Morphologically diverse organo-sedimentary structures (including microbial mats and stromatolites) provide a palaeobiological record through more than three billion years of Earth history. Since understanding much of the Archaean fossil record is contingent upon proving the biogenicity of such structures, mechanistic interpretations of well-preserved fossil microbialites can reinforce our understanding of their biogeochemistry and distinguish unambiguous biological characteristics in these structures, which represent some of the earliest records of life. Mechanistic morphogenetic understanding relies upon the analysis of geomicrobiological experiments. Herein, we report morphological-biogeochemical comparisons between micromorphologies observed in growth experiments using photosynthetic mats built by the cyanobacterium Coleofasciculus chthonoplastes (formerly Microcoleus) and green anoxygenic phototrophic Chloroflexus spp. (i.e., Coleofasciculus–Chloroflexus mats), and Precambrian organo-sedimentary structures, demonstrating parallels between them. In elevated ambient concentrations of Cu (toxic to Coleofasciculus), Coleofasciculus–Chloroflexus mats respond by forming centimetre-scale pinnacle-like structures (supra-lamina complexities) associated with large quantities of EPS at their surfaces. µPIXE mapping shows that Cu and other metals become concentrated within surficial sheath-EPS-Chloroflexus-rich layers, producing density-differential micromorphologies with distinct fabric orientations that are detectable using X-ray computed micro-tomography (X-ray µCT). Similar micromorphologies are also detectable in stromatolites from the 3.481 Ga Dresser Formation (Pilbara, Western Australia). The cause and response link between the presence of toxic elements (geochemical stress) and the development of multi-layered topographical complexities in organo-sedimentary structures may thus be considered an indicator of biogenicity, being an indisputably biological and predictable morphogenetic response reflecting, in this case, the differential responses of Coleofasciculus and Chloroflexus to Cu. Growth models for microbialite morphogenesis rely upon linking morphology to intrinsic (biological) and extrinsic (environmental) influences. Since the pinnacles of Coleofasciculus–Chloroflexus mats have an unambiguously biological origin linked to extrinsic geochemistry, we suggest that similar micromorphologies observed in ancient organo-sedimentary structures are indicative of biogenesis. An identical Coleofasciculus–Chloroflexus community subjected to salinity stress also produced supra-lamina complexities (tufts) but did not produce identifiable micromorphologies in three dimensions since salinity seems not to negatively impact either organism, and therefore cannot be used as a morphogenetic tool for the interpretation of density-homogeneous micro-tufted mats—for example, those of the 3.472 Ga Middle Marker horizon. Thus, although correlative microscopy is the keystone to confirming the biogenicity of certain Precambrian stromatolites, it remains crucial to separately interrogate each putative trace of ancient life, ideally using three-dimensional analyses, to determine, where possible, palaeoenvironmental influences on morphologies. Widespread volcanism and hydrothermal effusion into the early oceans likely concentrated toxic elements in early biomes. Morphological diversity in fossil microbialites could, therefore, reflect either (or both of) differential exposure to ambient fluids enriched in toxic elements and/or changing ecosystem structure and tolerance to elements through evolutionary time—for example, after incorporation into enzymes. Proof of biogenicity by deducing morphogenesis (i.e., a process preserved in the fossil record) overcomes many of the shortcomings inherent to the proof of biogenicity by descriptions of morphology alone.
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