Challenges faced by highly polyploid bacteria with limits on DNA inheritance

Abstract

Abstract Most studies of bacterial reproduction have centered on organisms that undergo binary fission. In these models, complete chromosome copies are segregated with great fidelity into two equivalent offspring cells. All genetic material is passed on to offspring, including new mutations and horizontally acquired sequences. However, some bacterial lineages employ diverse reproductive patterns that require management and segregation of more than two chromosome copies. Epulopiscium spp., and their close relatives within the Firmicutes phylum, are intestinal symbionts of surgeonfish (family Acanthuridae). Each of these giant (up to 0.6 mm long), cigar-shaped bacteria contains tens of thousands of chromosome copies. Epulopiscium spp. do not use binary fission but instead produce multiple intracellular offspring. Only ∼1% of the genetic material in an Epulopiscium sp. type B mother cell is directly inherited by its offspring cells. And yet, even in late stages of offspring development, mother-cell chromosome copies continue to replicate. Consequently, chromosomes take on a somatic or germline role. Epulopiscium sp. type B is a strict anaerobe and while it is an obligate symbiont, its host has a facultative association with this intestinal microorganism. Therefore, Epulopiscium sp. type B populations face several bottlenecks that could endanger their diversity and resilience. Multilocus sequence analyses revealed that recombination is important to diversification in populations of Epulopiscium sp. type B. By employing mechanisms common to others in the Firmicutes, the coordinated timing of mother-cell lysis, offspring development and congression may facilitate the substantial recombination observed in Epulopiscium sp. type B populations.