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Evolution of the structure and impact of Earth’s biosphere

Abstract

Life on Earth has existed for over 3.5 billion years and has caused fundamental changes in Earth’s biogeochemistry. However, the timing and impact of major events in the evolution of the biosphere are hotly contested, owing partially to the inherent difficulty in studying events that occurred in deep time. In this Review, we discuss the evolving structure of Earth’s biosphere and major changes in its capacity to alter geochemical cycles. We describe evidence that oxygenic photosynthesis evolved relatively early, but contend that marine primary productivity was low, surface oxygen was scarce and marine anoxia was prevalent for the majority of Earth’s history. Anoxygenic phototrophs were likely a key part of the marine biosphere in these low-oxygen oceans, and nutrient uptake by these organisms was one factor limiting the extent of marine oxygenic photosynthesis. Moreover, there are potential issues with the commonly held idea that the diversification of eukaryotes fundamentally altered ocean nutrient cycling and transformed the marine biological pump. Furthermore, we argue that terrestrial primary productivity was a substantial mode of biological carbon fixation following the widespread emergence of continental land masses, even before the rise of land plants, impacting carbon cycling on a global scale.

Key points

  • Although marine anoxia persisted for most of Earth’s history, inorganic geochemical information suggests appreciable traces of O2 in Earth’s surface environments hundreds of millions of years before the Great Oxidation Event.

  • Anoxygenic photosynthesis was likely a key metabolism in the early marine biosphere, and the presence of these organisms may have increased nutrient limitation amongst oxygenic phototrophs.

  • Terrestrial microbial mats in the Precambrian could have been responsible for a substantial fraction of global primary productivity.

  • The rise of animals or the rise of algae were not necessarily first-order controls on the nature of Earth’s marine biological carbon pump, but environmental factors could have induced dramatic changes in organic-carbon-remineralization efficiency over time.

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Fig. 1: Estimates of change in atmospheric oxygen, CO2 and isotopic composition of marine carbonates through time.
Fig. 2: Evolution of the structure of the biosphere and its impact on global biogeochemical cycling.
Fig. 3: Modern terrestrial cyanobacterial mats.
Fig. 4: Estimated annual net primary production from terrestrial microbial mats.
Fig. 5: Terrestrial oxygen-flux estimates in a microbial-mat-dominated world.

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Acknowledgements

This work was funded by the NASA Alternative Earths Astrobiology Institute and the David and Lucile Packard Foundation.

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N.J.P. wrote the paper, with input from all authors. All authors contributed substantially to researching data for the article and contributing to the discussion of its content. B.B. produced the estimates of Proterozoic benthic productivity.

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Correspondence to Noah J. Planavsky.

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Glossary

Carbon fixation

The transformation of carbon from inorganic to organic form, particularly carbon dioxide to organic carbon during photosynthesis.

Biotic scope

The relative importance of biological controls on Earth’s surface geochemical processes.

Oxygenic photosynthesis

Photosynthesis that produces free oxygen (O2).

Anoxygenic phototrophs

Microorganisms that capture light energy to produce ATP without oxygen production; water is, thus, not used as an electron donor.

Palaeosols

Ancient soils preserved in sedimentary successions.

Banded iron formations

Iron-rich, chemically precipitated sedimentary rocks characterized by interbedded iron oxides and cherts, found almost exclusively in Proterozoic and earlier sedimentary successions.

Secondary oxidation

Late-stage oxidation occurring after sediment burial and lithification, typically via surface weathering of exposed rock outcrops.

Chemosynthetic primary producers

Producing organic compounds using energy from inorganic chemical reactions, rather than sunlight.

Remineralization

The transformation of compounds from organic to inorganic form, particularly, organic carbon to carbon dioxide.

Photoferrotrophs

Anoxygenic phototrophic microbes that use ferrous iron as their primary electron donor and, in the process, produce ferric iron.

Net primary productivity

Rate at which carbon is fixed and O2 produced via photosynthesis, minus the carbon remineralized and O2 consumed via internal (autotrophic) respiration; equivalent to the net flux of O2 to the atmosphere from primary producers.

Dissimilatory sulfate reduction

The anaerobic respiration of sulfate.

Euxinia

Anoxic and sulfidic water-column conditions.

Ferruginous

Anoxic and iron-rich water-column conditions.

Stem-group

The group of extinct taxa within a clade that diverged prior to the most recent common ancestor of its living representatives.

Redoxcline

A steep, vertical gradient between oxidizing and reducing conditions in a water column.

Gross primary productivity

The rate at which carbon is fixed and O2 produced via photosynthesis, not accounting for internal respiration.

Biological pump

The transport of organic carbon from the surface to deep ocean.

Apatite

A group of calcium-phosphate minerals, which, when formed in marine systems, have the general formula Ca5(PO4)3(F,Cl,OH); the most common mineral form of phosphorous.

Weatherable shell

The uppermost layer of the lithosphere subject to weathering.

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Planavsky, N.J., Crowe, S.A., Fakhraee, M. et al. Evolution of the structure and impact of Earth’s biosphere. Nat Rev Earth Environ 2, 123–139 (2021). https://doi.org/10.1038/s43017-020-00116-w

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