Methane: Fuel or Exhaust at the Emergence of Life?

Abstract

As many of the methanogens first encountered at hydrothermal vents were thermophilic to hyperthermophilic and comprised one of the lower roots of the evolutionary tree, it has been assumed that methanogenesis was one of the earliest, if not the earliest, pathway to life. It being well known that hydrothermal springs associated with serpentinization also bore abiotic methane, it had been further assumed that emergent biochemistry merely adopted and quickened this supposed serpentinization reaction. Yet, recent hydrothermal experiments simulating serpentinization have failed to generate methane so far, thus casting doubt on this assumption. The idea that the inverse view is worthy of debate, that is, that methanotrophy was the earlier, is stymied by the “fact” that methanotrophy itself has been termed “reverse methanogenesis,” so allotting the methanogens the founding pedigree. Thus, attempting to suggest instead that methanogenesis might be termed reverse methanotrophy would require “unlearning”—a challenge to the subconscious! Here we re-examine the “impossibility” of methanotrophy predating methanogenesis as in what we have termed the “denitrifying methanotrophic acetogenic pathway.” Advantages offered by such thinking are that methane would not only be a fuel but also a ready source of reduced carbon to combine with formate or carbon monoxide—available in hydrothermal fluids—to generate acetate, a target molecule of the first autotrophs. And the nitrate/nitrite required for the putative oxidation of methane with activated NO would also be a ready source of fixed nitrogen for amination reactions. Theoretical conditions for such a putative pathway would be met in a hydrothermal green rust-bearing exhalative pile and associated chimneys subject to proton and electron counter gradients. This hypothesis could be put to test in a high-pressure hydrothermal reaction chamber in which a cool carbonate/nitrate/nitrite-bearing early acidulous ocean simulant is juxtaposed across a precipitate membrane to an alkaline solution of hydrogen and methane. Key Words: Green rust—Methanotrophy—Nitrate reduction—Emergence of life. Astrobiology 17, 1053–1066.

Green Rust: The Simple Organizing &lsquo;Seed&rsquo; of All Life?&nbsp;&nbsp;<strong> </strong>

“…And we alert the reader to a significant revision of the AHV theory since its first proposal, namely that although we still recognize that the job of life overall is to hydrogenate carbon dioxide, it may be that life first captured both the partially and fully reduced forms of C1 carbon as hydrothermal formate and methane, and only later (though well before LUCA) 'learnt' to reduce CO2 through all the required intermediates for CO2 autotrophy to emerge from its mineral placenta. [50, 54,55] At bottom is the assumption that the protonically and electronically powered nanoengines and disequilibrium conversions needed to drive those endergonic reactions required to produce life's many processors and its superstructures today were initially coopted from iron oxyhydroxides and sulfides, dosed with transition metals and phosphate, precipitated at the submarine alkaline vent. [13,280,281,282] However, even in the light of some experimental support we can see no clear path to the nucleotide world and, beyond intriguing suggestions of Greenwell and Coveney and others, the theory dissipates in hypotheses, ideas and speculation.…”

“…But showing how selection for the 'fittest' in this sense can happen, or does happen, in the mineral precipitates is the major challenge? [3,4,55,177] …”

“…However, as the submarine alkaline vent environment offers millimolar-levels of both the fully-reduced carbon end member CH4, as well as the stable fully-oxidized carbon end member CO2, we have formulated a hypothesis involving these feeds from either end of the full C1 redox span to produce activated acetate, the target molecule of the first step to metabolism. [23,24,51,52,53,54,55] This two-path model to activated acetate -an alternative possibility yet to be experimentally tested -has been termed 'denitrifying methanotrophic acetogenesis'. [54] In this model CO2 is reduced to formate or CO with electrons either initially provided by oxidation of FeII as in the experiments mentioned above, or by a reversal of the formate hydrogen lyase reaction.…”

Evidence for non-methanogenic metabolisms in globally distributed archaeal clades basal to theMethanomassiliicoccales

“…The current understanding of methanogenesis evolution is that ancestors of the Euryarchaeota phylum were methanogens (Evans et al , 2019), or potentially methanotrophs or alkanotrophs (Spang et al , 2017), with methanotrophy-driven acetogenesis also being proposed as an early metabolism type (Russell and Nitschke, 2017). It has been suggested that some euryarchaeal lineages, such as the Thermoplasmatales , lost the methanogenesis pathway, while others, such as the Methanomassiliicoccales , retained at least part of the pathway (Evans et al , 2019).…”

Subsurface exolife

“…However, in extreme (e.g. ice and permafrost) environments at ∼ 230 K, the turnover time is predicted to be several orders of magnitude higher(Price and Sowers, 2004).19 In this regard, we caution the reader that it is not yet clear as to whether methane may have served as the energy source or a byproduct of early life(Russell and Nitschke, 2017), and the existence of either methanogens or methanotrophs on subsurface worlds is not guaranteed.…”