Competition among marine phytoplankton for different chelated iron species

Abstract

Dissolved-iron availability plays a critical role in controlling phytoplankton growth in the oceans 1,2 . The dissolved iron is overwhelmingly (ϳ99%) bound to organic ligands with a very high affinity for iron 3-5 , but the origin, chemical identity and biological availability of this organically complexed Fe is largely unknown 6 . The release into sea water of complexes that strongly chelate iron could result from the inducible iron-uptake systems of prokaryotes (siderophore complexes) 7-9 or by processes such as zooplankton-mediated degradation and release of intracellular material (porphyrin complexes). Here we compare the uptake of siderophore-and porphyrin-complexed 55 Fe by phytoplankton, using both cultured organisms and natural assemblages. Eukaryotic phytoplankton efficiently assimilate porphyrin-complexed iron, but this iron source is relatively unavailable to prokaryotic picoplankton (cyanobacteria). In contrast, iron bound to a variety of siderophores is relatively more available to cyanobacteria than to eukaryotes, suggesting that the two plankton groups exhibit fundamentally different iron-uptake strategies. Prokaryotes utilize iron complexed to either endogenous 7-9 or exogenous siderophores 9 , whereas eukaryotes may rely on a ferrireductase system 10,11 that preferentially accesses iron chelated by tetradentate porphyrins, rather than by hexadentate siderophores. Competition between prokaryotes and eukaryotes for organicallybound iron may therefore depend on the chemical nature of available iron complexes, with consequences for ecological niche separation, plankton community size-structure and carbon export in low-iron waters.Extracellular chelators are produced by many marine cyanobacteria and heterotrophic bacteria as part of high-affinity Fe uptake systems 7,9,12 . Several investigators have noted the similarity between Fe-binding conditional stability constants (K cond ) of these siderophores and the uncharacterized ligands in sea water (for both, log K cond ¼ 19-23) 4,7,8 . The siderophores produced by various marine prokaryotes have diverse molecular structures, including hydroxamates, catecholates 7,9 , and mixed functional group (␤-hydroxy aspartate/catecholate) ligands 12 .Another likely source of strong chelators in the water column is through release of intracellular ligands by zooplankton grazing 13 or viral lysis 14 . Cells contain many organic molecules that can strongly complex iron. We chose tetrapyrroles to represent this type of cell breakdown ligand, since they are among the most abundant strong chelators of Fe in cells. Tetrapyrroles include porphyrins such as those in chlorophylls, cytochromes and haem proteins 6 , and linear tetrapyrroles such as the phycobilin pigments of cyanobacteria. Like siderophores, tetrapyrroles have very high conditional stability constants for Fe(III) binding that resemble those of the seawater ligands (ref. 4, and A.E.W., unpublished results). Faecal pellets of metazoan and protozoan grazers are highly enriched with phaeopigment porphyrins 15,16 ,...

A microarray for assessing transcription from pelagic marine microbial taxa

“…In contrast, idiA transcription by more eutrophic Synechococcus RCC307-like (sub-cluster 5.3A, MellaFlores et al, 2011) and Pelagibacter HTCC7211-like genotypes was higher in the Fe-amendment. The differences between coastal and open ocean species have been reported before in cultures and include differences in Fe requirements and sensing (for example, Sunda et al, 1991;Palenik et al, 2006), uptake of siderophore-or porphyrin-bound Fe (Hutchins et al, 1999) and post-translational regulation by antisense RNA (Hernández et al, 2006). This is the first report that validates differential Fe responses across a multitude of taxa in a mixed community.…”

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

“…The ligands used in all the experiments were prepared using trace metal clean methods and were deferrated as needed; details of preparation protocols are presented in Hutchins et al (1999) and Witter et al (2000). The model ligands chosen for the Fe uptake experiments were desferrioxamine (a trihydroxamate siderophore), ferrichrome (a trihydroxamate siderophore), rhodotorulic acid (a dihydroxamate siderophore), protoporphyrin IX (a porphyrin compound), and an uncharacterized ligand from the cultured marine cyanobacterium Synechococcus sp.…”

Dust iron dissolution in seawater: Results from a one‐year time‐series in the Mediterranean Sea

“…Seasonal variations of organic speciation have been demonstrated for copper [Croot, 2003] but, to our knowledge, this is the first report of the temporal variability of iron binding ligands at a yearly scale. Different biogenic sources for iron binding ligands have been proposed [Hutchins et al, 1999]: (1) synthesis and release by prokaryotic organisms in iron limited environments and (2) breakdown of biological material. In the present study, variation in ligand concentration presents a significant positive correlation with BA (r 2 = 0.73, p = 0.008, n = 10) and DOC (r 2 = 0.57, p = 0.01, n = 10) whereas no significant correlation is observed with TChla or any phytoplankton group.…”