Cyanochelin B: A siderophore produced by cyanobacterium Leptolyngbya sp. NIES-3755 with photolytic properties that negate iron monopolization in the UV-light

Abstract

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 employ {beta}-hydroxy-aspartate ({beta}-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 {beta}-OH-Asp-containing siderophore produced by filamentous cyanobacterium Leptolyngbya sp. NIES-3755. A combination of nuclear magnetic resonance, high resolution mass spectrometry and bioinformatic analyses complemented with Marfeys and Muratas 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-cultured Leptolyngbya together with Synechocystis PCC6803 as a reporter strain lacking siderophore production. The cultivation setup was based on membrane-separated compartments accommodating individual strains and employed alginate-embedded FeCl3 to simulate poorly accessible precipitated iron. Our results demonstrate that in the absence of UV-light cyanochelin B can monopolize iron in favor of Leptolyngbya. 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 of Phormidesmis from field material and discuss the phenomenon of photolytic siderophores in a broader context. ImportanceIron 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 {beta}-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 {beta}-OH-Asp and can function in a similar way.