On the Origin of Heterotrophy

doi:10.1016/j.tim.2015.10.003

Trends in Microbiology

Volume 24, Issue 1, January 2016, Pages 12-25

https://doi.org/10.1016/j.tim.2015.10.003 Get rights and content

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The physiology of anaerobic autotrophs is rich in exergonic, H₂-dependent CO₂ reductions and transition metal catalysis, properties shared with spontaneous chemical reactions at hydrothermal vents. If the first cells were autotrophs, how did the first heterotrophs arise?

By dry weight, modern cells are made mostly of protein (∼55%) and RNA (∼25%). A diet of that type was, we propose, the carbon and energy source for the first heterotrophs.

Clostridial-type amino acid and purine fermentations as well as sulfur-dependent fermentations of anaerobic archaea might hold clues about the physiology of the first heterotrophs.

At the high H₂ partial pressures of vents, anaerobic amino acid synthesis is exergonic. Amino acid fermentations can thus only have arisen at low H₂ partial pressures, for example in an extinguished vent or in accumulated cell sediments.

The theory of autotrophic origins of life posits that the first cells on Earth satisfied their carbon needs from CO₂. At hydrothermal vents, spontaneous synthesis of methane via serpentinization links an energy metabolic reaction with a geochemical homologue. If the first cells were autotrophs, how did the first heterotrophs arise, and what was their substrate? We propose that cell mass roughly similar to the composition of Escherichia coli was the substrate for the first chemoorganoheterotrophs. Amino acid fermentations, pathways typical of anaerobic clostridia and common among anaerobic archaea, in addition to clostridial type purine fermentations, might have been the first forms of heterotrophic carbon and energy metabolism. Ribose was probably the first abundant sugar, and the archaeal type III RubisCO pathway of nucleoside monophosphate conversion to 3-phosphoglycerate might be a relic of ancient heterotrophy. Participation of chemiosmotic coupling and flavin-based electron bifurcation – a soluble energy coupling process – in clostridial amino acid and purine fermentations is consistent with an autotrophic origin of both metabolism and heterotrophy, as is the involvement of S⁰ as an electron acceptor in the facilitated fermentations of anaerobic heterotrophic archaea.

Section snippets

Autotrophic Origins

Views on the earliest phases of evolution fall into two main camps: autotrophic origins vs. heterotrophic origins. Theories for autotrophic origins posit that the first cells satisfied their carbon needs from CO₂ 1, 2 while heterotrophic origin theories have it that the first cells lived from the fermentations of reduced organic compounds present in some kind of rich organic soup [3]. The heteotrophic origin theory, while traditionally favored by chemists [4], has two main drawbacks. Seen from

Cells: Much Better than Stardust and Mostly Protein

A logical consequence of autotrophic origins is that anaerobic autotrophs were not only the ancestors of the first heterotrophs, they were also the first viable substrate for heterotrophic growth (Box 1). Critics might interject that there were huge amounts of reduced carbon compounds delivered to Earth from space [35], and that such material also could have served as viable substrate for heterotrophs. Organics from space unquestionably did accumulate on the early Earth, but could they have

Amino Acid Fermentations: Bacteria

In bacteria, fermentations of the 20 proteinogenic amino acids involve their degradation to ammonia, CO₂, acetate, short-chain fatty acids, aromatic acids, and small amounts of H₂ [41]. Energy is conserved via substrate-level phosphorylation (SLP) and via phosphorylation driven by an electrochemical Na⁺ gradient (ion-gradient phosphorylation). In the Stickland reaction, carried out by Clostridium sporogenes [42], amino acids are fermented pairwise, one is oxidized and the other is reduced [43].

Amino Acid Fermentations: Archaea

Among the archaea, amino acid fermentation is widespread within the Thermococcales (euryarchaeotes) [56] and within the Thermoproteales (crenarchaeotes) [57]. Archaeal amino acid fermenters very often utilize elemental sulfur (S⁰) as a terminal electron acceptor 57, 58, 59. In these facilitated fermentations, S⁰ affords the microbe an easy means of maintaining redox balance, but ties growth to environments where S⁰ is available (geologically active habitats, for example). The overall scheme for

Hydrogen, Heterotrophy, and Shifting Equilibria

The thermodynamic favorability of fermentations depends upon environmental conditions. Under hydrothermal vent conditions (high H₂ partial pressures and moderate temperatures in the range of 50–70 °C), amino acid synthesis from NH₃, CO₂, and H₂ is exergonic 21, 71, 72. That is a strong argument in favor of autotrophic origins in the first place because the synthesis of the main building blocks of life had to be thermodynamically favorable. But that leads to an apparent paradox: the first

How Do Purine and Pyrimidine Fermentations Work?

Many bacteria are known that can satisfy their carbon, energy, and nitrogen needs from purines alone under anaerobic conditions 41, 82, 83. Only in comparatively few cases are the overall reaction and the exact energy balance known. One example is Clostridium acidiurici, the overall energy metabolic reaction of which, while growing on uric acid, is given by:C₅N₄H₄O₃ + 5.5 H₂O + 4 H⁺ → 0.75 CH₃COO^– + 3.5 CO₂ + 4 NH₄⁺ + 0.75 H⁺with ΔG_o’ = –144 kJ per mol uric acid and an energy yield of 1.25 mol ATP per mol uric

Ribose, the First Abundant Sugar

A prokaryote is about 20% by weight RNA (Table 1), and RNA is about 40% by weight ribose, meaning that a cell is roughly 8% pure ribose. This suggests that ribose clearly would have been among the most, if not the most, abundant early sugar substrate for fermentation. Ribose is indeed an excellent, energy-rich substrate for fermentations and it is furthermore central to many pathways in autotrophic metabolism (including nucleoside and RNA synthesis), meaning that the first autotrophs were

