Morphological, Chemical, and Genetic Diversity of Tropical Marine Cyanobacteria Lyngbya spp. and Symploca spp. ( Oscillatoriales )

Abstract

Although diverse natural products have been isolated from the benthic, filamentous cyanobacterium Lyngbya majuscula, it is unclear whether this chemical variation can be used to establish taxonomic relationships among disparate collections. We compared morphological characteristics, secondary-metabolite compositions, and partial 16S ribosomal DNA (rDNA) sequences among several collections of L. majuscula Gomont, Lyngbya spp., and Symploca spp. from Guam and the Republic of Palau. The morphological characteristics examined were cell length, cell width, and the presence or absence of a calyptra. Secondary metabolites were analyzed by twodimensional thin-layer chromatography. Each collection possessed a distinct cellular morphology that readily distinguished Lyngbya spp. from Symploca spp. Each collection yielded a unique chemotype, but common chemical characteristics were shared among four collections of L. majuscula. A phylogeny based on secondarymetabolite composition supported the reciprocal monophyly of Lyngbya and Symploca but yielded a basal polytomy for Lyngbya. Pairwise sequence divergence among species ranged from 10 to 14% across 605 bp of 16S rDNA, while collections of L. majuscula showed 0 to 1.3% divergence. Although the phylogeny of 16S rDNA sequences strongly supported the reciprocal monophyly of Lyngbya and Symploca as well as the monophyly of Lyngbya bouillonii and L. majuscula, genetic divergence was not correlated with chemical and morphological differences. These data suggest that 16S rDNA sequence analyses do not predict chemical variability among Lyngbya species. Other mechanisms, including higher rates of evolution for biosynthetic genes, horizontal gene transfer, and interactions between different genotypes and environmental conditions, may play important roles in generating qualitative and quantitative chemical variation within and among Lyngbya species.The benthic, filamentous cyanobacterium Lyngbya majuscula Gomont is distributed throughout the tropics in reef and lagoonal habitats (18,61,62), often forming dense mats that carpet benthic substrates. L. majuscula can compete with macroalgae (59) and is unpalatable to fish, crabs, urchins, and other macroherbivores (43,50,57). However, specialized mesoherbivores, such as the sea hare Stylocheilus striatus, may preferentially consume L. majuscula (8,41,51). Secondary metabolites produced by L. majuscula are responsible for both the deterrence of feeding by macroherbivores and the stimulation of feeding by mesoherbivores (41,51,57).Over 100 novel secondary metabolites have been isolated from collections of L. majuscula. Although these collections have been globally distributed, there is little evidence that any given types of secondary metabolites are associated with specific geographic regions (10). Indeed, collections within limited geographic areas are often extremely diverse. On Guam, L. majuscula collections have yielded indanone metabolites (45), lyngbyastatins (16,27,64), malyngamides (4, 5, 38), malyngolide (7), majusculamides (35), ...

Phylogenetic and Chemical Diversity of Three Chemotypes of Bloom-Forming Lyngbya Species ( Cyanobacteria : Oscillatoriales ) from Reefs of Southeastern Florida

“…Taxonomic studies of the Oscillatoriales, which includes many chemically rich species in genera such as Lyngbya, Oscillatoria, and Phormidium, have conventionally been based on morphological characteristics, including cell length and width, colony formation, extracellular sheath width, and pigmentation. Unfortunately, these diagnostic features exhibit plasticity in response to environmental parameters such as salinity, turbidity, and nutrient content (44,54,59). Molecular approaches to taxonomy, based on nitrogenase (nifH) and 16S rRNA gene sequences (18,24,25,59,63,64) and random amplified polymorphic DNA analysis (6,40), have revealed enormous phylogenetic diversity among environmental cyanobacteria not indicated by morphological classifications, suggesting that cyanobacterial taxonomy remains widely unresolved.…”

“…Unfortunately, these diagnostic features exhibit plasticity in response to environmental parameters such as salinity, turbidity, and nutrient content (44,54,59). Molecular approaches to taxonomy, based on nitrogenase (nifH) and 16S rRNA gene sequences (18,24,25,59,63,64) and random amplified polymorphic DNA analysis (6,40), have revealed enormous phylogenetic diversity among environmental cyanobacteria not indicated by morphological classifications, suggesting that cyanobacterial taxonomy remains widely unresolved. As a result, it has been a challenge to identify species-specific patterns of bioactive compound production in the Oscillatoriales.…”

Pharmacology and toxicology of pahayokolide A, a bioactive metabolite from a freshwater species of Lyngbya isolated from the Florida Everglades

“…Although well over 100 compounds have been isolated from L. majuscula and other marine species of Lyngbya (Thacker and Paul, 2004), very few have been reported from freshwater species, and, to the authors' knowledge, this is the first such compound to be purified and characterized from an Everglades isolate. That said, a survey of microalgae (Lewis et al, 2004) in the Everglades-Florida Bay transition zone identified Lyngbya as one of the dominant members of the benthic and periphyton communities in this area.…”

“…A number of compounds from Lyngbya are currently being investigated with respect to potential pharmaceutical development, as well as to human and environmental health implications of these compounds as naturally occurring toxins (Moore, 1996;Gerwick et al, 2001;Mayer and Gustafson, 2003;Shimizu, 2003;Thacker and Paul, 2004). Pharmacological activity of such Lyngbya-derived compounds ranges from microtubule inhibitors, such as curacin A (Gerwick et al, 1994), to potent sodium channel blockers and activators, such as kalkitoxin (Wu et al, 2000) and antillatoxin (Li et al, 2001).…”

“…However, the majority of the investigations on biologically active compounds from Lyngbya have focused only on a limited number of marine species (Moore, 1996;Gerwick et al, 2001;Thacker and Paul, 2004). To our knowledge, the pahayokolides are the first bioactive metabolites to be identified from a Lyngbya species from the Florida Everglades.…”