Nitrogen fixation sustained productivity in the wake of the Palaeoproterozoic Great Oxygenation Event

Luo, Genming; Junium, Christopher K.; Izon, Gareth; Ono, Shuhei; Beukes, Nicolas J.; Algeo, Thomas J.; Cui, Ying; Xie, Shucheng; Summons, Roger E.

doi:10.1038/s41467-018-03361-2

Cited by 53 publications

(28 citation statements)

References 74 publications

(150 reference statements)

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“…These results also suggest that local sources of nitrate may have been exploited by denitrifying microbes, while denitrifiers using nitrite or downstream products would not have proliferated until much later in Earth history, until the mid-Proterozoic, well after the Great Oxidation Event. This finding is consistent with previous geochemical studies that documented isotopic evidence of denitrification in the Neoarchean (Garvin et al, 2009b;Godfrey & Falkowski, 2009;Koehler et al, 2019) and Paleoproterozoic (Zerkle et al, 2017a;Kipp et al, 2018;Luo et al, 2018). Our results suggest that genes involved in nitrate reduction arose by approximately 2.8 Ga, indicating that nitrate was present and used as a metabolic substrate at that time.…”

Section: Discussionsupporting

confidence: 93%

“…The question of how these metabolisms unfolded over Earth's history has previously been addressed with both geochemical and phylogenetics-based approaches. Geochemical approaches, relying on the reconstruction of metabolisms based on the rock record, have suggested that biological nitrogen fixation emerged early (Stüeken et al, 2016a;Koehler et al, 2019;Ossa Ossa et al, 2019) and that the nitrogen cycle expanded considerably during the Neoarchean (2.8-2.5 Ga) and Paleoproterozoic (2.5-1.8 Ga) (Garvin et al, 2009a;Godfrey & Falkowski, 2009;Zerkle et al, 2017a;Kipp et al, 2018;Koehler et al, 2018;Luo et al, 2018).…”

Section: Introductionmentioning

confidence: 99%

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Radiation of nitrogen-metabolizing enzymes across the tree of life tracks environmental transitions in Earth history

Parsons

Stüeken

Rosen

et al. 2020

Preprint

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Nitrogen is an essential element to life and exerts a strong control on global biological productivity. The rise and spread of nitrogen-utilizing microbial metabolisms profoundly shaped the biosphere on the early Earth. Here we reconciled gene and species trees to identify birth and horizontal gene transfer events for key nitrogen-cycling genes, dated with a time-calibrated tree of life, in order to examine the timing of the proliferation of these metabolisms across the tree of life. Our results provide new insights into the evolution of the early nitrogen cycle that expand on geochemical reconstructions. We observed widespread horizontal gene transfer of molybdenum-based nitrogenase back to the early Archean, minor horizontal transfer of genes for nitrate reduction in the Archean, and an increase in the proliferation of genes metabolizing nitrite around the time of the Mesoproterozoic (~1.5 Ga). The latter coincides with recent geochemical evidence for a mid-Proterozoic rise in oxygen levels. Our findings provide important constraints for understanding the evolution of the nitrogen cycle over time and provide insights into the bioavailability of various nitrogen sources in the early Earth with possible implications for the emergence of eukaryotic life.

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Section: Discussionsupporting

confidence: 93%

Section: Introductionmentioning

confidence: 99%

Radiation of nitrogen-metabolizing enzymes across the tree of life tracks environmental transitions in Earth history

Parsons

Stüeken

Rosen

et al. 2020

Preprint

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“…Oxidation of NH 4 + would have been suppressed in an early Archean ocean characterized by extremely low O 2 concentrations (15)(16)(17). Free O 2 is produced through oxygenic photosynthesis, the rate of which is mainly controlled by the concentrations of bioavailable N and phosphorus (P) (19)(20)(21)(22)(23)(24). While the sedimentary δ 15 N record suggests that N was bioavailable and that diazotrophic molybdenum (Mo)-based nitrogenase dominated N 2 fixation in the Mesoarchean, the record also places a robust minimum age for the occurrence of aerobic N cycling at ∼2.72 Ga in the Neoarchean (e.g., refs.…”

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confidence: 99%

Limited oxygen production in the Mesoarchean ocean

Ossa

Hofmann

Spangenberg

et al. 2019

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

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The Archean Eon was a time of predominantly anoxic Earth surface conditions, where anaerobic processes controlled bioessential element cycles. In contrast to “oxygen oases” well documented for the Neoarchean [2.8 to 2.5 billion years ago (Ga)], the magnitude, spatial extent, and underlying causes of possible Mesoarchean (3.2 to 2.8 Ga) surface-ocean oxygenation remain controversial. Here, we report δ15N and δ13C values coupled with local seawater redox data for Mesoarchean shales of the Mozaan Group (Pongola Supergroup, South Africa) that were deposited during an episode of enhanced Mn (oxyhydr)oxide precipitation between ∼2.95 and 2.85 Ga. Iron and Mn redox systematics are consistent with an oxygen oasis in the Mesoarchean anoxic ocean, but δ15N data indicate a Mo-based diazotrophic biosphere with no compelling evidence for a significant aerobic nitrogen cycle. We propose that in contrast to the Neoarchean, dissolved O2levels were either too low or too limited in extent to develop a large and stable nitrate reservoir in the Mesoarchean ocean. Since biological N2fixation was evidently active in this environment, the growth and proliferation of O2-producing organisms were likely suppressed by nutrients other than nitrogen (e.g., phosphorus), which would have limited the expansion of oxygenated conditions during the Mesoarchean.

