Biomass recycling and Earth’s early phosphorus cycle
Phosphorus sets the pace of marine biological productivity on geological time scales. Recent estimates of Precambrian phosphorus levels suggest a severe deficit of this macronutrient, with the depletion attributed to scavenging by iron minerals. We propose that the size of the marine phosphorus reservoir was instead constrained by muted liberation of phosphorus during the remineralization of biomass. In the modern ocean, most biomass-bound phosphorus gets aerobically recycled; but a dearth of oxidizing power in Earth’s early oceans would have limited the stoichiometric capacity for remineralization, particularly during the Archean. The resulting low phosphorus concentrations would have substantially hampered primary productivity, contributing to the delayed rise of atmospheric oxygen.
Phosphorus (P) availability is thought to dictate the amount of primary productivity that can be sustained in the oceans on geologic time scales (1, 2). Estimating P concentrations in the ocean across Earth’s history is thus critical for understanding the growth of the biosphere and the evolution of major biogeochemical cycles—namely, the rise of atmospheric oxygen, which requires substantial burial of organic carbon generated via oxygenic photosynthesis. Multiple proxies have been used to reconstruct P levels, including the P content of iron (Fe) oxide–rich sedimentary rocks (3–5) and marginal marine siliciclastic sedimentary rocks (6). Although deriving quantitative assessments of P levels from these records has been notoriously difficult [for example, Bjerrum and Canfield (3) and Konhauser et al. (7)], recent work is beginning to converge on a low P ocean [<20% modern concentrations; modern, ~2 μM; (1, 2)], persisting in the Archean and perhaps through the Proterozoic (5, 6). The favored mechanism for P depletion in the Precambrian ocean is scavenging of P from the water column by incorporation into ferrous minerals or by adsorption onto Fe oxides (3, 5, 6). However, these models have not accounted for potential “upstream” throttles that could have kept P concentrations low without any influence of Fe scavenging. Here, we propose a new mechanism for maintaining low P: limited recycling of P in an oxidant-poor ocean.
The bioavailable P supply of the ocean derives almost entirely from riverine inputs, making P a scarce nutrient relative to carbon and nitrogen, which can be fixed from atmospheric sources (2). The modern riverine flux of bioavailable P is very small [~2 × 1012 g/year; (8)] compared to the amount annually used by the marine biosphere [~1200 × 1012 g/year; (8)]. This large discrepancy between supply and demand is sustained by the efficient recycling of P within the ocean. After the P in the surface ocean is exhausted during primary production, the remineralization of sinking biomass releases P back into the marine environment. This recycling increases the residence time of P in the ocean. As water masses mature in the deep ocean, they accumulate nutrients regenerated through biomass recycling and ultimately deliver these nutrients to the continental shelves via upwelling, enabling high rates of biological productivity. In the modern ocean, ~80 to 90% of primary productivity gets remineralized in the photic zone (upper, ~200 m; fig. S1), with most of the remainder being oxidized at depth or in marine sediments (9, 10). Only a very small percentage (≪1%) of net primary productivity (and its associated P) escapes remineralization and is ultimately buried in marine sediments. Thus, the magnitude of the P recycling flux has probably always dwarfed riverine inputs, even if early Precambrian riverine fluxes were an order of magnitude higher than today (11).
A critical difference between Precambrian and modern oceans is the availability of electron acceptors needed for the oxidation of biomass. In the oxygenated modern ocean, most organic matter degradation occurs aerobically (12). Even when localized water masses or sedimentary pore waters become anoxic, there is an ample supply of anaerobic electron acceptors [for example, sulfate (SO42−)] to fuel biomass decomposition (13). Before the establishment of oxidizing conditions at Earth’s surface, it is conceivable that the recycling of organic matter was limited by a scarcity of electron acceptors. Inhibited organic remineralization would mean that a greater proportion of sinking organic matter was preserved in marine sediments (that is, higher burial efficiency). However, the limited regeneration of P in this system might maintain low steady-state P concentrations in the deep ocean and upwelling waters, which would ultimately limit net primary productivity, total organic burial, and oxygenesis. We quantitatively explored this hypothesis by compiling estimates of the paleoconcentrations of the major electron acceptors in seawater (Fig. 1A) and stoichiometrically calculating the concentration of P that could have been maintained throughout Earth’s history.