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Published online on April 29, 2008, 10.1073/pnas.0707522105

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MICROBIOLOGY
Extreme polyploidy in a large bacterium

Jennifer E. Mendell*, Kendall D. Clements{dagger}, J. Howard Choat{ddagger}, and Esther R. Angert*,§

*Department of Microbiology, Cornell University, Ithaca, NY 14853; {dagger}School of Biological Sciences, University of Auckland, Auckland 1142, New Zealand; and {ddagger}School of Marine and Tropical Biology, James Cook University, Townsville, Queensland 4811, Australia

Edited by James M. Tiedje, Michigan State University, East Lansing, MI, and approved March 11, 2008 (received for review August 10, 2007)

Abstract

Cells rely on diffusion to move metabolites and biomolecules. Diffusion is highly efficient but only over short distances. Although eukaryotic cells have broken free of diffusion-dictated constraints on cell size, most bacteria and archaea are forced to remain small. Exceptions to this rule are found among the bacterial symbionts of surgeonfish; Epulopiscium spp. are cigar-shaped cells that reach lengths in excess of 600 µm. A large Epulopiscium contains thousands of times more DNA than a bacterium such as Escherichia coli, but the composition of this DNA is not well understood. Here, we present evidence that Epulopiscium contains tens of thousands of copies of its genome. Using quantitative, single-cell PCR assays targeting single-copy genes, we have determined that copy number is positively correlated with Epulopiscium cell size. Although other bacteria are known to possess multiple genomes, polyploidy of the magnitude observed in Epulopiscium is unprecedented. The arrangement of genomes around the cell periphery may permit regional responses to local stimuli, thus allowing Epulopiscium to maintain its unusually large size. Surveys of the sequences of single-copy genes (dnaA, recA, and ftsZ) revealed genetic homogeneity within a cell consistent with only a small amount ({approx}1%) of the parental DNA being transferred to the next generation. The results also suggest that the abundance of genome copies in Epulopiscium may allow for an unstable genetic feature, a long mononucleotide tract, in an essential gene. With the evolution of extreme polyploidy and large cell size, Epulopiscium has acquired some of the advantages of eukaryotic cells.

dnaA | Epulopiscium | large bacteria | mononucleotide repeat | polyploid


Footnotes

Author contributions: J.E.M. and E.R.A. designed research; J.E.M., K.D.C., and J.H.C. performed research; and J.E.M., K.D.C., J.H.C., and E.R.A. wrote the paper.

The authors declare no conflict of interest.

This article is a PNAS Direct Submission.

§To whom correspondence should be addressed. E-mail: era23{at}cornell.edu

© 2008 by The National Academy of Sciences of the USA


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