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“…Nitrogen in sediments is mainly present in two forms, organic‐bound nitrogen and clay‐bound nitrogen (mainly as NH 4 + ) (see reviews in Ader et al, 2016; Stüeken et al, 2016). Clay‐bound NH 4 + is generally sourced from the in situ deamination of organic nitrogen, but in some cases it may have additional origins from terrestrial input and/or diagenetic fluids (e.g., Luo et al, 2018). However, the strong positive correlation between TOC and TN ( R 2 = 0.829) in our samples, paired with a very small intercept on the TN axis (Figure 6b), indicates that the contribution of allochthonous clay‐bound N, if any, was minimal.…”

Section: Discussionmentioning

confidence: 99%

“…Denitrification and anammox preferentially release light 14 N to the atmosphere, rendering the residual nitrate pool in the ocean enriched in heavy 15 N, which, in most cases, would be quantitatively assimilated by photosynthetic organisms. These two processes are responsible for the positive δ 15 N values in modern seawater and sediments (Sigman et al, 2009; Tesdal et al, 2013) and have been widely used to interpret positive δ 15 N values in the geological record (Ader et al, 2014; Algeo et al, 2014; Garvin et al, 2009; Godfrey & Falkowski, 2009; Kipp et al, 2018; Koehler et al, 2017; Luo et al, 2018; Stüeken, 2013; Wang et al, 2013; Wang, Jiang, et al, 2018; Wang, Ling, et al, 2018; Zerkle et al, 2017). It is thus reasonable to infer that they also took effect during the deposition of the Gaoyuzhuang Member III.…”

Section: Discussionmentioning

confidence: 99%

Coupled Nitrate and Phosphate Availability Facilitated the Expansion of Eukaryotic Life at Circa 1.56 Ga

Wang

Shi

et al. 2020

JGR Biogeosciences

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Recent geochemical and paleontological studies have revealed a significant ocean oxygenation episode and an evolutionary leap of eukaryotes at the onset of the Mesoproterozoic. However, the potential role of nitrogen availability and its interaction with other nutrients in these environmental and biological events have not been investigated. Here we present an integrated study of nitrogen isotopes (δ 15 N), organic carbon isotopes (δ 13 C org ), and major and trace element concentrations from Member III of the Gaoyuzhuang Formation in the central North China Craton where the earliest macroscopic multicellular eukaryotic fossils were reported. The enrichments of redox-sensitive elements (Mo, U, and V), coupled with Mo-U covariations, δ 13 C org , and I/(Ca + Mg), indicate that the Gaoyuzhuang Member III in the study area was deposited in largely suboxic-anoxic environments with ephemeral occurrences of euxinia. These data reinforce previous inferences of a strongly redox stratified ocean during the early Mesoproterozoic, but a pulsed oxygenation event may have resulted in deepening of the chemocline. The high δ 15 N values from the study section are interpreted as a result of aerobic N cycling and the presence of a fairly stable nitrate pool in the surface oxic layer, possibly due to the combined effects of oxygenation and low primary productivity. Increased availability of nitrate could have contributed to the expansion of eukaryotic life at this time. However, our data also suggest that nitrate alone was not the only trigger. Instead, this evolutionary leap was likely facilitated by multiple environmental factors, including a rise in O 2 levels and increasing supplies of phosphorus and other bio-essential trace elements.Plain Language Summary The oldest macroscopic eukaryotes (algae) first appeared in ancient oceans about 1.56 billion years ago. Before that, only simple and microscopic fossils have been discovered. The reason behind this evolutionary leap is, however, still puzzling scientists. Here we use multiple proxies to study the change of nutrient and oxygen levels during this critical period. Our results demonstrate the availability of the nutrient nitrogen (in form of nitrate) in the oxic surface ocean owing largely to restrictive consumption by organic carbon decomposition, providing favorable N substance for bio-utilization. Furthermore, we also found evidence for the joint increase of O 2 level, seawater phosphorus, and some bio-essential trace elements along with the occurrence of these earliest algae. Our study provides important clues for untangling the triggers of biological innovation at circa 1.56 Ga.

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Nitrogen fixation sustained productivity in the wake of the Palaeoproterozoic Great Oxygenation Event

Cited by 53 publications

References 74 publications

Radiation of nitrogen-metabolizing enzymes across the tree of life tracks environmental transitions in Earth history

Radiation of nitrogen-metabolizing enzymes across the tree of life tracks environmental transitions in Earth history

Limited oxygen production in the Mesoarchean ocean

Coupled Nitrate and Phosphate Availability Facilitated the Expansion of Eukaryotic Life at Circa 1.56 Ga

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