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Biogeochemical signatures through time as inferred from whole microbial genomes
Open accessAbstract
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.
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In the citing paper
“This work suggests that the utilization of trace metals in biology generally follows the pattern of Fe >> Zn > Mn >> Mo, Co, Cu >> Ni > W, V.”
From Trace elements at the intersection of marine biological and geochemical evolution (2016) · cites this paper as Zerkle et al., 2005
Experimental — accuracy not yet measuredIn the citing paper
“Molybdenum utilization in organisms may have developed in tandem with increasing Mo availability following the early stages of biospheric oxygenation, at which point it became critical to nitrogen fixation (Williams and Frausto da Silva, 2002;2004;Zerkle et al., 2005;Boyd et al., 2011)”
From Trace elements at the intersection of marine biological and geochemical evolution (2016) · cites this paper as Zerkle et al., 2005
In the citing paper
“Inverse modeling based on the utilization of trace elements in metalloenzymes (Zerkle et al., 2005) further supports a strong linkage between evolving ocean chemistry and biological trace element dependency.”
From Trace elements at the intersection of marine biological and geochemical evolution (2016) · cites this paper as Zerkle et al., 2005
In the citing paper
“Initial estimates of Ni concentrations in the early ocean were derived from geochemical modeling (Saito et al., 2003) and microbial genomics (Zerkle et al., 2005). These studies suggested that seawater Ni concentrations were fairly uniform from the Archean through to the modern”
From Trace elements at the intersection of marine biological and geochemical evolution (2016) · cites this paper as Zerkle et al., 2005
In the citing paper
“Zerkle et al. (2005) suggested that since the onset of widespread ocean oxygenation in the Neoproterozoic, the biological utilization of Cu enzymes doubled, likely as a result of increased Cu availability.”
From Trace elements at the intersection of marine biological and geochemical evolution (2016) · cites this paper as Zerkle et al. (2005)
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Metadata
- Authors
- Zerkle, A. L.
- Affiliations
- Pennsylvania State University (US)
- Corresponding author
- Zerkle, A. L.
- ORCID
- Zerkle, A. L.
- Venue
- American Journal of Science
- Publisher
- American Journal of Science (AJS)
- Published
- 2005-06-01
- Volume
- 305
- Issue
- 6-8
- Pages
- 467-502
- ISSN
- 0002-9599 (ISSN-L)
- OpenAlex
- W2165838417
- Cited by
- 223
- References
- 201
- Citations by year
- 2026: 10 · 2025: 6 · 2024: 15 · 2023: 16 · 2022: 9 · 2021: 20 · 2020: 15 · 2019: 17 · 2018: 11 · 2017: 14 · 2016: 12 · 2015: 7 · 2014: 7 · 2013: 8 · 2012: 8
- FWCI
- 3.87
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- American Journal of Science (publishedVersion)
- Newcastle University ePrints (Newcastle Univesity)
- Topics
- Physical Sciences › Physics and Astronomy › Astronomy and Astrophysics › Origins and Evolution of Life
- Physical Sciences › Earth and Planetary Sciences › Paleontology › Paleontology and Stratigraphy of Fossils
- Physical Sciences › Environmental Science › Ecology › Microbial Community Ecology and Physiology
- Keywords
- carbon isotope fractionation, prokaryotic phylogeny, TCA cycle, Calvin cycle, methanogenesis, methanotrophic bacteria, nitrogen-fixing bacteria, cyanobacteria, early evolution of life, last common ancestor
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