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A centimeter-long bacterium with DNA compartmentalized in membrane-bound organelles

View ORCID ProfileJean-Marie Volland, Silvina Gonzalez-Rizzo, Olivier Gros, Tomáš Tyml, Natalia Ivanova, Frederik Schulz, Danielle Goudeau, Nathalie H Elisabeth, Nandita Nath, Daniel Udwary, Rex R Malmstrom, Chantal Guidi-Rontani, Susanne Bolte-Kluge, Karen M Davies, Maïtena R Jean, Jean-Louis Mansot, Nigel J Mouncey, Esther Angert, Tanja Woyke, Shailesh V Date
doi: https://doi.org/10.1101/2022.02.16.480423
Jean-Marie Volland
1Department of Energy Joint Genome Institute, Lawrence Berkeley National Laboratory, Berkeley, CA, USA
2Laboratory for Research in Complex Systems, Menlo Park, CA, USA
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  • ORCID record for Jean-Marie Volland
  • For correspondence: jvolland@lbl.gov twoyke@lbl.gov shailesh.date@lrc.systems
Silvina Gonzalez-Rizzo
3Institut de Systématique, Evolution, Biodiversité, Muséum National d’Histoire Naturelle, CNRS, Sorbonne Université, EPHE, Université des Antilles. Campus de Fouillole, Pointe-à-Pitre, France
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Olivier Gros
3Institut de Systématique, Evolution, Biodiversité, Muséum National d’Histoire Naturelle, CNRS, Sorbonne Université, EPHE, Université des Antilles. Campus de Fouillole, Pointe-à-Pitre, France
4Centre 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
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Tomáš Tyml
1Department of Energy Joint Genome Institute, Lawrence Berkeley National Laboratory, Berkeley, CA, USA
2Laboratory for Research in Complex Systems, Menlo Park, CA, USA
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Natalia Ivanova
1Department of Energy Joint Genome Institute, Lawrence Berkeley National Laboratory, Berkeley, CA, USA
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Frederik Schulz
1Department of Energy Joint Genome Institute, Lawrence Berkeley National Laboratory, Berkeley, CA, USA
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Danielle Goudeau
1Department of Energy Joint Genome Institute, Lawrence Berkeley National Laboratory, Berkeley, CA, USA
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Nathalie H Elisabeth
5Department of Energy Molecular Biophysics and Integrated Bioimaging, Lawrence Berkeley National Laboratory. Berkeley, CA, USA
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Nandita Nath
1Department of Energy Joint Genome Institute, Lawrence Berkeley National Laboratory, Berkeley, CA, USA
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Daniel Udwary
1Department of Energy Joint Genome Institute, Lawrence Berkeley National Laboratory, Berkeley, CA, USA
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Rex R Malmstrom
1Department of Energy Joint Genome Institute, Lawrence Berkeley National Laboratory, Berkeley, CA, USA
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Chantal Guidi-Rontani
6Institut de Systématique, Evolution, Biodiversité CNRS UMR 7205, Museum National d’Histoire Naturelle, Paris, France
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Susanne Bolte-Kluge
7Sorbonne Universités, UPMC Univ. Paris 06, CNRS FRE3631, Institut de Biologie Paris Seine, Paris France
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Karen M Davies
5Department of Energy Molecular Biophysics and Integrated Bioimaging, Lawrence Berkeley National Laboratory. Berkeley, CA, USA
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Maïtena R Jean
3Institut de Systématique, Evolution, Biodiversité, Muséum National d’Histoire Naturelle, CNRS, Sorbonne Université, EPHE, Université des Antilles. Campus de Fouillole, Pointe-à-Pitre, France
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Jean-Louis Mansot
4Centre 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
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Nigel J Mouncey
1Department of Energy Joint Genome Institute, Lawrence Berkeley National Laboratory, Berkeley, CA, USA
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Esther Angert
8Cornell University, College of Agriculture and Life Sciences, Department of Microbiology, Ithaca, NY, USA
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Tanja Woyke
1Department of Energy Joint Genome Institute, Lawrence Berkeley National Laboratory, Berkeley, CA, USA
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  • For correspondence: jvolland@lbl.gov twoyke@lbl.gov shailesh.date@lrc.systems
Shailesh V Date
2Laboratory for Research in Complex Systems, Menlo Park, CA, USA
9University of California San Francisco, San Francisco, CA, USA
10San Francisco State University, San Francisco, CA, USA
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  • For correspondence: jvolland@lbl.gov twoyke@lbl.gov shailesh.date@lrc.systems
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Abstract

Cells of most bacterial species are around 2 µm in length, with some of the largest specimens reaching 750 µm. Using fluorescence, x-ray, and electron microscopy in conjunction with genome sequencing, we characterized Ca. Thiomargarita magnifica, a bacterium with an average cell length greater than 9,000 µm that is visible to the naked eye. We found that these cells grow orders of magnitude over theoretical limits for bacterial cell size through unique biology, 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 in daughter cells. These features, along with compartmentalization of genomic material and protein synthesis in membrane-bound organelles, indicate gain of complexity in the Thiomargarita lineage, and challenge traditional concepts of bacterial cells.

One Sentence Summary Ca. T. magnifica are compartmentalized centimeter-long bacteria

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Posted February 18, 2022.
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A centimeter-long bacterium with DNA compartmentalized in membrane-bound organelles
Jean-Marie Volland, Silvina Gonzalez-Rizzo, Olivier Gros, Tomáš Tyml, Natalia Ivanova, Frederik Schulz, Danielle Goudeau, Nathalie H Elisabeth, Nandita Nath, Daniel Udwary, Rex R Malmstrom, Chantal Guidi-Rontani, Susanne Bolte-Kluge, Karen M Davies, Maïtena R Jean, Jean-Louis Mansot, Nigel J Mouncey, Esther Angert, Tanja Woyke, Shailesh V Date
bioRxiv 2022.02.16.480423; doi: https://doi.org/10.1101/2022.02.16.480423
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A centimeter-long bacterium with DNA compartmentalized in membrane-bound organelles
Jean-Marie Volland, Silvina Gonzalez-Rizzo, Olivier Gros, Tomáš Tyml, Natalia Ivanova, Frederik Schulz, Danielle Goudeau, Nathalie H Elisabeth, Nandita Nath, Daniel Udwary, Rex R Malmstrom, Chantal Guidi-Rontani, Susanne Bolte-Kluge, Karen M Davies, Maïtena R Jean, Jean-Louis Mansot, Nigel J Mouncey, Esther Angert, Tanja Woyke, Shailesh V Date
bioRxiv 2022.02.16.480423; doi: https://doi.org/10.1101/2022.02.16.480423

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