Caldora penicillata gen. nov., comb. nov. (cyanobacteria), a pantropical marine species with biomedical relevance

Abstract

Many tropical marine cyanobacteria are prolific producers of bioactive secondary metabolites with ecological relevance and promising pharmaceutical applications. One species of chemically rich, tropical marine cyanobacteria that was previously identified as Symploca hydnoides or Symploca sp. corresponds to the traditional taxonomic definition of Phormidium penicillatum. In this study, we clarified the taxonomy of this biomedically and ecologically important cyanobacterium by comparing recently collected specimens with the original type material and the taxonomic description of P. penicillatum. Molecular phylogenetic analyses of the 16S rRNA gene and the 16S-23S internal transcribed spacer regions showed that P. penicillatum formed an independent clade sister to the genus Symploca, and distantly related to Phormidium and Lyngbya. We propose the new genus Caldora for this clade, with Caldora penicillata comb. nov. as the type species and designate as the epitype the recently collected strain FK13-1. Furthermore, the production of bioactive secondary metabolites among various geographically dispersed collections of C. penicillata showed that this species consistently produced the metabolite dolastatin 10 and/or the related compound symplostatin 1, which appear to be robust autapomorphic characters and chemotaxonomic markers for this taxon.

Fig. 1

Environmental pictures illustrating morphological variability in shape and coloration between different Caldora penicillata specimens. Note external parts of specimens vary in color between reddish, greenish, to orange, while internal bases are always whitish or colorless. (a) Amorphic puffball-shaped specimen (BCBC11-25) growing on gorgonians of South Water Cay, Belize. (b) Small puffball-shaped tufts of C. penicillata attached to corals. (c) C. penicillata with feathery morphology and red coloration growing on shallow coral reef at Looe Key, FL (courtesy of B. Lapointe). (d) C. penicillata on coral reef at Carrie Bow Cay, Belize (courtesy of A. Wood). (e) C. penicillata on gorgonians of Miskito keys, Honduras (courtesy of Z. Foltz). (f) Greenish C. penicillata specimen (NAB11-29) on hard-bottom on a shallow-water reef of Lac Bay, Bonaire.

Fig. 2

Morphological characterization of external and internal sections of Caldora penicillata strain FK12-26. (a) Underwater picture of C. penicilla attached to gorgonians at depth of 7-8 m at Looe Key, FL (courtesy of B. Lapointe). Arrows highlight sections used for scanning electron microscopy (SEM) imaging in b-d. (b) Whitish, mucilaginous interior bases composed of empty polysaccharide sheath material. (c) Exterior section of cyanobacterial thallus, predominantly containing live, pigmented filaments. (d) Higher resolution SEM image of C. penicillata filaments. (e) Light microscopic image of C. penicillata filaments. (f) Consortium of C. penicillata filaments mixed with other filamentous cyanobacteria. Scale bars: (b) 100 μm, (c) 100 μm, (d) 20 μm, (e) 15 μm, and (f) 22 μm.

Fig. 3

Evolutionary tree based on SSU (16S) rRNA gene sequences with Caldora penicillata as well as Symploca, Lyngbya, and Phormidium clades highlighted with gray boxes. Phylogenetic inferences were performed using Bayesian Inference (BI) and Maximum Likelihood (ML) analyses. Support values are indicated at the nodes as posterior probability and bootstrap support. Reference strains are designated as (^R) and type strains as (^T). Unicellular Gloeobacter violaceus PCC 7421^R strain (GenBank acc. nr. NC005125) was outgroup. Specimens indicated as species or strain; GenBank accession numbers in brackets. Scale bar depicts 0.04 expected nucleotide substitutions per site using GTR+I+G substitution model.

Fig. 4

Phylogenetic inference of Caldora penicillata specimens based on 16S-23S internal transcribed spacer (ITS) regions highlighted in gray box, as well as Symploca, Lyngbya, and Phormidium clades. Support values indicated as posterior probability (BI) and bootstrap support (ML). Scale bar indicates 0.02 expected nucleotide substitutions per site using GTR+G substitution model.

Fig. 5

Molecular structures of bioactive secondary metabolites dolastatin 10, symplostatin 1, and largazole; distribution of compounds among Caldora penicillata specimens shown in Table 1.