Nitrate limitation in early Neoproterozoic oceans delayed the ecological rise of eukaryotes

Abstract

The early Neoproterozoic Era witnessed the initial ecological rise of eukaryotes at ca. 800 Ma. To assess whether nitrate availability played an important role in this evolutionary event, we measured nitrogen isotope compositions (δ 15 N) of marine carbonates from the early Tonian (ca. 1000 Ma to ca. 800 Ma) Huaibei Group in North China. The data reported here fill a critical gap in the δ 15 N record and indicate nitrate limitation in early Neoproterozoic oceans. A compilation of Proterozoic sedimentary δ 15 N data reveals a stepwise increase in δ 15 N values at ~800 Ma. Box model simulations indicate that this stepwise increase likely represents a ~50% increase in marine nitrate availability. Limited nitrate availability in early Neoproterozoic oceans may have delayed the ecological rise of eukaryotes until ~800 Ma when increased nitrate supply, together with other environmental and ecological factors, may have contributed to the transition from prokaryote-dominant to eukaryote-dominant marine ecosystems.

Emergence ofProchlorococcusin the Tonian oceans and the initiation of Neoproterozoic oxygenation

“…This is supported through the biomarker record, which indicates a dominance of cyanobacterial primary production until after the Sturtian glaciation (Brocks, 2018). It is also supported by the Tonian N-isotope record, which implies a limited contribution from nitrate assimilation to primary production at this time (Kang et al, 2023). Importantly, the adaptation of the Prochlorococcus LCA to lower-light would also allow it to better compete with low-light adapted anoxygenic phototrophs that would likely have populated anoxic regions of the Tonian euphotic zone with strong potential to cause ocean oxygenation (Johnston et al, 2009a; Jones et al, 2015; Ozaki et al, 2019).…”

Tonian Carbonates Record Phosphate‐Rich Shallow Seas

“…Thermodynamic considerations suggest that ammonia probably dominated the fixed-N pool through the Archean and perhaps much of the Proterozoic (Fennel et al, 2005;Ward et al, 2021), but models predict that before the emergence of the "modern" oxidative N-cycle, initial increases in O 2 would have first promoted N-limitation as ammonia was efficiently converted to nitrite/nitrate, and eventually reduced to N 2 gas (Fennel et al, 2005). Consistent with this, available sedimentary N-isotope data do appear to record an oxidative signal through the later Tonian, which may reflect an increasing importance of oxidative N-cycling, but further work is required to constrain the availability of fixed N to the Tonian biosphere (Kang et al, 2023). Nevertheless, if increasing oxygenation caused N-limitation to spread beyond shallow water settings, then a literal reading of shale and carbonate records indicates that this progressed through the late Tonian, culminating in a pronounced decrease in shale-hosted TOC concentrations coincident with a precipitous rise in bulk P concentration just prior to the onset of the Sturtian glaciation (Figure 8).…”

Amoebozoan testate amoebae illuminate the diversity of heterotrophs and the complexity of ecosystems throughout geological time

“…This inferred radiation of early arcellinids provides compelling evidence for the capability of Neoproterozoic shallow marine ecosystems to support heterotrophic microbial eukaryotes. Biomarkers, fossil records, and molecular data suggest that at approximately 800 mya the Tonian period witnessed a significant transition from prokaryotic-dominated to eukaryotic-dominated ecosystems (Riedman and Sadler, 2018;Porter, 2020;Cohen and Kodner, 2022;Mills et al, 2022;Kang et al, 2023;). This transition was likely facilitated by factors such as increased availability of nitrate, phosphorous, silica, and reduced toxicity, which provided a favorable foundation for the diversification of phototrophic eukaryotes (Siever, 1992;Reinhard et al, 2017;Reinhard et al, 2020;Kang et al, 2023 ).…”

“…Biomarkers, fossil records, and molecular data suggest that at approximately 800 mya the Tonian period witnessed a significant transition from prokaryotic-dominated to eukaryotic-dominated ecosystems (Riedman and Sadler, 2018;Porter, 2020;Cohen and Kodner, 2022;Mills et al, 2022;Kang et al, 2023;). This transition was likely facilitated by factors such as increased availability of nitrate, phosphorous, silica, and reduced toxicity, which provided a favorable foundation for the diversification of phototrophic eukaryotes (Siever, 1992;Reinhard et al, 2017;Reinhard et al, 2020;Kang et al, 2023 ). Similarly, molecular clock analyses have indicated the divergence of multiple heterotrophic eukaryotes around the same time (Parfrey et al, 2011;Eme et al, 2014).…”

“…Evidence from fossils, biomarkers, geochemical proxies, genomic data, and molecular clocks indicate that the diversification of eukaryotes occurred during the late Mesoproterozoic Stenian period (1200-1000 Ma) and early Neoproterozoic Tonian period (1000-720 Ma) (Xiao et al, 2018;Li et al, 2020;Tang et al, 2020;Del Cortona et al, 2020;. This led to a transition from a prokaryotic-dominant to a eukaryotic-dominant marine environment (Porter, 2020;Cohen and Kodner, 2022;Mills et al, 2022;Kang et al, 2023), which occurred around 800 million years ago, likely triggered by increased phosphorus, nitrate, and silica availability and other favorable geochemical and biological conditions (Siever, 1992;Kang et al, 2023;Reinhard et al, 2017;Reinhard et al, 2020). From around this time, Neoproterozoic vase-shaped microfossils (VSMs) represent the remnants of early eukaryotic diversification in the marine fossil record (Porter and Knoll, 2000;Porter et al, 2003;Morais et al, 2019).…”