Incorporation of Hydroxamate Siderophore and Associated Fe Into Marine Particles in Natural Seawater

Peng Lin,Peter H Santschi,Chen Xu,Luni Sun,Wei Xing

doi:10.3389/fmars.2020.584628

Peng Lin, Peter H Santschi + Show 3 more

Open Access

https://doi.org/10.3389/fmars.2020.584628

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Abstract

Microorganisms produce soluble low-molecular-weight (LMW, <1 kDa) siderophores, one of the strongest Fe-binding agents, to respond to the scarcity of Fe in the ocean. The presence of siderophores in marine particles/colloids is mostly not considered. Here, experimental evidence is provided to suggest the possibility of siderophore incorporation into marine particles. An incubation experiment with a 59Fe-complexed desferrioxamine (DFO, siderophore-model compound) was conducted using natural seawater (<3µm) at dark condition to examine the size re-distribution of DFO and its associated Fe during microbial growth. 59Fe and DFO in suspended particles/aggregates, colloids and dissolved phase were quantified after the incubation. Our results showed that ~55% of the 59Fe, originally in the form of LMW DFO-Fe, was incorporated in the suspended particles/aggregates. Noticeably, a minor amount (0.395±0.020%) of the DFO was incorporated into the particulate phase. This finding is novel in that while the DFO facilitating Fe incorporation into microbial biomass was released back into the dissolved phase, still a minor fraction of the siderophores could be ‘retained’ in particles. This could have become cumulatively more important in more complex natural systems that involves the interplay between minerals, bacteria, phytoplankton and zooplankton. Furthermore, our results indirectly suggest a balance of the two different mechanisms during the Fe-siderophore transport. Our results are in favor of the processes occurring outside of the cells (Fe dissociation from the Fe-siderophore complex followed by the microbial Fe uptake) but the second mechanism can also exist (uptake of intact Fe-siderophore complex into the microbial intracellular fractions), albeit to a lesser extent.

Highlights

Dissolved Fe concentrations are at trace levels (≤1.0 nM) in the ocean compared to particulate Fe which consist of 74–99% of the total Fe pool (Boyd et al, 2010; Lam et al, 2012; Buck et al, 2015) dFe concentration can be higher than 1.0 nM in deeper ocean (Bennett et al, 2008; Nishioka et al, 2013)
In response to the scarcity of Fe, microorganisms produce a variety of Fe-binding ligands, e.g., siderophores, that create highly soluble forms of dFe by chelation that are transformed to bioavailable Fe through microbial enzymatic solubilization reactions (Morel and Price, 2003; Gledhill and Buck, 2012; Hassler et al, 2015)
Fe is one of the most important micronutrients for the microbial growth and primary production in the ocean (Quigg et al, 2011, 2016), with most of the Fe being associated with strong organic ligands

Summary

Introduction

Dissolved Fe (dFe) concentrations are at trace levels (≤1.0 nM) in the ocean compared to particulate Fe which consist of 74–99% of the total Fe pool (Boyd et al, 2010; Lam et al, 2012; Buck et al, 2015) dFe concentration can be higher than 1.0 nM in deeper ocean (Bennett et al, 2008; Nishioka et al, 2013) This low dFe concentration can limit microalgal productivity (Quigg, 2016) by as much as 30–40% in the upper water column of oceans, in high-nutrient, low-chlorophyll (HNLC) regions Direct evidence for this incorporation is still insufficient, while it can provide new insights into the transport and cycling of Fe in the ocean

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