A statistical analysis of the carbon isotope record from the Archean to Phanerozoic and implications for the rise of oxygen

Krissansen‐Totton, Joshua; Buick, Roger; Catling, David C.

doi:10.2475/04.2015.01

Cited by 146 publications

(185 citation statements)

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“…PTOX and AOX provide electron drains in the electron transport chains of both systems, and chloroplasts and Prochlorococcus both use chlorophyll b as well as a (6 Our framework has implications for Earth history. If biospheric self-amplification driven by the sun enhanced the burial of organics and carbonates (120,121) simply by increasing their production, it would help explain the drawdown of atmospheric CO2 and the rise of atmospheric O2 across several stages of Earth history (122,123). Perhaps not coincidentally, marine picocyanobacteria are estimated to have emerged near the transition from the Neoproterozoic (1,000-541 Ma) to the Phanerozoic (541 Ma to present) (124,125), when sediments indicate the occurrence of global glaciations (126,127), global carbon cycle perturbations (128)(129)(130), enhanced organic carbon burial (120,121), and a second major rise in atmospheric O2 toward modern levels (123,(131)(132)(133).…”

Section: Emergence Of Mutualism In Oceanic Microbial Ecosystems Finamentioning

confidence: 99%

Metabolic evolution and the self-organization of ecosystems

Braakman

Follows

Chisholm

2017

Proc. Natl. Acad. Sci. U.S.A.

148

169

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Metabolism mediates the flow of matter and energy through the biosphere. We examined how metabolic evolution shapes ecosystems by reconstructing it in the globally abundant oceanic phytoplankter Prochlorococcus. To understand what drove observed evolutionary patterns, we interpreted them in the context of its population dynamics, growth rate, and light adaptation, and the size and macromolecular and elemental composition of cells. This multilevel view suggests that, over the course of evolution, there was a steady increase in Prochlorococcus' metabolic rate and excretion of organic carbon. We derived a mathematical framework that suggests these adaptations lower the minimal subsistence nutrient concentration of cells, which results in a drawdown of nutrients in oceanic surface waters. This, in turn, increases total ecosystem biomass and promotes the coevolution of all cells in the ecosystem. Additional reconstructions suggest that Prochlorococcus and the dominant cooccurring heterotrophic bacterium SAR11 form a coevolved mutualism that maximizes their collective metabolic rate by recycling organic carbon through complementary excretion and uptake pathways. Moreover, the metabolic codependencies of Prochlorococcus and SAR11 are highly similar to those of chloroplasts and mitochondria within plant cells. These observations lead us to propose a general theory relating metabolic evolution to the self-amplification and selforganization of the biosphere. We discuss the implications of this framework for the evolution of Earth's biogeochemical cycles and the rise of atmospheric oxygen. metabolic evolution | Prochlorococcus | microbial oceanography | mutualism | Earth history M etabolism sustains the nonequilibrium chemical order of the biosphere by continually supplying the energy and building blocks of all cells on Earth (1-5). Here we ask: How does cellular metabolic evolution shape the mass and energy flows of ecosystems? The oceanic phytoplankter Prochlorococcus (6), the most abundant photosynthetic cell on Earth (7,8), provides an ideal model system for addressing this question. Prochlorococcus and its deeper-branching sister lineage marine Synechococcus make up the marine picocyanobacteria and have a characteristic biogeography (9). Prochlorococcus "ecotypes" have geographically (10, 11) and seasonally (12) dynamic populations that in warm, stable stratified water columns always return to the same general structure: Recently diverging highlight-adapted (HL) ecotypes are most abundant toward the surface, whereas deeper branching low-light-adapted (LL) ecotypes are most abundant at depth (10-14) (Fig. 1).What selective forces drove this niche partitioning in Prochlorococcus, and what were the consequences for the ocean ecosystem in general? To address these questions, we reconstructed (15, 16) (Fig. 2) the evolution of core metabolism in strains representing the major clades of Prochlorococcus. To interpret the observed patterns, we developed an evolutionary framework that illuminates the driving forces that produc...

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Section: Emergence Of Mutualism In Oceanic Microbial Ecosystems Finamentioning

confidence: 99%

Metabolic evolution and the self-organization of ecosystems

Braakman

Follows

Chisholm

2017

Proc. Natl. Acad. Sci. U.S.A.

