Cyanochelin B: A siderophore produced by cyanobacteriumLeptolyngbyasp. NIES-3755 with photolytic properties that negate iron monopolization in the UV-light
Authors: Falcao Berness P. , Matteo Viviana Di , Hrouzek Pavel , Štenclová Lenka , Urajová Petra , Mareš Jan , Kuta Jan , Yerena José Alberto Martínez , Kozlíková-Zapomělová Eliška , Esposito Germana , Mangoni Alfonso , Costantino Valeria , Galica Tomáš 
Published: January 2025

Siderophores are low-molecular-weight compounds excreted by microorganisms to facilitate iron uptake in times of its unavailability. Microbes may produce siderophores to monopolize iron and achieve competitive exclusion of other strains. Alternatively, siderophores may be exchanged for other substrates in mutualistic relationships. Siderophores that employβ-hydroxy-aspartate (β-OH-Asp) for iron chelation were shown to undergo UV-mediated photolytic cleavage with simultaneous reduction of Fe3+to Fe2+. Photolytic siderophores can mediate algal-bacterial mutualism, where the bacteria provide iron in exchange for dissolved organic carbon.

We use an interdisciplinary strategy to provide a complex characterization of cyanochelin B, a photolytic β-OH-Asp-containing siderophore produced by filamentous cyanobacteriumLeptolyngbyasp. NIES-3755. A combination of nuclear magnetic resonance, high resolution mass spectrometry and bioinformatic analyses complemented with Marfey’s and Murata’s methods yielded the structure of cyanochelin B with the configuration of its stereocenters. Cyanochelin B-iron complexes exposed to UV- light photolyze within minutes (t1/2= 8.9 min; ∼3.5 uE UV-A) and release reduced Fe2+. We have co-culturedLeptolyngbyatogether withSynechocystisPCC6803 as a reporter strain lacking siderophore production. The cultivation setup was based on membrane-separated compartments accommodating individual strains and employed alginate-embedded FeCl3to simulate poorly accessible precipitated iron. Our results demonstrate that in the absence of UV-light cyanochelin B can monopolize iron in favor ofLeptolyngbya.However, UV-light eliminates any monopolization of iron and makes it available to competing organisms. Finally, we report the isolation of novel cyanochelin B-producing strains ofPhormidesmisfrom field material and discuss the phenomenon of photolytic siderophores in a broader context.

Importance

Iron is an essential micronutrient that is required by all living organisms as a cofactor of indispensable enzymes. Due to its specific properties it is mostly precipitated and biologically unavailable. To facilitate iron uptake, microbes produce siderophores - low-molecular-weight compounds that bind iron. Siderophores are mediators of microbial interactions and facilitate competitive exclusion of non-compatible strains or foster mutualistic partners and cheater strains. We report a full structural elucidation of cyanochelin B, a photolytic cyanobacterial siderophore that contains β-OH-Asp. Our co-culture experiments show that cyanochelin B may monopolize iron to its producer or make it accessible to other strains depending on the presence of UV light. Moreover, our data suggest that the benefits from production of photolytic siderophores are not restricted to symbiotic partners of the producer but rather available to the whole irradiated community. Of known siderophores, 17.5% contain the photoreactive β-OH-Asp and can function in a similar way.