanogenic pathways.
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Acknowledgements |
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This work was supported by Department of Energy Grant No. DE-FG02-95ER20198 (J.G.F.), the National Aeronautics and Space Administration (NASA) Astrobiology Institute (J.G.F. and C.H.H.), and NASA Grant No. NNG05GN50G (C.H.H.).
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Footnotes |
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William Martin, Associate Editor
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References |
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