Cyanobacterial Siderophores-Physiology, Structure, Biosynthesis, and Applications

Abstract

Siderophores are low-molecular-weight metal chelators that function in microbial iron uptake. As iron limits primary productivity in many environments, siderophores are of great ecological importance. Additionally, their metal binding properties have attracted interest for uses in medicine and bioremediation. Here, we review the current state of knowledge concerning the siderophores produced by cyanobacteria. We give an overview of all cyanobacterial species with known siderophore production, finding siderophores produced in all but the most basal clades, and in a wide variety of environments. We explore what is known about the structure, biosynthesis, and cycling of the cyanobacterial siderophores that have been characterized: Synechobactin, schizokinen and anachelin. We also highlight alternative siderophore functionality and technological potential, finding allelopathic effects on competing phytoplankton and likely roles in limiting heavy-metal toxicity. Methodological improvements in siderophore characterization and detection are briefly described. Since most known cyanobacterial siderophores have not been structurally characterized, the application of mass spectrometry techniques will likely reveal a breadth of variation within these important molecules.

Keywords: Anabaena; Synechococcus; anachelin; cyanobacteria; schizokinen; siderophore; synechobactin.

Figure 1

The structures of schizokinen, produced by some Anabaena strains, and synechobactin A produced by Synechococcus sp. PCC 7002. Iron-binding oxygen-atoms are marked in red. The synechobactins are a suite of siderophores with different fatty-acid chain lengths in the (*) marked position.

Figure 2

The structures of the catecholate siderophores anachelin, which are produced by Anabaena cylindrica. Anachelins have a tripartite structure, composed of a polyketide (blue), a tripeptide (black) and an alkaloid containing the iron binding catechol moiety (green).

Figure 3

A cartoon demonstrating synthesis of peptide chains by non-ribosomal peptide synthases (NRPS) by a sequence of modules. Amino-acids are activated by the adenylation domain (A), transferred by the peptidyl carrier domain (PCP) and bound to each other by condensation domain (C). A final thioesterase (TE) domain releases the peptide. (Created with Biorender.com).

Figure 4

An overview of siderophore cycling in a generic organism. Typically, iron-loaded siderophores are imported through TonB-dependent transporters (TBDT) in the outer membrane, with power supplied by a TonB-ExbB-ExbD-complex in the inner membrane. Further transport is done by ABC-transporters. Export of siderophores can happen by a variety of transporter types. Note that the iron is reduced to Fe²⁺ at some point during this cycle, but the timing and location of this is often not clear. Created with Biorender.com.

Figure 5

The overview of known siderophores with associated organisms, cell morphology, habitat and phylogenetic association. The type of siderophore is only determined structurally in a few organisms (indicated by asterisks). The phylogenetic class designations (A–G) from References [96] have been used. In classes where no siderophore-producing organisms are known, representative species are indicated. A question mark (“?”) indicates that the type of siderophore is not known. Species names of the original studies are shown, with updated species names indicated by “=”. Where genetic data is not available, proxy-species with known phylogenetic positions were assigned based on described characteristics of the organism.