Co-evolution of eukaryotes and ocean oxygenation in the Neoproterozoic era

Lenton, Timothy M.; Boyle, Richard A.; Poulton, Simon W.; Shields, Graham A.; Butterfield, Nicholas J.

doi:10.1038/ngeo2108

Cited by 341 publications

(278 citation statements)

References 98 publications

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“…It has been proposed that marine sponges may have played a vital role in the removal of phosphate to marine sediment and the expansion of the oxic zone at the ocean bottom, eventually paving the way for animal evolution (34). Based on our findings, microbial symbionts in sponges may have made significant contributions to this benthic P cycle in early Earth history.…”

Section: Sponge Samplesupporting

confidence: 59%

Phosphorus sequestration in the form of polyphosphate by microbial symbionts in marine sponges

Zhang

Blasiak

Karolin

et al. 2015

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

127

112

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Marine sponges are major habitat-forming organisms in coastal benthic communities and have an ancient origin in evolution history. Here, we report significant accumulation of polyphosphate (polyP) granules in three common sponge species of the Caribbean coral reef. The identity of the polyP granules was confirmed by energy-dispersive spectroscopy (EDS) and by the fluorescence properties of the granules. Microscopy images revealed that a large proportion of microbial cells associated with sponge hosts contained intracellular polyP granules. Cyanobacterial symbionts cultured from sponges were shown to accumulate polyP. We also amplified polyphosphate kinase (ppk) genes from sponge DNA and confirmed that the gene was expressed. Based on these findings, we propose here a potentially important phosphorus (P) sequestration pathway through symbiotic microorganisms of marine sponges. Considering the widespread sponge population and abundant microbial cells associated with them, this pathway is likely to have a significant impact on the P cycle in benthic ecosystems.phosphorus sequestration | sponge | microbial symbionts | polyphosphate

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Section: Sponge Samplesupporting

confidence: 59%

Phosphorus sequestration in the form of polyphosphate by microbial symbionts in marine sponges

Zhang

Blasiak

Karolin

et al. 2015

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

127

112

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“…Geochemical estimates of atmospheric pO 2 levels during the Proterozoic before the emergence and ecological expansion of metazoan life span orders of magnitude, from less than 0.1% PAL (11) to ∼10% PAL (18,19). Estimates thus span levels well below what active aerobic metazoans would have been able to tolerate on long timescales to values well above those that should be required for animal respiration (Fig.…”

Section: Significancementioning

confidence: 99%

Earth’s oxygen cycle and the evolution of animal life

Reinhard

Planavsky

Olson

et al. 2016

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

227

153

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The emergence and expansion of complex eukaryotic life on Earth is linked at a basic level to the secular evolution of surface oxygen levels. However, the role that planetary redox evolution has played in controlling the timing of metazoan (animal) emergence and diversification, if any, has been intensely debated. Discussion has gravitated toward threshold levels of environmental free oxygen (O 2 ) necessary for early evolving animals to survive under controlled conditions. However, defining such thresholds in practice is not straightforward, and environmental O 2 levels can potentially constrain animal life in ways distinct from threshold O 2 tolerance. Herein, we quantitatively explore one aspect of the evolutionary coupling between animal life and Earth's oxygen cycle-the influence of spatial and temporal variability in surface ocean O 2 levels on the ecology of early metazoan organisms. Through the application of a series of quantitative biogeochemical models, we find that large spatiotemporal variations in surface ocean O 2 levels and pervasive benthic anoxia are expected in a world with much lower atmospheric pO 2 than at present, resulting in severe ecological constraints and a challenging evolutionary landscape for early metazoan life. We argue that these effects, when considered in the light of synergistic interactions with other environmental parameters and variable O 2 demand throughout an organism's life history, would have resulted in long-term evolutionary and ecological inhibition of animal life on Earth for much of Middle Proterozoic time (∼1.8-0.8 billion years ago).oxygen | animals | evolution | Proterozoic A long-standing and pervasive view is that there have been intimate mechanistic links between the evolution of complex life on Earth-in other words, the emergence and ecological expansion of eukaryotic cells and their aggregation into multicellular organisms-and the secular evolution of ocean−atmosphere oxygen levels (1). Molecular oxygen (O 2 ) is by far the most energetic of the abundant terminal oxidants used in biological metabolism (e.g., ref.2). When this energetic capacity is harnessed by mitochondria in eukaryotic cells, the energy flux supported by a given genome size increases by a factor of ∼8,000 (3), potentially paving the way for increased complexity at the cellular level (but see ref. 4). Oxygen is also a crucial component of enzymatic pathways leading to the synthesis of regulatory membrane lipids (5) and structural proteins (6) in eukaryotic organisms and provides a powerful shield against solar UV radiation at Earth's surface through stratospheric ozone production. Furthermore, O 2 is the only respiratory electron acceptor that can meet the metabolic demands required for attaining the large sizes and active lifestyles characteristic of metazoan life (e.g., ref. 7). There is thus ample support for the view that Earth's oxygen cycle provided a crucial evolutionary and ecological constraint on the road to increased biotic complexity, both at the cellular level and on the road ...

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“…The temporal correlation between oxygenation, a succession of low-latitude glaciations (Hoffman et al, 1998), and the rise of architecturally complex life (Marshall, 2006;Narbonne, 2005) invites many hypotheses proposing cause-and-effect relationships between these events (Butterfield, 2009;Lenton et al, 2014;Sperling et al, 2013), but so far no single compelling story exists. A high-resolution record of nitrogen isotope ratios across Neoproterozoic glaciations is lacking, and so possible linkages between these events and the evolution of the nitrogen cycle are unknown.…”

Section: Neoproterozoic (10-05 Gyr)mentioning

confidence: 99%

The evolution of Earth's biogeochemical nitrogen cycle

Stüeken

Kipp

Koehler

et al. 2016

Earth-Science Reviews

315

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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Co-evolution of eukaryotes and ocean oxygenation in the Neoproterozoic era

Cited by 341 publications

References 98 publications

Phosphorus sequestration in the form of polyphosphate by microbial symbionts in marine sponges

Phosphorus sequestration in the form of polyphosphate by microbial symbionts in marine sponges

Earth’s oxygen cycle and the evolution of animal life

The evolution of Earth's biogeochemical nitrogen cycle

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