Diversity of C6 Metabolism Suggests That It Came Late

Although glycolysis is often called a universally conserved pathway [8], it is not universally conserved by any means, especially when archaea are considered. There are deep differences in sugar and sugar phosphate metabolism between bacteria and archaea 90, 93, 96. The diversity of nonphosphorylated and phosphorylated C6 sugar metabolism both within archaea and across the archaea–bacteria divide 90, 93, 96, entailing long lists of unrelated and independently arisen enzymes, suggests that C6

Surprising Type III RubisCO

A very intriguing aspect of the origin of heterotrophy concerns archaeal type III RubisCO (ribulose-1,5-bisphosphate carboxylase/oxygenase). The enzyme, long a mystery in archaeal genomes, was recently shown to catalyze the last step in a short pathway (Figure 1D), sometimes encoded in a small gene cluster, that converts nucleotides into 3-phosphoglycerate 102, 103, 104. The first enzyme in the pathway cleaves the nucleotide via phosphorolysis to release the base (a fermentable substrate in the

Concluding Remarks

Anaerobic autotrophs that use the acetyl-CoA pathway – acetogens and methanogens – are a simple, stable, and ‘down to Earth’ starting point for the further evolution of microbial physiology. Fermentations were possibly the next step in physiological evolution (see Outstanding Questions) because a minimum of biochemical invention was required to harness the rich reserves of carbon and energy that cells harbor. But for thermodynamic reasons, heterotrophy had to evolve at much lower H₂ partial

Acknowledgments

We thank Volker Müller, Harold Drake, Gerhard Gottschalk, Bernhard Schink, and Jan Andreesen for advice, Georg Fuchs and Rolf Thauer for extensive comments on an earlier draft, Jan Amend and Tom McCollom for permission to summarize their published data in Table 2, Filipa L. Sousa for many helpful discussions, Verena Zimorski for help in preparing the manuscript, the DFG (P.S., W.B.) and the ERC (W.F.M.) for funding.

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Trends in Microbiology

ReviewOn the Origin of Heterotrophy

Trends

Section snippets

Autotrophic Origins

Cells: Much Better than Stardust and Mostly Protein

Amino Acid Fermentations: Bacteria

Amino Acid Fermentations: Archaea

Hydrogen, Heterotrophy, and Shifting Equilibria

How Do Purine and Pyrimidine Fermentations Work?

Ribose, the First Abundant Sugar

Diversity of C6 Metabolism Suggests That It Came Late

Surprising Type III RubisCO

Concluding Remarks

Acknowledgments

Phys. Life Rev.

Prog. Biophys. Mol. Biol.

J. Biol. Chem.

Biochim. Biophys. Acta

Geochim. Cosmochim. Acta

Cell

Biochim. Biophys. Acta

Biochim. Biophys. Acta

Methods Enzymol.

Curr. Opin. Microbiol.

J. Biol. Chem.

Curr. Opin. Microbiol.

FEBS Lett.

Curr. Opin. Microbiol.

Fructose 1,6-bisphosphate aldolase/phosphatase may be an ancestral gluconeogenic enzyme

Nature

Alternative pathways of carbon dioxide fixation: insights into the early evolution of life?

Annu. Rev. Microbiol.

Some like it hot, but not the first biomolecules

Science

The implausibility of metabolic cycles on the prebiotic earth

PLoS Biol.

RNA evolution and the origins of life

Nature

Common origins of RNA, protein and lipid precursors in a cyanosulfidic protometabolism

Nat. Chem.

Non-enzymatic glycolysis and pentose phosphate pathway-like reactions in a plausible Archean ocean

Mol. Syst. Biol.

Prebiotic cytosine synthesis: a critical analysis and implications for the origin of life

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

Miller-Urey and beyond: what have we learned about prebiotic organic synthesis reactions in the past 60 years?

Annu. Rev. Earth Planet. Sci.

Submarine hydrothermal vents and associated gradient environments as sites for the origin and evolution of life

Orig. Life Evol. Biosph.

The emergence of life from iron monosulphide bubbles at a submarine hydrothermal redox and pH front

J. Geol. Soc. London

On the origin of biochemistry at an alkaline hydrothermal vent

Philos. Trans. R. Soc. Lond. B: Biol. Sci.

The origin of life: look up and look down

Astrobiology

Pathways for abiotic organic synthesis at submarine hydrothermal fields

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

Serpentinization, carbon and deep life

Rev. Mineral. Geochem.

Serpentinites, hydrogen, and life

Elements

Energetics of biomolecule synthesis on early Earth

Environmental genomics reveals a single-species ecosystem deep within Earth

Science

A hydrogen-based subsurface microbial community dominated by methanogens

Nature

Acetogenesis in deep subseafloor sediments of the Juan de Fuca Ridge flank: a synthesis of geochemical, thermodynamic, and gene-based evidence

Geomicrobiol. J.

Autotrophic carbon fixation in archaea

Nat. Rev. Microbiol.

Abiogenic hydrocarbon production at Lost City Hydrothermal Field

Science

Archean (3.33 Ga) microbe-sediment systems were diverse and flourished in a hydrothermal context

Geology

Evidence from fluid inclusions for microbial methanogenesis in the early archaean era

Nature

Archaeal phylogenomics provides evidence in support of a methanogenic origin of the Archaea and a thaumarchaeal origin for the eukaryotes

Proc. R. Soc. Lond. B

The two-domain tree of life is linked to a new root for the Archaea

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

Review
On the Origin of Heterotrophy

Bio-inspired CO₂ conversion by iron sulfide catalysts under sustainable conditions