On the co‐evolution of surface oxygen levels and animals

Cole, Devon B.; Mills, Daniel B.; Erwin, Douglas H.; Sperling, Erik A.; Porter, Susannah M.; Reinhard, Christopher T.; Planavsky, Noah J.

doi:10.1111/gbi.12382

Cited by 113 publications

(103 citation statements)

References 193 publications

(304 reference statements)

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“…The oxygenation of Earth's ocean‐atmosphere system marks one of the most dramatic transformations in our planet's history. Quantifying both the magnitude and the timing of this biogeochemical change has been the focus of much work over the last few decades and has major implications for our understanding of the relationship between the evolution of the environment and the biosphere (Cole et al, 2020; Lenton et al, 2014; Sperling, Knoll, & Girguis, 2015). More recently, with the widespread implementation of high‐precision analytical techniques, this work has heavily utilized “nontraditional” isotope proxies aimed at reconstructing redox evolution.…”

Section: Introductionmentioning

confidence: 99%

Uranium Isotope Fractionation in Non‐sulfidic Anoxic Settings and the Global Uranium Isotope Mass Balance

Cole

Planavsky

Longley

et al. 2020

Global Biogeochemical Cycles

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Uranium isotopes (238U/235U) have been used widely over the last decade as a global proxy for marine redox conditions. The largest isotopic fractionations in the system occur during U reduction, removal, and burial. Applying this basic framework, global U isotope mass balance models have been used to predict the extent of ocean floor anoxia during key intervals throughout Earth's history. However, there are currently minimal constraints on the isotopic fractionation that occurs during reduction and burial in anoxic and iron‐rich (ferruginous) aquatic systems, despite the consensus that ferruginous conditions are thought to have been widespread through the majority of our planet's history. Here we provide the first exploration of δ238U values in natural ferruginous settings. We measured δ238U in sediments from two modern ferruginous lakes (Brownie Lake and Lake Pavin), the water column of Brownie Lake, and sedimentary rocks from the Silurian‐Devonian boundary that were deposited under ferruginous conditions. Additionally, we provide new δ238U data from core top sediments from anoxic but nonsulfidic settings in the Peru Margin oxygen minimum zone. We find that δ238U values from sediments deposited in all of these localities are highly variable but on average are indistinguishable from adjacent oxic sediments. This forces a reevaluation of the global U isotope mass balance and how U isotope values are used to reconstruct the evolution of the marine redox landscape.

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Section: Introductionmentioning

confidence: 99%

Uranium Isotope Fractionation in Non‐sulfidic Anoxic Settings and the Global Uranium Isotope Mass Balance

Cole

Planavsky

Longley

et al. 2020

Global Biogeochemical Cycles

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“…It should also be noted that some researchers argue for an opposite relationship that the rises in oxygen could have been driven by animals. For example, the metazoans can fundamentally transform the redox balance of modern marine settings by changing the nature of the biological pump (Butterfield, 2018;Cole et al, 2020).…”

Section: Stepwise Oxygenation and Biological Innovationsmentioning

confidence: 99%

The oxygen cycle and a habitable Earth

Huang

Liu

Shen

et al. 2021

Sci. China Earth Sci.

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As an important contributor to the habitability of our planet, the oxygen cycle is interconnected with the emergence and evolution of complex life and is also the basis to establish Earth system science. Investigating the global oxygen cycle provides valuable information on the evolution of the Earth system, the habitability of our planet in the geologic past, and the future of human life. Numerous investigations have expanded our knowledge of the oxygen cycle in the fields of geology, geochemistry, geobiology, and atmospheric science. However, these studies were conducted separately, which has led to onesided understandings of this critical scientific issue and an incomplete synthesis of the interactions between the different spheres of the Earth system. This review presents a five-sphere coupled model of the Earth system and clarifies the core position of the oxygen cycle in Earth system science. Based on previous research, this review comprehensively summarizes the evolution of the oxygen cycle in geological time, with a special focus on the Great Oxidation Event (GOE) and the mass extinctions, as well as the possible connections between the oxygen content and biological evolution. The possible links between the oxygen cycle and biodiversity in geologic history have profound implications for exploring the habitability of Earth in history and guiding the future of humanity. Since the Anthropocene, anthropogenic activities have gradually steered the Earth system away from its established trajectory and had a powerful impact on the oxygen cycle. The human-induced disturbance of the global oxygen cycle, if not controlled, could greatly reduce the habitability of our planet.

