Biogeochemical signatures through time as inferred from whole microbial genomes

Abstract

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 13 C 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 ӷ Zn > Mn ӷ Mo, Co, Cu ӷ 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 ...

High Molybdenum availability for evolution in a Mesoproterozoic lacustrine environment

“…This implies a high potential for the sequestration of metals as sulphides, a possibility which merits further research. The Stoer Group data are also consistent with evidence for a greater diversity of eukaryotes in marginal marine environments compared with offshore marine environments, which was hypothesized to reflect the scarcity of Mo in offshore waters distant from continental run-off 13 .The availability of trace metals was a key influence on the development of multicellular life 57,64 , and Mo-dependent enzymes in particular are essential to eukaryotic cell biology 57,58,[64][65][66] . The evolution of Mo usage is regarded as a fundamental aspect of the diversification of eukaryotes, probably from 1.5 to 1.0 Ga (ref.…”

“…An important control on high Mo levels ARTICLE in the Stoer Group was the high content of sulphide in the lake water, which reflects a high enough level of atmospheric oxygenation to allow ready weathering of sulphides on the continents 36 and hence the ready availability of sulphate to surface environments in the late Mesoproterozoic. Mo is essential to biological N fixation [57][58][59] , so the record of Mo availability to the Stoer Group lake supports models in which N-fixing cyanobacteria could flourish in the Mesoproterozoic lacustrine environment while being inhibited in the ocean. The high burial rates for Mo in the Stoer Group could be interpreted to imply a high concentration of Mo in the water column, assuming steadystate conditions.…”

Carbonaceous biosignatures of diverse chemotrophic microbial communities from chert nodules of the Ediacaran Doushantuo Formation

“…CO 2 , dissolved inorganic carbon-DIC, CH 4 , acetate) and the metabolic pathway (e.g. phototropy, chemotrophy) of assimilation (House et al, 2003;Zerkle et al, 2005). Thus the carbon isotopic compositions of organic matter and carbonate preserved in sedimentary rocks can be used to infer biological processes and the carbon cycle in geological past (e.g.…”

Inorganic Polyphosphate Modulates TRPM8 Channels

“…Moreover, in the absence of a zinc supply, they were forced to confront unfamiliar minerals, in particular those containing iron. At that time the dominating transition metal ion in sea water would have been Fe 2+ [90,220,221]. Iron, unlike zinc, is redox-active and can generate harmful hydroxyl radicals [222][223][224][225].…”