Co‐acquisition of mineral‐bound iron and phosphorus by natural Trichodesmium colonies

Abstract

Low iron (Fe) and phosphorus (P) ocean regions are often home to the globally important N 2 -fixing cyanobacterium Trichodesmium spp., which are physiologically adapted to Fe/P co-limitation. Given Trichodesmium's eminent ability to capture particles and the common associations between Fe and P in sediments and aerosols, we hypothesized that mineral bio-dissolution by Trichodesmium spp. may enable them to co-acquire Fe and P. We present a new sensitive assay to determine P uptake from particles, utilizing 33 P-labeled ferrihydrite. To validate the method, we examined single natural Trichodesmium thiebautii colonies in a high-resolution radiotracer ß-imager, identifying strong colony-mineral interactions, efficient removal of external 33 P-labeled ferrihydrite, and elevated 33 P uptake in the colony core. Next, we determined bulk P uptake rates, comparing natural Red Sea colonies and P-limited Trichodesmium erythraeum cultures. Uptake rates by natural and cultured Trichodesmium were similar to P release rates from the mineral, suggesting tight coupling between dissolution and uptake. Finally, synthesizing P-ferrihydrite labeled with either 33 P or 55 Fe, we probed for Fe/P co-extraction by common microbial mineral solubilization pathways. Dissolution rates of ferrihydrite were accelerated by exogenous superoxide and strong Fe-chelator and subsequently enhanced 33 P release and uptake by Trichodesmium. Our method and findings can facilitate further Fe/P co-acquisition studies and highlight the importance of biological mechanisms and microenvironments in controlling bioavailability and nutrient fluxes from particles.

Phosphorus deficiency alleviates iron limitation in Synechocystis cyanobacteria through direct PhoB-mediated gene regulation

“…The highly episodic aerosol dust deposition in marine ecosystems may also lead to a simultaneous deficiency or enrichment of these two elements 9,50,51 . At the cellular level, mineral bio-dissolution by natural cyanobacterial colonies could enable them to co-acquire Fe and P 5 . And the intracellular storage of Fe in cyanobacteria and higher plants is also tightly associated with P 52 .…”

“…Nutrient availability constrains the rate of biological production and the structure of ecosystem communities on a global scale 1,2 . As essential nutrients required by all living organisms, iron (Fe) and phosphorus (P) participate in a series of metabolic processes, and their chemical roles are deeply interconnected [3][4][5] . While the critical role of Fe and P in controlling primary productivity has long been recognized [6][7][8] , recent studies demonstrate that limitation by Fe and P could occur simultaneously 9,10 .…”

Costs of Dust Collection by Trichodesmium: Effect on Buoyancy and Toxic Metal Release

“…Natural Trichodesmium is often limited, or co‐limited, by iron (Fe) and phosphorus (P) (Cerdan‐Garcia et al., 2022; Held et al., 2020). Aerosol dust deposited on the ocean surface is considered an important nutrient source, but the low solubility of Fe and P minerals restrict their bioavailability for phytoplankton (Mills et al., 2004; Shaked et al., 2023; Shaked & Lis, 2012; Stockdale et al., 2016). Incubation studies revealed that Trichodesmium successfully grow on aerosol or dust (Chen et al., 2011; Polyviou et al., 2018), and even increase the bioavailability of dust‐borne Fe and P (Basu et al., 2019; Basu & Shaked, 2018; Shaked et al., 2023).…”

“…An intriguing finding, which was reaffirmed in several studies, is the ability of Trichodesmium colonies to actively collect and transport dust particles into the colony core (Kessler, Armoza‐Zvuloni, et al., 2020; Rubin et al., 2011; Wang et al., 2022). Particle centering may not only enhance dust dissolution, but could also minimize nutrient loss by diffusion, and thus optimize uptake (Eichner et al., 2023; Shaked et al., 2023). While these nutritional benefits are well established, studies exploring negative sides of particle collection to Trichodesmium, remain scarce.…”

“…Aerosol dust deposited on the ocean surface is considered an important nutrient source, but the low solubility of Fe and P minerals restrict their bioavailability for phytoplankton (Mills et al., 2004; Shaked et al., 2023; Shaked & Lis, 2012; Stockdale et al., 2016). Incubation studies revealed that Trichodesmium successfully grow on aerosol or dust (Chen et al., 2011; Polyviou et al., 2018), and even increase the bioavailability of dust‐borne Fe and P (Basu et al., 2019; Basu & Shaked, 2018; Shaked et al., 2023). An intriguing finding, which was reaffirmed in several studies, is the ability of Trichodesmium colonies to actively collect and transport dust particles into the colony core (Kessler, Armoza‐Zvuloni, et al., 2020; Rubin et al., 2011; Wang et al., 2022).…”