Energy metabolism in anaerobic eukaryotes and Earth's late oxygenation

Abstract

Eukaryotes arose about 1.6 billion years ago, at a time when oxygen levels were still very low on Earth, both in the atmosphere and in the ocean. According to newer geochemical data, oxygen rose to approximately its present atmospheric levels very late in evolution, perhaps as late as the origin of land plants (only about 450 million years ago). It is therefore natural that many lineages of eukaryotes harbor, and use, enzymes for oxygen-independent energy metabolism. This paper provides a concise overview of anaerobic energy metabolism in eukaryotes with a focus on anaerobic energy metabolism in mitochondria. We also address the widespread assumption that oxygen improves the overall energetic state of a cell. While it is true that ATP yield from glucose or amino acids is increased in the presence of oxygen, it is also true that the synthesis of biomass costs thirteen times more energy per cell in the presence of oxygen than in anoxic conditions. This is because in the reaction of cellular biomass with O2, the equilibrium lies very far on the side of CO2. The absence of oxygen offers energetic benefits of the same magnitude as the presence of oxygen. Anaerobic and low oxygen environments are ancient. During evolution, some eukaryotes have specialized to life in permanently oxic environments (life on land), other eukaryotes have remained specialized to low oxygen habitats. We suggest that the Km of mitochondrial cytochrome c oxidase of 0.1–10 μM for O2, which corresponds to about 0.04%–4% (avg. 0.4%) of present atmospheric O2 levels, reflects environmental O2 concentrations that existed at the time that the eukaryotes arose.

Anaerobic metabolism of Foraminifera thriving below the seafloor

“…4c). Under conditions of prolonged anaerobiosis, propionate is preferentially formed as opposed to succinate in anaerobic mitochondria, whereby one additional ATP and one CO 2 are formed from D-methylmalonyl-CoA via propionyl-CoA carboxylase ( 41, 42 ). We detected expression of a Foraminifera ORF with similarity to propionyl-CoA carboxylase at 28 cmbsf (data not shown) indicating that prolonged anoxic conditions stimulate production of propionate in Foraminifera mitochondria.…”

“…A key intermediate in the anaerobic energy metabolism of most eukaryotes is malate ( 41, 42 ). During anaerobic respiration in many eukaryotes malate is converted to fumarate via the enzyme fumarase running in reverse, and the resulting fumarate then can be used as the terminal electron acceptor ( 41, 42 ).…”

“…A key intermediate in the anaerobic energy metabolism of most eukaryotes is malate ( 41, 42 ). During anaerobic respiration in many eukaryotes malate is converted to fumarate via the enzyme fumarase running in reverse, and the resulting fumarate then can be used as the terminal electron acceptor ( 41, 42 ). This fumarate reduction is coupled to an anaerobic electron transport chain in which electrons are transferred from NADH to fumarate via a specialized complex I and a mitochondrial membrane associated fumarate reductase ( 41, 42 ).…”

“…During anaerobic respiration in many eukaryotes malate is converted to fumarate via the enzyme fumarase running in reverse, and the resulting fumarate then can be used as the terminal electron acceptor ( 41, 42 ). This fumarate reduction is coupled to an anaerobic electron transport chain in which electrons are transferred from NADH to fumarate via a specialized complex I and a mitochondrial membrane associated fumarate reductase ( 41, 42 ). This physiology is typical of anaerobic mitochondria, that exist in the Foraminifera species Valvulineria and Gromia , and are widely distributed amongst eukaryotes including Bivalvia, Polychaeta, Platyhelminthes, Nematoda, Euglenida, and Ciliophora ( 41 ).…”

Debating Eukaryogenesis—Part 2: How Anachronistic Reasoning Can Lure Us into Inventing Intermediates

“…Martin and co‐workers make some very interesting points regarding aerobic (mitochondrial) metabolism. [ 27 ] First of all, they stress the fact that the much‐lauded efficiency gained using O 2 as the final acceptor comes at a steep price, because O 2 is such a strong electron acceptor. Recalculating energy efficiency in that respect shows alternative acceptors in a more favorable light.…”