Metal limitation of cyanobacterial N₂fixation and implications for the Precambrian nitrogen cycle

Abstract

Nitrogen fixation is a critical part of the global nitrogen cycle, replacing biologically available reduced nitrogen lost by denitrification. The redox‐sensitive trace metals Fe and Mo are key components of the primary nitrogenase enzyme used by cyanobacteria (and other prokaryotes) to fix atmospheric N2 into bioessential compounds. Progressive oxygenation of the Earth's atmosphere has forced changes in the redox state of the oceans through geologic time, from anoxic Fe‐enriched waters in the Archean to partially sulfidic deep waters by the mid‐Proterozoic. This development of ocean redox chemistry during the Precambrian led to fluctuations in Fe and Mo availability that could have significantly impacted the ability of prokaryotes to fix nitrogen. It has been suggested that metal limitation of nitrogen fixation and nitrate assimilation, along with increased rates of denitrification, could have resulted in globally reduced rates of primary production and nitrogen‐starved oceans through much of the Proterozoic. To test the first part of this hypothesis, we grew N2‐fixing cyanobacteria in cultures with metal concentrations reflecting an anoxic Archean ocean (high Fe, low Mo), a sulfidic Proterozoic ocean (low Fe, moderate Mo), and an oxic Phanerozoic ocean (low Fe, high Mo). We measured low rates of cellular N2 fixation under [Fe] and [Mo] estimated for the Archean ocean. With decreased [Fe] and higher [Mo] representing sulfidic Proterozoic conditions, N2 fixation, growth, and biomass C:N were similar to those observed with metal concentrations of the fully oxygenated oceans that likely developed in the Phanerozoic. Our results raise the possibility that an initial rise in atmospheric oxygen could actually have enhanced nitrogen fixation rates to near modern marine levels, providing that phosphate was available and rising O2 levels did not markedly inhibit nitrogenase activity.

Nitrogen cycle feedbacks as a control on euxinia in the mid-Proterozoic ocean

“…Although changes in water column stratification and/or global sulphate budgets 28 are, of course, relevant to euxinia, we argue that the 'electron tower' of respiratory-free energy yield 14 dictates that nitrate availability is a stronger first-order control. Similarly, the ongoing debate as to the significance of trace element limitation leading to stalls at various points in the nitrogen cycle 12,13,29,30 is not theoretically inconsistent with our arguments and may yet gain empirical validation. We suggest that as data become more available the empirical community should conduct a systematic cross-referencing exercise between the implicit occurrence of euxinia and the presence/absence of nitrogen fixation/nitrate-limited production.…”

“…Interestingly, some such OAEs appear on the basis of isotopic and biomarker evidence to have coincided with high rates of nitrogen fixation in the surface ocean 11 . A related link between Proterozoic euxinia and nitrogen cycle perturbation via trace element stress has been suggested 12 , but quantitative support for this 'bioinorganic bridge' hypothesis is presently lacking 13 .…”

The evolution of Earth's biogeochemical nitrogen cycle

“…Under experimental conditions with cultures of modern cyanobacteria, N 2 -fixation rates decline significantly if Mo drops below 5-10nM, depending on the organism used (Glass et al, 2010;Zerkle et al, 2006). Fixation rates are still measurable but 80% suppressed with 1-5nM Mo (Zerkle et al, 2006). These thresholds coincide with the 1-10nM range of Mo that has most recently been proposed for the mid-Proterozoic ocean (Reinhard et al, 2013b), making Molimitation conceivable.…”

“…Under experimental conditions with cultures of modern cyanobacteria, N 2 -fixation rates decline significantly if Mo drops below 5-10nM, depending on the organism used (Glass et al, 2010;Zerkle et al, 2006). Fixation rates are still measurable but 80% suppressed with 1-5nM Mo (Zerkle et al, 2006).…”

Basinal restriction, black shales, Re‐Os dating, and the Early Toarcian (Jurassic) oceanic anoxic event

“…Third, such a scenario is able to succinctly explain isotopic excursions in both d 98 Mo and 187 Os/ 188 Os through the interval (documented in Figure 6), as we explain in later sections. Finally, a problem with whole ocean interpretations of rsMo/TOC is that low values in sediments imply drawdown of Mo in the oceans, a drawdown that might limit primary production and make continued black shale deposition impossible to sustain [Zerkle et al, 2006;Scott et al, 2008]. This limitation does not apply to a restricted basin scenario because the more dominant role of the low-salinity surface layer can provide both nutrients and Mo for primary production.…”