Abstract
Some cyanobacteria are capable of differentiating a variety of cell types in response to environmental factors. For instance, in low nitrogen conditions, some cyanobacteria form heterocysts, which are specialized for N2 fixation. Many heterocyst-forming cyanobacteria have DNA elements interrupting key N2 fixation genes, elements that are excised during heterocyst differentiation. While the mechanism for the excision of the element has been well-studied, many questions remain regarding the introduction of the elements into the cyanobacterial lineage and whether they have been retained ever since or have been lost and reintroduced. To examine the evolutionary relationships and possible function of DNA sequences that interrupt genes of heterocyst-forming cyanobacteria, we identified and compared 101 interruption element sequences within genes from 38 heterocyst-forming cyanobacterial genomes. The interruption element lengths ranged from about 1 kb (the minimum able to encode the recombinase responsible for element excision), up to nearly 1 Mb. The recombinase gene sequences served as genetic markers that were common across the interruption elements and were used to track element evolution. Elements were found that interrupted 22 different orthologs, only five of which had been previously observed to be interrupted by an element. Most of the newly identified interrupted orthologs encode proteins that have been shown to have heterocyst-specific activity. However, the presence of interruption elements within genes with no known role in N2 fixation, as well as in three non-heterocyst-forming cyanobacteria, indicates that the processes that trigger the excision of elements may not be limited to heterocyst development or that the elements move randomly within genomes. This comprehensive analysis provides the framework to study the history and behavior of these unique sequences, and offers new insight regarding the frequency and persistence of interruption elements in heterocyst-forming cyanobacteria.
Highlights
Interruption Elements in Cyanobacterial Genomes. Cyanobacteria can alter their cell shape and size, cell wall thickness, and filament orientation in response to environmental conditions varying from nutrient limitation to predation [1,2,3]
We identified 101 interruption elements within 28 genomes of heterocyst-forming cyanobacteria, while an additional 10 genomes did not have any observed elements (Fig 2)
A lack of homology between the two recombinase superfamilies implies at least two distinct origins and evolutionary paths of interruption elements in heterocystforming cyanobacterial ancestry
Summary
Cyanobacteria can alter their cell shape and size, cell wall thickness, and filament orientation in response to environmental conditions varying from nutrient limitation to predation [1,2,3]. The morphological diversity of cyanobacteria extends to cell differentiation as some filamentous cyanobacteria can form akinetes, hormogonia, and heterocysts, in addition to vegetative cells. Akinetes are spore-like cells formed during unfavorable growth conditions [4], while hormogonia are small-celled, motile filaments that are especially important in symbiosis initiation [5]. Heterocysts are the sites of N2 fixation under nitrogen (N) limitation [6]. N2 fixation, the process of converting N2 to NH3, can be a means of avoiding a common nutrient limitation for microbial growth in a variety of environments [7,8]. Heterocysts create and maintain a microoxic microenvironment by shutting down the activity of O2evolving photosystem II, increasing respiratory O2 uptake, and creating a thick envelope around the cell wall to restrict gas diffusion [6]
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