Abstract
BackgroundEpulopiscium sp. type B, a large intestinal bacterial symbiont of the surgeonfish Naso tonganus, does not reproduce by binary fission. Instead, it forms multiple intracellular offspring using a process with morphological features similar to the survival strategy of endospore formation in other Firmicutes. We hypothesize that intracellular offspring formation in Epulopiscium evolved from endospore formation and these two developmental programs share molecular mechanisms that are responsible for the observed morphological similarities.ResultsTo test this, we sequenced the genome of Epulopiscium sp. type B to draft quality. Comparative analysis with the complete genome of its close, endospore-forming relative, Cellulosilyticum lentocellum, identified homologs of well-known sporulation genes characterized in Bacillus subtilis. Of the 147 highly conserved B. subtilis sporulation genes used in this analysis, we found 57 homologs in the Epulopiscium genome and 87 homologs in the C. lentocellum genome.ConclusionsGenes coding for components of the central regulatory network which govern the expression of forespore and mother-cell-specific sporulation genes and the machinery used for engulfment appear best conserved. Low conservation of genes expressed late in endospore formation, particularly those that confer resistance properties and encode germinant receptors, suggest that Epulopiscium has lost the ability to form a mature spore. Our findings provide a framework for understanding the evolution of a novel form of cellular reproduction.
Highlights
Epulopiscium sp. type B, a large intestinal bacterial symbiont of the surgeonfish Naso tonganus, does not reproduce by binary fission
The comparative analysis of the draft Epulopiscium sp. type B genome with the complete C. lentocellum genome substantiates our hypothesis that the production of intracellular offspring in Epulopiscium evolved from endospore formation
All of the genes identified in C. lentocellum that function in engulfment as well as the core transcriptional regulatory cascade, and the associated intracellular communication network that coordinates sigma factor activation, were found in the Epulopiscium genome
Summary
Epulopiscium sp. type B, a large intestinal bacterial symbiont of the surgeonfish Naso tonganus, does not reproduce by binary fission. Type B, a large intestinal bacterial symbiont of the surgeonfish Naso tonganus, does not reproduce by binary fission Instead, it forms multiple intracellular offspring using a process with morphological features similar to the survival strategy of endospore formation in other Firmicutes. Endospores endure environmental conditions that would kill most other bacterial cells, including prolonged periods of insufficient nutrients, moderate levels of organic solvents, exposure to phage, extremes in pH, proteases and cell wall degrading enzymes, freezing, desiccation and excessive heat or radiation [3,4] This form of sporulation preserves the genome in a remarkably dispersible and dormant cell type that can resume vegetative growth when the environment improves. These multicellular filaments live attached to the lining of the small intestine, and to disperse or reposition itself in the gut, each cell in a filament forms either an endospore containing two cells or two non-dormant intracellular offspring [7,8]
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