Nocturnal Production of Endospores in Natural Populations ofEpulopiscium-Like Surgeonfish Symbionts

Abstract

Prior studies have described a morphologically diverse group of intestinal microorganisms associated with surgeonfish. Despite their diversity of form, 16S rRNA gene surveys and fluorescent in situ hybridizations indicate that these bacteria are low-G؉C gram-positive bacteria related to Epulopiscium spp. Many of these bacteria exhibit an unusual mode of reproduction, developing multiple offspring intracellularly. Previous reports have suggested that some Epulopiscium-like symbionts produce dormant or phase-bright intracellular offspring. Close relatives of Epulopiscium, such as Metabacterium polyspora and Clostridium lentocellum, are endospore-forming bacteria, which raises the possibility that the phase-bright offspring are endospores. Structural evidence and the presence of dipicolinic acid demonstrate that phase-bright offspring of Epulopiscium-like bacteria are true endospores. In addition, endospores are formed as part of the normal daily life cycle of these bacteria. In the populations studied, mature endospores were seen only at night and the majority of cells in a given population produced one or two endospores per mother cell. Phylogenetic analyses confirmed the close relationship between the endospore-forming surgeonfish symbionts characterized here and previously described Epulopiscium spp. The broad distribution of endospore formation among the Epulopiscium phylogenetic group raises the possibility that sporulation is a characteristic of the group. We speculate that spore formation in Epulopiscium-like symbionts may be important for dispersal and may also enhance survival in the changing conditions of the fish intestinal tract.

Sporulation during Growth in a Gut Isolate of Bacillus subtilis

“…Several species or morphotypes of Epulopiscium, an intestinal symbiont of the surgeonfish, are also known to use endospore formation as a form of survival and dispersion. For Epulopiscium-like organisms, endospore differentiation is closely coordinated with fish behavior and follows a circadian rhythm, which enhances dispersal to additional host fish (64,65). Other intestinal symbionts of mammals, termed "segmented filamentous bacteria," which are related to the Clostridia, may also produce multiple endospores (66)(67)(68)(69)(70)(71).…”

Polyploidy in Archaea and Bacteria: About Desiccation Resistance, Giant Cell Size, Long-Term Survival, Enforcement by a Eukaryotic Host and Additional Aspects

“…Epulopiscium is not only exceptional because of its giant cell size and hyperpolyploidy but also because of its unusual way of reproduction [Angert, 2012;Angert and Clements, 2004;Bresler et al, 1998;Flint et al, 2005;Ward , 2009]. In short, small offspring cells are generated at the cell poles, which are engulfed by the mother cell.…”

Transcriptional patterns in both host and bacterium underlie a daily rhythm of anatomical and metabolic change in a beneficial symbiosis

“…In contrast, extracellular symbioses, such as those in animal gut tracts or light-emitting organs, often have connections to the external environment through which excess cells produced by a growing symbiont population are released (3,4). In such symbioses, the host may assure stability by controlling symbiont number and/or activity on a daily, or ''diel,'' rhythm (5,6).…”