Diversity of bioactive compound content across 71 genera of marine, freshwater, and terrestrial cyanobacteria

Abstract

Cyanobacterial blooms have increased in frequency, distribution, and intensity due to climate change and anthropogenic nutrient input. The release of bioactive compounds accumulated in these blooms can affect the health of humans and the environment. The co-occurrence of bioactive metabolites is well-documented in bloom samples from marine and freshwater ecosystems, with fewer reports from unialgal isolates. Cyanobacteria also are important terrestrial ecosystem components, especially in drylands, but reports on bioactive molecules from terrestrial cyanobacteria are sparse. This study determined bioactive metabolite profiles for 71 genera of cyanobacteria from seven orders isolated from freshwater (12 genera), marine (15 genera), and terrestrial (44 genera) habitats originally. Cultures were harvested for bioactive metabolites when entering the late-exponential phase for all 157 strains, and 33 were sampled at both early and late exponential phases. Bioactive metabolites were analyzed using an ultra high performance/pressure liquid chromatography in-line with a time-of-flight mass spectrometer. Overall, 12 bioactive classes of the 28 identified were ubiquitous in all samples. On average, each freshwater genus produced ∼12 bioactive classes, whereas each marine genus contained > 4 bioactive classes, and each terrestrial genus contained ∼6 bioactive classes. While 10 of 12 freshwater genera produced at least 10 bioactive classes, only a single genus each from marine and terrestrial habitats had the same number of bioactive classed accumulated. Aeruginosin was found in 58 of 71 total genera, carmabin in 51 of 71 genera, and anabaenopeptin in 48 of 71 genera. Chemotaxonomic use of these secondary metabolites may help resolve higher-level genetic classification(s). An additional growth curve experiment showed that bioactive metabolites were produced at both early and late exponential growth phases. The bioactive metabolite accumulation pattern between early and late exponential phases differed by bioactive classes, genera, and habitats. This survey of 55 bioactive classes in cyanobacteria isolated from freshwater, marine, and terrestrial habitats (71 genera) provides as one of the first systematic bioactive metabolite profiles for cyanobacteria, which should be useful in environmental and drinking water management. Further, it offers novel insights about the toxin potential of selected terrestrial cyanobacteria.