Direct use of inorganic colloidal iron by marine mixotrophic phytoplankton

Abstract

Three species of photosynthetic flagellates capable of phagotrophy (mixotrophic species) were tested for their abilities to use inorganic iron colloids for growth. Ochromonas sp., Chrysochromulina ericina (a coastal strain), and C. ericina (an oceanic strain) were grown in iron-free seawater supplemented with 1 M Fe-ferrihydrite (amorphous hydrous ferric oxide), magnetite (Fe 3 O 4 )/maghemite (␥-Fe 2 O 3 ), hematite (␣-Fe 2 O 3 ), or goethite (␣-FeOOH). Desferrioxamine B, an iron-binding siderophore, was used to reduce the concentration of dissolved iron in the colloid-amended media, and none of the flagellates were able to use its iron complex as an iron source under the conditions of the experiments. Both strains of Chrysochromulina grew at 35%-70% of their maximum rates with goethite, hematite, and magnetite/maghemite but were unable to use ferrihydrite. Ochromonas grew well with ferrihydrite but could not use any of the other forms. Thalassiosira oceanica (clone 1003) and Thalassiosira pseudonana (clone 3H), diatoms that could only take up dissolved forms of iron, were unable to use any of the colloids tested. The mechanism of iron acquisition by the flagellates appeared to involve ingestion of the iron colloids, because bacteria resident in the cultures were too iron poor to be a significant source of iron and were unable to use the iron contained in the colloids themselves. Variations in the sizes of the colloids were hypothesized to account for differences in their availability, independent of colloid chemical stability. The results provide the first strong evidence for direct use (i.e., without prior dissolution) of colloidal iron by mixotrophic phytoplankton and document a new pathway of iron acquisition that may be important for their survival in low-iron waters of the sea.

The Iron Biogeochemical Cycle Past and Present

“…Ingested iron minerals are subjected to low pH processing in the gut that enhances bioavailability. Nodwell and Price (2001) showed that some species of mixotrophic flagellates were able to use goethite, haematite and magnetite but not ferrihydrite, whilst other species could only use ferrihydrite. In all cases uptake appeared to involve ingestion and thus represents the direct use of colloidal iron by eukaryotic organisms.…”

Impact of icebergs on net primary productivity in the Southern Ocean

“…However, Hassler and Schoemann (2009) found no direction link between soluble and bioavailable Fe because organic ligands have the differential effects on the solubility and the bioavailability. Several studies seem to suggest that organic colloidal Fe provides an important pool to sustain Fe bioavailability to phytoplankton (e.g., Nodwell and Price, 2001;Chen et al, 2003;Wang and Dei, 2003). Finally, icebergs themselves could have other effects on NPP.…”

Grain size, morphometry and mineralogy of airborne input in the Canary basin: evidence of iron particle retention in the mixed layer

“…This anomalous retention of denser minerals could reveal the biological interaction of iron particles with microorganisms described by some authors (Nodwell and Price 2001, Sohm 2011, Benavides et al 2013. Under the sedimentological point of view, this anomalous "low sinking behaviour" of the densest iron oxyhydroxide particles is another innovation presented in this research.…”

“…Several studies have shown that phagotrophic flagellates could ingest even micrometric iron particles or colloids, dissolving and regenerating some types of particulate iron during digestion (Barbeau et al 1996, Chase and Price 1998, Barbeau and Moffett 2000, and retaining the mineral in the water column (Nodwell and Price 2001). Moreover, it has been suggested that colony formation in Trichodesmium is an adaptive strategy to trap the dust and enhance iron acquisition (Rubin 2011), dissolving dust and oxides.…”