Phylogenetic inferences reveal a large extent of novel biodiversity in chemically rich tropical marine cyanobacteria

Abstract

Benthic marine cyanobacteria are known for their prolific biosynthetic capacities to produce structurally diverse secondary metabolites with biomedical application and their ability to form cyanobacterial harmful algal blooms. In an effort to provide taxonomic clarity to better guide future natural product drug discovery investigations and harmful algal bloom monitoring, this study investigated the taxonomy of tropical and subtropical natural product-producing marine cyanobacteria on the basis of their evolutionary relatedness. Our phylogenetic inferences of marine cyanobacterial strains responsible for over 100 bioactive secondary metabolites revealed an uneven taxonomic distribution, with a few groups being responsible for the vast majority of these molecules. Our data also suggest a high degree of novel biodiversity among natural product-producing strains that was previously overlooked by traditional morphology-based taxonomic approaches. This unrecognized biodiversity is primarily due to a lack of proper classification systems since the taxonomy of tropical and subtropical, benthic marine cyanobacteria has only recently been analyzed by phylogenetic methods. This evolutionary study provides a framework for a more robust classification system to better understand the taxonomy of tropical and subtropical marine cyanobacteria and the distribution of natural products in marine cyanobacteria.

Fig 1

Evolutionary tree of marine cyanobacteria known to produce NPs. The main NP-producing groups (highlighted with blue boxes) are placed in perspective with other cyanobacterial groups, in particular, their corresponding reference strains or type strains (highlighted with green boxes). The phylogram is based on SSU (16S) rRNA gene sequences using the Bayesian method (MrBayes), and the support values are indicated as posterior probabilities at the nodes. Note that gene sequences of <1,250 bp are removed in this analysis. All gene sequences from Table 1, including those of clades V, VI, and VIII, are available in Fig. S1 in the supplemental material. The specimens are indicated as species and strain (GenBank accession number). The scale bar indicates 0.05 expected nucleotide substitutions per site.

Fig 2

Taxonomic distribution of NPs in marine cyanobacteria on the basis of the published taxonomy of all (n = 533) marine cyanobacteria available in the 2011 Marine Literature Database (a) and NP-producing strains phylogenetically inferred in this study (n = 126) (b).