Feeling anaemic? Have some siderophores!

Iron is a fundamental element involved in many biochemical processes including oxidative phosphorylation, photosynthesis, nitrogen fixation, and the detoxification of free radicals. However, dissolved inorganic Fe is scarce in the marine environment due to its propensity to precipitate in the presence of oxygen and relatively high oceanic pH levels. Fe is rapidly scavenged onto particles under such conditions leading to mean global concentrations of just 0.07 nmol kg^-1. Of this dissolved iron 99.9% exists bound to disparate organic ligands which are present in high numbers. So does this mean that organically bound iron is unavailable to marine heterotrophic bacteria for growth?

Siderophores are small molecules with a high affinity for chelating and forming complexes with Fe³⁺ and are produced in response to iron depravation by microorganisms. Siderophores are released extracellularly where they bind inorganic iron and ‘steal’ iron from other organic complexes with lower affinities. Siderophores are then internalised and the iron assimilated to help fulfil cellular iron requirements for growth. This study investigated how heterotrophic marine bacteria acquired iron for growth and the extent to which siderophores played a role in iron acquisition.

Seven gram-negative heterotrophic marine bacteria strains isolated from the Gulf of Mexico, Sargasso Sea, and NE subarctic Pacific were grown under iron-replete (8.4 µM) and iron-deplete (12.5 nM) conditions. Cellular iron uptake rates and iron quotas were quantified using the radioactive isotope  ⁵⁵Fe. The growth rates of all 7 strains were reduced on average by 50% on the iron-deplete growth medium and iron quotas were significantly reduced.

Separate culture medium was used for the isolation of siderophores and their iron binding strength determined. Iron chelating compounds were produced by 4 of the 7 strains with one siderophore isolated from the Gulf of Mexico having an extremely high affinity for Fe, binding >99% of available iron. Importantly siderophore production only occurred under iron limiting conditions. However all strains utilised Fe bound to at least one siderophore whether or not that strain produced its own.

 The importance of siderophores in the rate of iron uptake was quantified by comparing Fe uptake of all 7 strains on iron-deplete medium with and without the addition of siderophores isolated from 2 of the 7 strains, and a terrestrial fungal siderophore. The results showed that one marine siderophore and the fungal siderophore increased Fe uptake in the majority of strains, while the other isolated marine siderophore inhibited Fe uptake in 5 of the 7 strains whilst significantly increasing Fe uptake in the producing strain.

Two representative strains were used to elucidate the significance of organic vs inorganic iron uptake. The measured Fe uptake rates of inorganic Fe were tiny compared to the expected uptake rates based on diffusive flux. An ecological implication being that marine heterotrophic bacteria are not optimised to acquire inorganic iron for growth. Instead they rely on organically bound iron, unlike many eukaryotic phytoplankton species which require inorganic iron for growth.

The utilisation of siderophores of differing provenance (terrestrial as well as marine) suggest that perhaps only a finite amount of iron chelating compounds exist and that bacteria have evolved to be able to utilise iron bound to siderophores that it does not/cannot synthesise. Conversely a bacterium may monopolise iron in certain situations by specialising in the production of an uncommon ligand with high iron affinity that binds much of the available iron, thus inhibiting the growth of neighbouring bacterial heterotrophs.

I found the paper a valuable contribution to the in vitro study of siderophores and iron acquisition by bacteria. Further characterisation of marine siderophores and cellular uptake mechanisms need to be investigated to better understand the significance of siderophores in ocean biogeochemical cycles. For example; in this study differing bacteria were isolated from distinctly different water masses and it would be purposeful to see if differences in siderophores and siderophore specificity reflects their ecology and iron acquisition strategy.

Reference

Granger, Julie, and Neil M. Price. "The importance of siderophores in iron nutrition of heterotrophic marine bacteria." Limnology and Oceanography 44.3 (1999): 541-555.

http://m.avto.aslo.info/lo/toc/vol_44/issue_3/0541.pdf