Biogeochemical signatures through time as inferred from whole microbial genomes

Abstract

Throughout geologic time, a strong feedback has existed between the geosphere and the biosphere; therefore biological evolution and innovation can be linked to the evolution of ancient environments on Earth. Here we deduce geochemical signatures and phylogenetic relationships of prokaryotes from whole genome sequences and use this link to infer geochemical aspects of the biosphere through time. In particular, we have investigated two potential biosignatures for modern and ancient biochemistry: the magnitude of microbial carbon isotopic fractionation, and the use of metals in microbial cells. The distribution of carbon fixation pathways on microbial phylogenies suggests that: (1) both low and moderate carbon isotope fractionation were established quickly in the early evolution of life; and (2) methanotrophic and ethanotrophic metabolisms capable of producing biomass with extreme 13C depletions are not primitive, but rather evolved after the major groups of Prokaryotes had already diverged. The universal importance of the TCA cycle, which results in low carbon isotopic fractionation, indicates it may have evolved especially early making it perhaps the most likely carbon fixation pathway for the last common ancestor (LCA). Low isotopic fractionation by the reductive TCA cycle can be considered consistent with carbon isotope ratios found in 3,800 million year old Isua sediments. Additionally, moderately fractionated biomass from up to 3,500 million years ago can now likely be attributed to carbon fixation by anoxygenic photoautotrophs using the reductive pentose phosphate cycle (Calvin cycle). In addition to carbon, cells require a number of other elements that could potentially provide biosignatures, including bioactive trace metals. We calculated “model metallomes” for 52 prokaryotes based on the number of atoms of trace metals required to express one molecule of each metallo-enzyme coded for in the corresponding genomes. Our results suggest that the use of metals in prokaryotes as a group generally follows the hierarchy: Fe ≫ Zn > Mn ≫ Mo, Co, Cu ≫ Ni > W, V. However, model metallomes vary with metabolism, oxygen tolerance, optimum growth temperature, and phylogeny. The model metallome of methanogens shows a unique metal signature, suggesting that elevated requirements of nickel and tungsten might be translated to the expressed metallome providing a biosignature for methanogenesis. The model metallomes of diazotrophs and cyanobacteria do not show unique signatures; however changes in enzyme expression under some conditions could still translate into a metal biosignature in the expressed cellular metal content. In a separate analysis, we made inferences about the timing of the evolution of individual metallo-enzymes based on their function and occurrence in modern organisms. The results suggest that fluctuations in the redox state of the Earth’s oceans and atmosphere have forced changes in the proportions of metals used in biology. In this model, biological use of copper and molybdenum has developed along with bioavailability; biological use of iron and manganese has developed counter to bioavailability; and biological use of zinc, cobalt, and nickel has not changed significantly through time. Using this technique, we estimated a model metallome for the LCA based on the metallo-enzymes we infer to have been present at that time. This metallome for the LCA differs greatly from one extrapolated from the distribution of model metallomes on microbial phylogenies, supporting the idea that gene loss, metal substitution, and lateral gene transfer have been important in shaping the enzymatic composition of extant organisms.