Bioavailability of iron to Trichodesmium colonies in the western subtropical Atlantic Ocean

Abstract

Trichodesmium provides new nitrogen (N) to marine surface waters via N 2 fixation, a process that requires a substantial amount of iron (Fe). Organic ligands in seawater that bind Fe could either increase or reduce the bioavailability of Fe. Electrochemical techniques indicate that these naturally occurring ligands have Fe-binding constants similar to those of siderophores and porphyrins, suggesting that these chelators play an important role in determining the bioavailability of Fe to cyanobacteria. We conducted Fe uptake experiments using model ligands labeled with 55 Fe to compare the bioavailability of inorganic Fe(III), porphyrin-bound Fe(III), and siderophorebound Fe(III) to field-collected Trichodesmium colonies. Inorganic Fe(III) and siderophore-bound Fe(III) were more bioavailable to Trichodesmium colonies than was porphyrin-bound Fe(III). Furthermore, the bioavailability of the siderophore-bound Fe(III) can be characterized by the functional groups of the siderophore. The dihydroxamate siderophore and an uncharacterized ligand from a cultured Synechococcus sp. increased the bioavailability of Fe compared to the trihydroxamate siderophores. Except for experiments with desferrioxamine B, dark incubations resulted in lower Fe uptake rates for all treatments, relative to parallel lighted incubations. This suggests that light enhances the photochemical dissociation of most of the ligand complexes or that light energy is required for the active transport of Fe complexed to the model ligands. The Fe uptake rate of Trichodesmium colonies also differed slightly on the basis of colony morphology, with higher uptake rates with ''puffs'' than ''tufts.'' These experiments show that Trichodesmium colonies are capable of discriminating between Fe bound to different organic complexes.

Ocean acidification slows nitrogen fixation and growth in the dominant diazotroph Trichodesmium under low-iron conditions

“…Although the mechanism of Fe uptake by Trichodesmium remains to be fully elucidated, it has been shown that the uptake process can involve a bio-reduction step, as has been demonstrated in some model diatom species (26)(27)(28). Trichodesmium apparently is capable of accessing Fe from Fe oxide, aerial dust, and siderophores (29,30) in which Fe bioavailability should be less sensitive to pH than in our EDTA-buffered medium (4). Our results clearly demonstrate that, over the range of interest, the effects of pCO 2 /pH on Fe uptake in Trichodesmium are caused by changes in the chemistry of the medium, not by a physiological response of the organism, in agreement with previous findings in other phytoplankton species (4).…”

The role of siderophores in iron acquisition by photosynthetic marine microorganisms

“…Colonies of Trichodesimum sp. collected in the subtropical Atlantic Ocean were able to access iron from a range of siderophores including desferrioxamine, rhodotorulic acid, and ferrichrome, though it should be noted that other bacterial species associated with the colonies could have contributed to uptake (Achilles et al 2003). The widespread ability to acquire iron from chelates regardless of siderophore structure by organisms which appear to lack TonB-dependent outer membrane receptors suggests that an alternate uptake pathway is used.…”

New insights into iron acquisition by cyanobacteria: an essential role for ExbB-ExbD complex in inorganic iron uptake

“…Complexation by siderophores and other uncharacterized organic ligands increases the solubility of the dissolved iron (Mawji et al, 2008) but reduces its availability to many taxa. At the extreme, such reduced iron bioavailability can impair phytoplankton growth (Boyd et al, 2007;Falkowski and Raven, 2007;Chappell et al, 2012;Wilhelm et al, 2013) and is thought to limit the primary productivity in as much as 40% of global ocean (Martin et al, 1994;Falkowski et al, 1998;Achilles et al, 2003) and some freshwater habitats (North et al, 2007;Havens et al, 2012).…”

“…However, the siderophoremediated iron uptake pathway described in non-photosynthetic bacteria has not been fully confirmed in cyanobacterial species (Stevanovic et al, 2012). The following observations are pertinent: (i) although cyanobacteria possess an OM and are commonly considered as Gram-negative bacteria, their cell envelopes are partly characteristic of Gram-positive bacteria, which do not possess the TonB-ExbB-ExbD system (Hoiczyk and Hansel, 2000); (ii) while some species produce strong siderophores, most cyanobacteria do not (Ito and Butler, 2005;Hopkinson and Morel, 2009;Mirus et al, 2009);and (iii) some cyanobacteria can use the iron bound to siderophores of other organisms (Kranzler et al, 2011). Hopkinson and Morel (2009) suggested that the role of siderophores in marine environments is probably overestimated but could reach no definitive conclusion, because the iron acquisition mechanisms of cyanobacteria are poorly understood.…”