Iron utilization in marine cyanobacteria and eukaryotic algae

Abstract

Iron is essential for aerobic organisms. Additionally, photosynthetic organisms must maintain the iron-rich photosynthetic electron transport chain, which likely evolved in the iron-replete Proterozoic ocean. The subsequent rise in oxygen since those times has drastically decreased the levels of bioavailable iron, indicating that adaptations have been made to maintain sufficient cellular iron levels in the midst of scarcity. In combination with physiological studies, the recent sequencing of marine microorganism genomes and transcriptomes has begun to reveal the mechanisms of iron acquisition and utilization that allow marine microalgae to persist in iron limited environments.

Keywords: algae; cyanobacteria; diatoms; genomics; iron; phytoplankton; prasinophytes.

Figure 1

Examples of iron limitation in the ocean as evidenced by rapid growth of diatoms and other plankton after iron fertilization experiments. Circle color indicates dominant plankton in resultant blooms: orange – diatoms; green – picophytoplankton; pink – zooplankton. 1 – IronEx-I, 1993; 2 – IronEx-II, 1995; 3 – SOIREE, 1999; 4 – EisenEx, 2000; 5 – SEEDS-I, 2001; 6 – SERIES, 2002; 7 – SOFeX North, 2002; 8 – SOFeX South, 2002; 9 – SEEDS-II, 2004; 10 – EIFEX, 2004; 11 – SAGE, 2004; 12 – PAPA-SEEDS, 2006; 13 – LOHAFEX, 2009. Adapted from Trick et al. (2010).

Figure 2

Potential iron homeostasis systems in marine cyanobacteria, as predicted by genomic analyses. At least in part, iron uptake in cyanobacteria is likely facilitated by the concentration of Fe(III) in the periplasmic space by FutA, followed by transport into the cytoplasm by the FutB/FutC ABC transporter system. The presence of FeoA/B genes in marine cyanobacteria genomes suggests Fe(II) uptake could also occur. Finally, the Synechococcus sp. PCC 7002 genome contains genes for siderophore biosynthesis, as well as Fe-siderophore (Fe-S.) uptake via a TonB dependent receptor system. Within the cell, iron could be sequestered by bacterioferritin and Dps.

Figure 3

Potential iron homeostasis systems in marine diatoms, as predicted by genomic analyses. Iron-regulated ferric reductase genes have been identified in T. pseudonana and P. tricornutum. These could reduce Fe(III) and Fe bound by siderophores (Fe–S), as could photoreduction (hv). Fe(II) could then enter the cytoplasm through iron-regulated transporters: ZIP in P. tricornutum, and NRAMP in T. pseudonana (although if TpNRAMP is localized to the tonoplast, it could also serve to release iron from the vacuole during iron starvation). In T. pseudonana, extracellular Fe(II) could also be reoxidized and transported through a yeast-like Fe(III) uptake system, utilizing the iron-regulated multi-copper ferroxidase (TpFET3) and Fe(III) permeases (TpFTR1 and TpFTR2). If ferritin is present (it is present in some pennate diatom genomes, but not in T. pseudonana), it can store iron, likely in the plastid.