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Research Article

Polynucleobacter necessarius, a model for genome reduction in both free-living and symbiotic bacteria

Vittorio Boscaro, Michele Felletti, Claudia Vannini, Matthew S. Ackerman, Patrick S. G. Chain, Stephanie Malfatti, Lisa M. Vergez, Maria Shin, Thomas G. Doak, Michael Lynch, and Giulio Petroni
PNAS first published October 28, 2013; https://doi.org/10.1073/pnas.1316687110
Vittorio Boscaro
aDepartment of Biology, Pisa University, 56126 Pisa, Italy;
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Michele Felletti
aDepartment of Biology, Pisa University, 56126 Pisa, Italy;
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Claudia Vannini
aDepartment of Biology, Pisa University, 56126 Pisa, Italy;
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Matthew S. Ackerman
bDepartment of Biology, Indiana University, Bloomington, IN 47401;
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Patrick S. G. Chain
cLos Alamos National Laboratory, Los Alamos, NM 87545;
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Stephanie Malfatti
dJoint Genome Institute, Walnut Creek, CA 94598;
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Lisa M. Vergez
eLawrence Livermore National Laboratory, Livermore, CA 94550; and
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Maria Shin
fEureka Genomics, Hercules, CA 94547
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Thomas G. Doak
bDepartment of Biology, Indiana University, Bloomington, IN 47401;
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Michael Lynch
bDepartment of Biology, Indiana University, Bloomington, IN 47401;
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Giulio Petroni
aDepartment of Biology, Pisa University, 56126 Pisa, Italy;
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  • For correspondence: gpetroni@biologia.unipi.it
  1. Edited by Nancy A. Moran, University of Texas at Austin, Austin, TX, and approved October 1, 2013 (received for review September 6, 2013)

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Significance

We have investigated multiple aspects of the Euplotes-Polynucleobacter system, which provides a unique opportunity for the study of an obligate symbiont with a closely related free-living organism that itself possesses a peculiarly reduced genome and metabolism. We confirmed the robustness and generality of patterns in the evolution of bacterial symbionts’ genome, adding at the same time new elements and hypotheses concerning genome reduction in both symbiotic and free-living bacteria. We argue that this system will provide an exceptionally useful model for investigations on symbiosis, because of its peculiarities and the commonness and ease of handling of the ciliate hosts. Genome sequences for independently derived Polynucleobacter symbionts will be particularly telling.

Abstract

We present the complete genomic sequence of the essential symbiont Polynucleobacter necessarius (Betaproteobacteria), which is a valuable case study for several reasons. First, it is hosted by a ciliated protist, Euplotes; bacterial symbionts of ciliates are still poorly known because of a lack of extensive molecular data. Second, the single species P. necessarius contains both symbiotic and free-living strains, allowing for a comparison between closely related organisms with different ecologies. Third, free-living P. necessarius strains are exceptional by themselves because of their small genome size, reduced metabolic flexibility, and high worldwide abundance in freshwater systems. We provide a comparative analysis of P. necessarius metabolism and explore the peculiar features of a genome reduction that occurred on an already streamlined genome. We compare this unusual system with current hypotheses for genome erosion in symbionts and free-living bacteria, propose modifications to the presently accepted model, and discuss the potential consequences of translesion DNA polymerase loss.

  • symbiosis
  • nonsynonymous mutation rates
  • Burkholderiales
  • protozoa
  • genome streamlining

Footnotes

  • ↵1V.B. and M.F. contributed equally to this work.

  • ↵2Present address: Department of Chemistry, University of Konstanz, 78457 Konstanz, Germany.

  • ↵3To whom correspondence should be addressed. E-mail: gpetroni{at}biologia.unipi.it.
  • Author contributions: C.V., M.L., and G.P. designed research; C.V., P.S.G.C., S.M., L.M.V., and M.S. performed research; V.B., M.F., M.S.A., P.S.G.C., S.M., L.M.V., M.S., and T.G.D. analyzed data; V.B. and M.F. wrote the paper; and G.P. coordinated research.

  • The authors declare no conflict of interest.

  • This article is a PNAS Direct Submission.

  • Data deposition: The sequence reported in this paper has been deposited in the GenBank database (accession no. NC_010531.1).

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1316687110/-/DCSupplemental.

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Polynucleobacter necessarius genome reduction
Vittorio Boscaro, Michele Felletti, Claudia Vannini, Matthew S. Ackerman, Patrick S. G. Chain, Stephanie Malfatti, Lisa M. Vergez, Maria Shin, Thomas G. Doak, Michael Lynch, Giulio Petroni
Proceedings of the National Academy of Sciences Oct 2013, 201316687; DOI: 10.1073/pnas.1316687110

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Polynucleobacter necessarius genome reduction
Vittorio Boscaro, Michele Felletti, Claudia Vannini, Matthew S. Ackerman, Patrick S. G. Chain, Stephanie Malfatti, Lisa M. Vergez, Maria Shin, Thomas G. Doak, Michael Lynch, Giulio Petroni
Proceedings of the National Academy of Sciences Oct 2013, 201316687; DOI: 10.1073/pnas.1316687110
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