Microbial feedbacks optimize ocean iron availability

Jonathan Maitland Lauderdale, Rogier Braakman, Gaël Forget, Stephanie Dutkiewicz, and Michael J. Follows

PNAS March 3, 2020 117 (9) 4842-4849

Iron, nitrogen, carbon, and other elements in the surface ocean are consumed by microbes, leading to a flux of sinking and subducted organic matter that is respired in deeper waters, ultimately releasing those nutrients back into dissolved (inorganic) form. Ocean circulation returns resource-rich deep waters back to the surface layer, maintaining global ocean productivity and sustaining a biologically mediated reservoir of inorganic carbon at depth, drawing down atmospheric CO₂.

Significance

Marine microbe growth is limited by iron over about half of the global ocean surface. Dissolved iron is quickly lost from the ocean, but its availability to marine microbes may be enhanced by binding with organic molecules which, in turn, are produced by microbes. We hypothesize this forms a reinforcing cycle between biological activity and iron cycling that locally matches the availability of iron and other nutrients, leading to global-scale resource colimitation between macronutrients and micronutrients, and maximizing biological productivity. Idealized models support this hypothesis, depending on the specific relationships between microbial sources and sinks of organic molecules. An evolutionary selection may have occurred which optimizes these characteristics, resulting in “just enough” iron in the ocean.

Abstract

Iron is the limiting factor for biological production over a large fraction of the surface ocean because free iron is rapidly scavenged or precipitated under aerobic conditions. Standing stocks of dissolved iron are maintained by association with organic molecules (ligands) produced by biological processes. We hypothesize a positive feedback between iron cycling, microbial activity, and ligand abundance: External iron input fuels microbial production, creating organic ligands that support more iron in seawater, leading to further macronutrient consumption until other microbial requirements such as macronutrients or light become limiting, and additional iron no longer increases productivity. This feedback emerges in numerical simulations of the coupled marine cycles of macronutrients and iron that resolve the dynamic microbial production and loss of iron-chelating ligands. The model solutions resemble modern nutrient distributions only over a finite range of prescribed ligand source/sink ratios where the model ocean is driven to global-scale colimitation by micronutrients and macronutrients and global production is maximized. We hypothesize that a global-scale selection for microbial ligand cycling may have occurred to maintain “just enough” iron in the ocean.

See https://www.pnas.org/content/117/9/4842

Figure 1: Schematic of the “ligand–iron–microbe” feedback. Free iron (Fe'Fe′) is added to the ocean from external sources like dust and sedimentary mobilization, and lost due to scavenging, precipitation, and burial. Iron retention is increased by complexation with organic ligands (LTLT; FeT=Fe'+FeLFeT=Fe′+FeL and LT=L'+FeLLT=L′+FeL). Microbial production of biomass (B) is dependent on iron, and is a source of ligands, for example, by siderophore production, excretion of organic carbon, and release of cell detritus during remineralization. The production of ligands retains a greater concentration of iron, fueling more microbial production, and so on, until the other resources that microbial production requires, such as macronutrients, become limiting. Thus the “ligand–iron–microbe” feedback maintains “just enough” iron in the ocean to match the availability of other resources, resulting in colimitation.