A centimeter-long bacterium with DNA contained in metabolically active, membrane-bound organelles

Author:

Volland Jean-Marie12ORCID,Gonzalez-Rizzo Silvina3ORCID,Gros Olivier34ORCID,Tyml Tomáš12ORCID,Ivanova Natalia1ORCID,Schulz Frederik1ORCID,Goudeau Danielle1ORCID,Elisabeth Nathalie H.5ORCID,Nath Nandita1,Udwary Daniel1ORCID,Malmstrom Rex R.1ORCID,Guidi-Rontani Chantal6,Bolte-Kluge Susanne7ORCID,Davies Karen M.58,Jean Maïtena R.3,Mansot Jean-Louis4,Mouncey Nigel J.1ORCID,Angert Esther R.9ORCID,Woyke Tanja1210ORCID,Date Shailesh V.21112ORCID

Affiliation:

1. Department of Energy Joint Genome Institute, Lawrence Berkeley National Laboratory, Berkeley, CA, USA.

2. Laboratory for Research in Complex Systems, Menlo Park, CA, USA.

3. Institut de Systématique, Evolution, Biodiversité, Université des Antilles, Muséum National d’Histoire Naturelle, CNRS, Sorbonne Université, EPHE, Campus de Fouillole, Pointe-à-Pitre, France.

4. Centre Commun de Caractérisation des Matériaux des Antilles et de la Guyane, Université des Antilles, UFR des Sciences Exactes et Naturelles, Pointe-à-Pitre, Guadeloupe, France.

5. Department of Energy Molecular Biophysics and Integrated Bioimaging, Lawrence Berkeley National Laboratory, Berkeley, CA, USA.

6. Institut de Systématique, Evolution, Biodiversité CNRS UMR 7205, Museum National d’Histoire Naturelle, Paris, France.

7. Sorbonne Universités, UPMC Univ. Paris 06, CNRS FRE3631, Institut de Biologie Paris Seine, Paris, France.

8. Department of Molecular and Cell Biology, University of California, Berkeley, USA.

9. Cornell University, College of Agriculture and Life Sciences, Department of Microbiology, Ithaca, NY, USA.

10. University of California Merced, School of Natural Sciences, Merced, CA, USA.

11. University of California San Francisco, San Francisco, CA, USA.

12. San Francisco State University, San Francisco, CA, USA.

Abstract

Cells of most bacterial species are around 2 micrometers in length, with some of the largest specimens reaching 750 micrometers. Using fluorescence, x-ray, and electron microscopy in conjunction with genome sequencing, we characterized Candidatus ( Ca. ) Thiomargarita magnifica, a bacterium that has an average cell length greater than 9000 micrometers and is visible to the naked eye. These cells grow orders of magnitude over theoretical limits for bacterial cell size, display unprecedented polyploidy of more than half a million copies of a very large genome, and undergo a dimorphic life cycle with asymmetric segregation of chromosomes into daughter cells. These features, along with compartmentalization of genomic material and ribosomes in translationally active organelles bound by bioenergetic membranes, indicate gain of complexity in the Thiomargarita lineage and challenge traditional concepts of bacterial cells.

Publisher

American Association for the Advancement of Science (AAAS)

Subject

Multidisciplinary

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