EVOLUTIONARY ASSEMBLY OF CAMBRIAN-MESOZOIC TERRESTRIAL PLANT MICROBIOMES INFERRED FROM METAGENOMIC ANALYSIS OF MODERN ANALOGS

Shotgun metagenomic sequence analyses were conducted for modern, early-diverging host-microbiome systems having fossil analogs ranging in age from Cambrian-Mesozoic times, to represent ancient communities of terrestrial autotrophs and associated bacteria, protists, fungi, and invertebrate animals. Microbiome comparisons based on multiple lines of evidence (multiple taxonomic markers, genomic sequences that mark key functions such as N-fixation and methane oxidation, and correlative microscopy) indicate that terrestrial autotrophs accreted functions of global ecological significance over deep time. Earliest Ordovician-Silurian terrestrial plants, represented by early-diverging mosses and liverworts, likely inherited key microbiome features from Cambrian aquatic-terrestrial streptophyte algae–namely vitamin B₁₂ biosynthesis, N-fixation, methane-oxidation, and partnerships with early-diverging fungi–then added P-mobilizing fungal associates and early-diverging terrestrial micrometazoa (e.g. springtails representing early hexapods). Similar information inferred for Devonian lichens and early vascular plants of the Mesozoic, expands this new window into terrestrial community assembly. Such observations on deep time microbiome community assembly, together with ecological information available for modern systems, can be employed to quantitatively estimate deep time carbon and nitrogen cycle impacts. For example, streptophyte algal-associated methane oxidation has been estimated at 10¹⁴ kg over the past 485 million years, with 10¹⁹ kg added since the rise of wetland mosses by at least 454 Ma. Metagenomic approaches can illuminate the early evolution of terrestrial communities and aid estimation of past, present, and future biogeochemical impacts.