148

169

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“…Prior to the evolution of oxygenic photosynthesis, productivity may have been more than 10 times smaller than today, but once oxygenic photosynthesis evolved, it may have only been 5-10 times lower than modern levels throughout the Precambrian Canfield et al, 2006). The presumed constancy of organic carbon burial since at least 3.5 Gyr (Krissansen-Totton et al, 2015) perhaps further supports a continuously high nitrogen demand similar to the modern, exceeding plausible abiotic fluxes. A significant abiotic nitrogen source is further inconsistent with the isotopic record.…”

Section: Was There a Significant Source Of Abiotically Fixed Nitrogen?mentioning

confidence: 99%

The evolution of Earth's biogeochemical nitrogen cycle

Stüeken

Kipp

Koehler

et al. 2016

Earth-Science Reviews

312

287

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Nitrogen is an essential nutrient for all life on Earth and it acts as a major control on biological productivity in the modern ocean. Accurate reconstructions of the evolution of life over the course of the last four billion years therefore demand a better understanding of nitrogen bioavailability and speciation through time. The biogeochemical nitrogen cycle has evidently been closely tied to the redox state of the ocean and atmosphere. Multiple lines of evidence indicate that the Earth"s surface has passed in a non-linear fashion from an anoxic state in the Hadean to an oxic state in the later Phanerozoic. It is therefore likely that the nitrogen cycle has changed markedly over time, with potentially severe implications for the productivity and evolution of the biosphere. Here we compile nitrogen isotope data from the literature and review our current understanding of the evolution of the nitrogen cycle, with particular emphasis on the Precambrian. Combined with recent work on redox conditions, trace metal availability, sulfur and iron cycling on the early Earth, we then use the nitrogen isotope record as a platform to test existing and new hypotheses about biogeochemical pathways that may have controlled nitrogen availability through time. Among other things, we conclude that (a) abiotic nitrogen sources were likely insufficient to sustain a large biosphere, thus favoring an early origin of biological N 2 fixation, (b) evidence of nitrate in the Neoarchean and Paleoproterozoic confirm current views of increasing surface oxygen levels at those times, (c) abundant ferrous iron and sulfide in the midPrecambrian ocean may have affected the speciation and size of the fixed nitrogen reservoir, and (d) nitrate availability alone was not a major driver of eukaryotic evolution.

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“…Further, the activities of O 2 -producing organisms, for example, cyanobacteria, and the rates of organic carbon burial may have changed little across the GOE 6,11 , requiring a significant reduction in the amount or efficiency of O 2 sinks 12 , to cause the rise of O 2 . While this change may be permitted given the carbon isotopic record of organic and inorganic carbon 13 , it remains unclear whether the required increase of organic carbon burial relative to total carbon input to the surficial reservoir could happen within 200-300 Myr-that is, over the timescale of the GOE.…”

mentioning

confidence: 97%

Rise of Earth’s atmospheric oxygen controlled by efficient subduction of organic carbon

2017

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The net flux of carbon between the Earth's interior and exterior, which is critical for redox evolution and planetary habitability, relies heavily on the extent of carbon subduction. While the fate of carbonates during subduction has been studied, little is known about how organic carbon is transferred from the Earth's surface to the interior, although organic carbon sequestration is related to sources of oxygen in the surface environment. Here we use high pressure-temperature experiments to determine the capacity of rhyolitic melts to carry carbon under graphite-saturated conditions in a subducting slab, and thus to constrain the subduction e ciency of organic carbon, the remnants of life, through time. We use our experimental data and a thermodynamic model of CO 2 dissolution in slab melts to quantify organic carbon mobility as a function of slab parameters. We show that the subduction of graphitized organic carbon, and the graphite and diamond formed by reduction of carbonates with depth, remained e cient even in ancient, hotter subduction zones where oxidized carbon subduction probably remained limited. We suggest that immobilization of organic carbon in subduction zones and deep sequestration in the mantle facilitated the rise (∼10 3-5 fold) and maintenance of atmospheric oxygen since the Palaeoproterozoic and is causally linked to the Great Oxidation Event. Our modelling shows that episodic recycling of organic carbon before the Great Oxidation Event may also explain occasional whi s of atmospheric oxygen observed in the Archaean.

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A statistical analysis of the carbon isotope record from the Archean to Phanerozoic and implications for the rise of oxygen

Cited by 146 publications

References 72 publications

Metabolic evolution and the self-organization of ecosystems

Metabolic evolution and the self-organization of ecosystems

The evolution of Earth's biogeochemical nitrogen cycle

Rise of Earth’s atmospheric oxygen controlled by efficient subduction of organic carbon

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