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. Life on Earth has evolved and impacted Earth’s biogeochemistry for more than 3.5 billion years. This Review examines evidence of major events in the composition and structure of Earth’s biosphere, updates existing viewpoints on the impact of these events and argues for new lines of biogeochemical work to be explored. 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. 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.