Archetypal Melanin-Like PAH-Based Multifunctionality at the Origin of Life?

Marco d’Ischia, Paola Manini, Zita Martins, Laurent Remusat, Conel M.O’D. Alexander, Cristina Puzzarini, Vincenzo Barone, Raffaele Saladino

Physics of Life Reviews
Available online 18 March 2021

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“Highlights

• The IOM in chondrites is remarkably similar to the allomelanins in microorganisms.
• Allomelanins can promote phenomena and processes of astrobiological relevance.
• Being similar to allomelanins, IOM may have played a role in the origin of life.”

“An interdisciplinary review of the chemical literature that points to a unifying scenario for the origin of life, referred to as the Primordial Multifunctional organic Entity (PriME) scenario, is provided herein. In the PriME scenario it is suggested that the Insoluble Organic Matter (IOM) in carbonaceous chondrites, as well as interplanetary dust particles from meteorites and comets may have played an important role in the three most critical processes involved in the origin of life, namely 1) metabolism, via a) the provision and accumulation of molecules that are the building blocks of life, b) catalysis (e.g., by templation), and c) protection of developing life molecules against radiation by excited state deactivation; 2) compartmentalization, via adsorption of compounds on the exposed organic surfaces in fractured meteorites, and 3) replication, via deaggregation, desorption and related physical phenomena. This scenario is based on the hitherto overlooked structural and physicochemical similarities between the IOM and the dark, insoluble, multifunctional melanin polymers found in bacteria and fungi and associated with the ability of these microorganisms to survive extreme conditions, including ionizing radiation. The underlying conceptual link between these two materials is strengthened by the fact that primary precursors of bacterial and fungal melanins (collectively referred to herein as allomelanins) are hydroxylated aromatic compounds like homogentisic acid and 1,8-dihydroxynaphthalene, and that similar hydroxylated aromatic compounds, including hydroxynaphthalenes, figure prominently among possible components of the organic materials on dust grains and ices in the interstellar matter, and may be involved in the formation of IOM in meteorites. Inspired by this rationale, a vis-à-vis review of the properties of IOM from various chondrites and non-nitrogenous allomelanin pigments from bacteria and fungi is provided herein. The unrecognized similarities between these materials may pave the way for a novel scenario at the origin of life, in which IOM-related complex organic polymers delivered to the early Earth are proposed to serve as PriME and were preserved and transformed in those primitive forms of life that shared the ability to synthesize melanin polymers playing an important role in the critical processes underlying the establishment of terrestrial eukaryotes.”