Evolutionary roots of plant microbiomes and biogeochemical impacts of nonvascular autotroph-microbiome systems over deep time

Abstract

Since rooted vascular plants rose to dominance, associated microbiota have powerfully influenced global biogeochemistry by mobilizing N and P and otherwise aiding plant health, thereby fostering sequestration of CO2 into coal and soil organics. Less well understood are evolutionary history and biogeochemical roles of microbiomes of ecologically significant nonvascular plants and related algae, whose lineages penetrate more deeply into time. Because analyses of diverse host-microbiome systems indicate that evolutionary history commonly influences microbiome composition and function, we mapped onto a geological time frame biogeochemical features inferred in our previous metagenomic studies of a phylogenetic spectrum of multicellular, freshwater-terrestrial, nonvascular autotroph-microbiome systems: Nostoc commune, representing microbialite-forming cyanobacteria; the Nostoc lichen Peltigera ponojensis; chlorophyte Cladophora glomerata; streptophyte alga Coleochaete pulvinata; moss Sphagnum fimbriatum; and liverwort Conocephalum conicum. Widespread and often abundant today, these species represent ancient lineages of minimal ages ranging from 1450 to 380 Ma, information we used to estimate present global annual magnitudes of organic/inorganic C sequestration, N fixation, and methane oxidation and to calculate biogeochemical impacts during periods from lineage origin to the rise of vascular plants and from lineage origins to present. Functional comparisons indicated that (1) functionally diverse bacterial associates have likely enhanced global C-and N-cycle roles of cyanobacteria for ∼1.5 billion years; (2) by 700–800 Ma, chlorophyte microbiomes retaining ancient functional features (e.g., vitamin B12 biosynthesis and N fixation) had added diverse methane-oxidizing bacteria and eukaryotes, including early metazoans; (3) by ∼500 Ma, streptophyte algal microbiomes possessing ancient functions had incorporated early-diverging fungi; (4) by 450 Ma, microbiomes of early plants included diverse prokaryotes, protists, fungi, and early terrestrial animals; and (5) by 385 Ma, plant microbiomes included P-mobilizing fungi. Autotroph-microbiome systems appear to have accreted functions of global significance over deep time, a new concept that illuminates the early evolution of terrestrial life and that aids modeling past, present, and future biogeochemical impacts.