Ideas and perspectives: Development of nascent autotrophic carbon fixation systems in various redox conditions of the fluid degassing on early Earth

Abstract

Abstract. The origin and development of the primary autotrophic metabolism on early Earth were influenced by the two main regimes of degassing of the Earth – reducing (predominance CH4) and oxidative (CO2). Among the existing theories of the autotrophic origin of life in hydrothermal environments, CO2 is usually considered to be the carbon source for nascent autotrophic metabolism. However, the ancestral carbon used in metabolism may have been derived from CH4 if the outflow of magma fluid to the surface of the Earth consisted mainly of methane. In such an environment, the primary autotrophic metabolic systems had to be methanotrophic. Due to the absence of molecular oxygen in the Archean conditions, this metabolism would have been anaerobic; i.e., oxidation of methane must be realized by inorganic high-potential electron acceptors. In light of the primacy and prevalence of CH4-dependent metabolism in hydrothermal systems of the ancient Earth, we propose a model of carbon fixation where the methane is fixed or transformed in a sequence of reactions in an autocatalytic methane–fumarate cycle. Nitrogen oxides are thermodynamically the most favorable among possible oxidants of methane; however, even the activity of oxygen created by mineral buffers of iron in hydrothermal conditions is sufficient for methanotrophic acetogenesis. The hydrothermal system model is considered in the form of a phase diagram, which demonstrates the area of redox and P and T conditions favorable for the development of the primary methanotrophic metabolism.

Chemical Basis of Carbon Fixation Autotrophic Paleometabolism

“…The initiating step in the anaerobic oxidation of both aromatic and aliphatic hydrocarbons is their binding with fumarate (Haynes and Gonzalez, 2014), and the reaction of methane with fumarate С 4 Н 4 О 4 (fumarate) + СН 4 = С 5 Н 8 О 4 (2-methylsuccinate) satisfies the energy requirements for autotrophic growth (Thauer and Shima 2008;Beasley and Nunny, 2012;Averesch and Kracke, 2018). This suggests the possibility of its participation in the incipient autotrophic metabolism (Marakushev and Belonogova, 2019), precisely within the above-discussed universal "chemical space" of intermediates: carboxy-and α-keto acids.…”

“…Let us consider the construction of a metabolic network that combines a part of the above universal core of paleometabolism (sequence of the TCA cycle) (Fig. 1), with the supposed methano-fumarate (MF) cycle (Marakushev and Belonogova, 2019), as a model of methanotrophic metabolism (Fig. 3), which origi-…”