Abstract
Cyanobacterial morphology is diverse, ranging from unicellular spheres or rods to multicellular structures such as colonies and filaments. Multicellular species represent an evolutionary strategy to differentiate and compartmentalize certain metabolic functions for reproduction and nitrogen (N2) fixation into specialized cell types (e.g. akinetes, heterocysts and diazocytes). Only a few filamentous, differentiated cyanobacterial species, with genome sizes over 5 Mb, have been sequenced. We sequenced the genomes of two strains of closely related filamentous cyanobacterial species to yield further insights into the molecular basis of the traits of N2 fixation, filament formation and cell differentiation. Cylindrospermopsis raciborskii CS-505 is a cylindrospermopsin-producing strain from Australia, whereas Raphidiopsis brookii D9 from Brazil synthesizes neurotoxins associated with paralytic shellfish poisoning (PSP). Despite their different morphology, toxin composition and disjunct geographical distribution, these strains form a monophyletic group. With genome sizes of approximately 3.9 (CS-505) and 3.2 (D9) Mb, these are the smallest genomes described for free-living filamentous cyanobacteria. We observed remarkable gene order conservation (synteny) between these genomes despite the difference in repetitive element content, which accounts for most of the genome size difference between them. We show here that the strains share a specific set of 2539 genes with >90% average nucleotide identity. The fact that the CS-505 and D9 genomes are small and streamlined compared to those of other filamentous cyanobacterial species and the lack of the ability for heterocyst formation in strain D9 allowed us to define a core set of genes responsible for each trait in filamentous species. We presume that in strain D9 the ability to form proper heterocysts was secondarily lost together with N2 fixation capacity. Further comparisons to all available cyanobacterial genomes covering almost the entire evolutionary branch revealed a common minimal gene set for each of these cyanobacterial traits.
Highlights
Cyanobacteria are among the most successful primary producing aquatic organisms, having populated the Earth for approximately 2.8 billion years [1]
Cyanobacteria are responsible for noxious or harmful algal blooms (HABs), and this phenomenon is compounded by the fact that some cyanobacteria produce potent cyanotoxins, which have been classified according to their mode of action and effects on mammals [2]
Our results strongly indicate that this organism could be the closest ancestor of filamentous cyanobacteria
Summary
Cyanobacteria are among the most successful primary producing aquatic organisms, having populated the Earth for approximately 2.8 billion years [1]. Cyanobacteria have evolved alternative morphologies, including unicellular and diverse multicellular forms ranging from simple colonies to branched filaments. Phylogenetic analysis has suggested that cyanobacteria capable of cell differentiation are monophyletic [3]. Within this monophyletic group some cyanobacteria further evolved from filaments in which a small number of vegetative cells differentiated into either heterocysts or akinetes (resting stages). When mineral and organic nitrogen sources, such as nitrate or ammonium, are depleted from the growth medium, some filamentous cyanobacteria maintain photosynthetic activity (including O2 generation) in vegetative cells and differentiate heterocysts to provide an anoxic environment suitable for N2 fixation [6]
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