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“…Despite deoxygenation tolerance in some species, overall, sponge diversity and abundance is likely limited by seasonal anoxia (20). Growth and reproduction may be impacted by seasonal anoxia because collagen synthesis is oxygen dependent; however it is still possible in very low oxygen concentrations (see 99). Sponge larvae may also require elevated oxygen due to their motility.…”

Section: Potential Adaptations Of the Sponge Host To Seasonal Anoxiamentioning

confidence: 99%

The effects of seasonal anoxia on the microbial community structure in demosponges in a marine lake (Lough Hyne, Ireland)

Schuster

Strehlow

Eckford-Soper

et al. 2020

Preprint

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Climate change is expanding marine oxygen minimum zones (OMZs), while anthropogenic nutrient input depletes oxygen concentrations locally. The effects of deoxygenation on animals are generally detrimental; however, some sponges (Porifera) exhibit hypoxic and anoxic tolerance through currently unknown mechanisms. Sponges harbor highly specific microbiomes, which can include microbes with anaerobic capabilities. Sponge-microbe symbioses must also have persisted through multiple anoxic/hypoxic periods throughout Earth history. Since sponges lack key components of the hypoxia-inducible factor (HIF) pathway responsible for hypoxic responses in other animals, it was hypothesized that sponge tolerance to deoxygenation may be facilitated by its microbiome. To test this hypothesis, we determined the microbial composition of sponge species tolerating seasonal anoxia and hypoxia in situ in a semi-enclosed marine lake, using 16S rRNA amplicon sequencing. We discovered a high degree of cryptic diversity among sponge species tolerating seasonal deoxygenation, including at least nine encrusting species of the orders Axinellida and Poecilosclerida. Despite significant changes in microbial community structure in the water, sponge microbiomes were species specific and remarkably stable under varied oxygen conditions, though some symbiont sharing occurred under anoxia. At least three symbiont combinations, all including large populations of Thaumarchaeota, corresponded with deoxygenation tolerance, and some combinations were shared between distantly related hosts. We propose hypothetical host-symbiont interactions following deoxygenation that could confer deoxygenation tolerance.ImportanceThe oceans have an uncertain future due to anthropogenic stressors and an uncertain past that is becoming clearer with advances in biogeochemistry. Both past and future oceans were, or will be, deoxygenated compared to present conditions. Studying how sponges and their associated microbes tolerate deoxygenation provides insights into future marine ecosystems. Moreover, sponges form the earliest branch of the animal evolutionary tree and they likely resemble some of the first animals. We determined the effects of variable environmental oxygen concentrations on the microbial communities of several demosponge species during seasonal anoxia in the field. Our results indicate that anoxic tolerance in some sponges may depend on their symbionts, but anoxic tolerance was not universal in sponges. Therefore, some sponge species could likely outcompete benthic organisms like corals in future, reduced-oxygen ecosystems. Our results support the molecular evidence that sponges and other animals have a Neoproterozoic origin, and that animal evolution was not limited by low-oxygen conditions.

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On the co‐evolution of surface oxygen levels and animals

Cited by 113 publications

References 193 publications

Uranium Isotope Fractionation in Non‐sulfidic Anoxic Settings and the Global Uranium Isotope Mass Balance

Uranium Isotope Fractionation in Non‐sulfidic Anoxic Settings and the Global Uranium Isotope Mass Balance

The oxygen cycle and a habitable Earth

The effects of seasonal anoxia on the microbial community structure in demosponges in a marine lake (Lough Hyne, Ireland)

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