Environ. Sci. Technol. 2008, 42, 8675–8680
Hydroxamate Siderophores: Occurrence and Importance in the Atlantic Ocean E D W A R D M A W J I , † M A R T H A G L E D H I L L , * ,† JAMES A. MILTON,† GLEN A. TARRAN,‡ SIMON USSHER,§ ANU THOMPSON,| GEORGE A. WOLFF,| PAUL J. WORSFOLD,§ AND ERIC P. ACHTERBERG† School of Ocean and Earth Science, National Oceanography Centre, University of Southampton, Southampton SO14 3ZH, Plymouth Marine Laboratory, Plymouth PL1 3DH, School of Earth, Ocean and Environmental Sciences, University of Plymouth, Plymouth PL4 8AA, and Department of Earth and Ocean Sciences, University of Liverpool, Liverpool L69 3GP, United Kingdom
Received July 8, 2008. Revised manuscript received September 30, 2008. Accepted October 4, 2008.
Siderophores are chelates produced by bacteria as part of a highly specific iron uptake mechanism. They are thought to be important in the bacterial acquisition of iron in seawater and to influence iron biogeochemistry in the ocean. We have identified and quantified two types of siderophores in seawater samples collected from the Atlantic Ocean. These siderophores were identified as hydroxamate siderophores, both ferrioxamine species representative of the more soluble marine siderophores characterized to date. Ferrioxamine G was widely distributed in surface waters throughout the Atlantic Ocean, while ferrioxamine E had a more varied distribution. Total concentrations of the two siderophores were between 3 and 20 pM in the euphotic zone. If these compounds are fully complexed in seawater, they represent approximately 0.2-4.6% of the 99%) complexed by organic ligands (11-13) in seawater. These ligands buffer dissolved iron concentrations by preventing the formation of insoluble oxyhydroxides (14). Complexing ligands have been observed in most oceans with concentrations ranging from 0.4 to 8 nM, but the chemical nature and identification of these ligands remain poorly constrained. Increases in concentrations of organic iron-complexing ligands have been reported in the equatorial Pacific (IronEx II) (15), the Southern Ocean (16, 17), and the subarctic Pacific (18) during phytoplankton blooms induced by iron fertilization experiments. These findings indicate that the release of ligands is linked to microbial biomass and thus their source is biological. One potential group of biologically produced iron-binding ligands are siderophores. Reported iron-binding ligands in seawater have stability constants (log KFe3+L ) 18-23 (19)) similar to those of laboratory-isolated siderophores (log KFe3+L ) 21-24) (19). Measurements of iron ligands from the California coastal upwelling region have shown that a large proportion of the ligands are similar in size (300-1000 Da) and contain iron-binding functional groups similar to siderophores (20). Laboratory-based studies have identified various marine cyano- and heterotrophic bacteria that produce siderophores under iron stress (6, 7, 21-27). Many of these have fatty acid side chains (8), and the majority contain either hydroxamate (6, 24) or mixed ligand R-hydroxycarboxylic acid/hydroxamate (7, 23, 27) functional groups. Using recently developed high-performance liquid chromatography-mass spectrometry methods, we studied the distribution of hydroxamate siderophores in contrasting biogeochemical provinces of the Atlantic Ocean. Surface ocean samples were collected along a cruise track (31° S, 16° E to 47° N, 13° W) through the southern and northern oligotrophic gyres, the equatorial upwelling, and the northern and southern temperate regions (Figure 1). Siderophore distributions are compared to bacterial abundances and concentrations of dissolved iron to gain a preliminary understanding of the importance of these compounds to the biogeochemical cycling of iron in the Atlantic Ocean.
Introduction Iron is an essential element for growth and metabolism in marine organisms. Iron-containing proteins are involved in the photosynthetic and respiratory systems, in nitrate and nitrite reduction, and in N2 fixation (1). Due to the low solubility of iron(III) and the formation of highly insoluble oxyhydroxides in oxygenated waters, iron is present at extremely low concentrations (
