Mechanisms and heterogeneity of mineral use by natural colonies of the cyanobacteriumTrichodesmium

Abstract

The keystone marine nitrogen fixer Trichodesmium thrives in high dust environments, and while experimental observations suggest that Trichodesmium colonies can access the essential nutrient iron from dust particles, it is not known the extent to which this occurs in the field. Here we demonstrate that Trichodesmium colonies actively process mineral particles in nature with direct molecular impacts. Microscopy and synchrotron-based imaging demonstrated heterogeneous associations with particles consistent with iron oxide and iron silicate minerals. Metaproteomic analysis of individual colonies revealed enrichment of biogeochemically-relevant proteins including photosynthesis proteins and metalloproteins containing iron, nickel, copper and zinc when particles were present. The iron-storage protein ferritin was particularly enriched implying accumulation of particle-derived iron, and multiple iron acquisition pathways including Fe(II), Fe(III), and Fe-siderophore transporters were engaged, including evidence of superoxide-driven particle dissolution. While the particles clearly provided iron, there was also evidence that the concentrated metals had toxic effects. The molecular mechanisms allowing Trichodesmium to interact with particulate minerals are fundamental to its success and global impact on nitrogen biogeochemistry, and may contribute to the leaching of particulate trace metals with implications for global iron and carbon cycling.

Colonies of the marine cyanobacterium Trichodesmium optimize dust utilization by selective collection and retention of nutrient-rich particles

“…An ability to remove particles also enables colonies to rapidly change their pool of particles and replace nutrient-exhausted particles with fresh ones, potentially providing larger nutrient fluxes. The documented ability to control the amount (and possibly type) of particles may hereby explain a recent report by Held et al, 2020a), who collected both particle-free and particle-loaded colonies from a single net tow in the Caribbean Sea (Held et al, 2020a).…”

“…This is in contrast to the $80-fold higher cellular requirements for P compared with Fe (San ˜udo- Wilhelmy et al, 2001Wilhelmy et al, , 2004. Despite the low overall solubility of both Fe and P from dust, typically estimated 0.1%-10% (Aguilar-Islas et al, 2010;Mahowald et al, 2005Mahowald et al, , 2008Stockdale et al, 2016), Trichodesmium can employ a variety of biochemical pathways and physical mechanisms in order to enhance the solubility and bioavailability of Fe from dust (Basu et al, 2019;Basu and Shaked, 2018;Eichner et al, 2019Eichner et al, , 2020Held et al, 2020a;Kessler et al, 2020b;Rubin et al, 2011). The effect of such mechanisms on dust-P solubility has not yet been studied, but as P is often associated with Fe, it is likely that Trichodesmium can also modify dust-P and enhance its bioavailability.…”

“…The ability to remove particles provides flexibility with regards to the amount and type of particles colonies can retain. Such flexibility enables colonies to offset the potential negative effects of a high particle load such as buoyancy loss, exposure to toxic trace elements present in dust, increased visibility to predators, self-shading by particles, and restricted diffusion of solutes (Held et al, 2020a;Kessler et al, 2020b;Paytan et al, 2009;Walsby, 1992). An ability to remove particles also enables colonies to rapidly change their pool of particles and replace nutrient-exhausted particles with fresh ones, potentially providing larger nutrient fluxes.…”

“…The quantitative agreement between our studies indicate that Red Sea colonies-dust interactions are robust, iScience Article making our findings applicable to additional oceanic environments. Indeed, several recent studies from the South Atlantic and Caribbean Sea reported the significant accumulation of mineral particles by natural colonies (Bif and Yunes, 2017;Held et al, 2020a).…”