Generation of Bacterial Diversity by Segregation of DNA Strands

Overview

Journal Front Microbiol

Specialty Microbiology

Date 2021 Apr 8

PMID 33828535

Citations 4

Authors

Vic Norris

Camille Ripoll

Affiliations

Soon will be listed here.

Abstract

The generation in a bacterial population of a diversity that is coherent with present and future environments is a fundamental problem. Here, we use modeling to investigate growth rate diversity. We show that the combination of (1) association of extended assemblies of macromolecules with the DNA strands and (2) the segregation of DNA strands during cell division allows cells to generate different patterns of growth rate diversity with little effect on the overall growth rate of the population and thereby constitutes an example of "order for free" on which evolution can act.

Citing Articles

Hypothesis: bacteria live on the edge of phase transitions with a cell cycle regulated by a water-clock.

Norris V Theory Biosci. 2024; 143(4):253-277.

PMID: 39505803 DOI: 10.1007/s12064-024-00427-2.

Hunting the Cell Cycle .

Norris V Life (Basel). 2024; 14(10).

PMID: 39459514 PMC: 11509034. DOI: 10.3390/life14101213.

Open Questions about the Roles of DnaA, Related Proteins, and Hyperstructure Dynamics in the Cell Cycle.

Kohiyama M, Herrick J, Norris V Life (Basel). 2023; 13(9).

PMID: 37763294 PMC: 10532879. DOI: 10.3390/life13091890.

The Ring World: Eversion of Small Double-Stranded Polynucleotide Circlets at the Origin of DNA Double Helix, RNA Polymerization, Triplet Code, Twenty Amino Acids, and Strand Asymmetry.

Norris V, Demongeot J Int J Mol Sci. 2022; 23(21).

PMID: 36361702 PMC: 9657125. DOI: 10.3390/ijms232112915.

References

Montero Llopis P, Jackson A, Sliusarenko O, Surovtsev I, Heinritz J, Emonet T . Spatial organization of the flow of genetic information in bacteria. Nature. 2010; 466(7302):77-81. PMC: 2896451. DOI: 10.1038/nature09152. View

Weng X, Bohrer C, Bettridge K, Lagda A, Cagliero C, Jin D . Spatial organization of RNA polymerase and its relationship with transcription in . Proc Natl Acad Sci U S A. 2019; 116(40):20115-20123. PMC: 6778201. DOI: 10.1073/pnas.1903968116. View

Calabrese F, Voloshynovska I, Musat F, Thullner M, Schlomann M, Richnow H . Quantitation and Comparison of Phenotypic Heterogeneity Among Single Cells of Monoclonal Microbial Populations. Front Microbiol. 2020; 10:2814. PMC: 6933826. DOI: 10.3389/fmicb.2019.02814. View

Chen B, You C, Shu C . The common misuse of noise decomposition as applied to genetic systems. Biosystems. 2020; 198:104269. DOI: 10.1016/j.biosystems.2020.104269. View

Binenbaum Z, Parola A, Zaritsky A, Fishov I . Transcription- and translation-dependent changes in membrane dynamics in bacteria: testing the transertion model for domain formation. Mol Microbiol. 1999; 32(6):1173-82. DOI: 10.1046/j.1365-2958.1999.01426.x. View

Boeneman K, Fossum S, Yang Y, Fingland N, Skarstad K, Crooke E . Escherichia coli DnaA forms helical structures along the longitudinal cell axis distinct from MreB filaments. Mol Microbiol. 2009; 72(3):645-57. PMC: 2888790. DOI: 10.1111/j.1365-2958.2009.06674.x. View

Konto-Ghiorghi Y, Norris V . Hypothesis: nucleoid-associated proteins segregate with a parental DNA strand to generate coherent phenotypic diversity. Theory Biosci. 2020; 140(1):17-25. DOI: 10.1007/s12064-020-00323-5. View

Slodzian G, Daigne B, Girard F, Boust F, Hillion F . Scanning secondary ion analytical microscopy with parallel detection. Biol Cell. 1992; 74(1):43-50. DOI: 10.1016/0248-4900(92)90007-n. View

Norris V, den Blaauwen T, Doi R, Harshey R, Janniere L, Jimenez-Sanchez A . Toward a hyperstructure taxonomy. Annu Rev Microbiol. 2007; 61:309-29. DOI: 10.1146/annurev.micro.61.081606.103348. View

10.

Sunako Y, Onogi T, Hiraga S . Sister chromosome cohesion of Escherichia coli. Mol Microbiol. 2002; 42(5):1233-41. DOI: 10.1046/j.1365-2958.2001.02680.x. View

11.

Mayer F . Cytoskeletal elements in bacteria Mycoplasma pneumoniae, Thermoanaerobacterium sp., and Escherichia coli as revealed by electron microscopy. J Mol Microbiol Biotechnol. 2006; 11(3-5):228-43. DOI: 10.1159/000094057. View

12.

Qian Z, Zhurkin V, Adhya S . DNA-RNA interactions are critical for chromosome condensation in . Proc Natl Acad Sci U S A. 2017; 114(46):12225-12230. PMC: 5699063. DOI: 10.1073/pnas.1711285114. View

13.

Gaal T, Bratton B, Sanchez-Vazquez P, Sliwicki A, Sliwicki K, Vegel A . Colocalization of distant chromosomal loci in space in E. coli: a bacterial nucleolus. Genes Dev. 2016; 30(20):2272-2285. PMC: 5110994. DOI: 10.1101/gad.290312.116. View

14.

Li S, Li Z, Park J, King C, Rabinowitz J, Wingreen N . Escherichia coli translation strategies differ across carbon, nitrogen and phosphorus limitation conditions. Nat Microbiol. 2018; 3(8):939-947. PMC: 6278830. DOI: 10.1038/s41564-018-0199-2. View

15.

Ladouceur A, Parmar B, Biedzinski S, Wall J, Tope S, Cohn D . Clusters of bacterial RNA polymerase are biomolecular condensates that assemble through liquid-liquid phase separation. Proc Natl Acad Sci U S A. 2020; 117(31):18540-18549. PMC: 7414142. DOI: 10.1073/pnas.2005019117. View

16.

Duderstadt K, Mott M, Crisona N, Chuang K, Yang H, Berger J . Origin remodeling and opening in bacteria rely on distinct assembly states of the DnaA initiator. J Biol Chem. 2010; 285(36):28229-39. PMC: 2934688. DOI: 10.1074/jbc.M110.147975. View

17.

Wang W, Li G, Chen C, Xie X, Zhuang X . Chromosome organization by a nucleoid-associated protein in live bacteria. Science. 2011; 333(6048):1445-9. PMC: 3329943. DOI: 10.1126/science.1204697. View

18.

Kuwada N, Traxler B, Wiggins P . Genome-scale quantitative characterization of bacterial protein localization dynamics throughout the cell cycle. Mol Microbiol. 2014; 95(1):64-79. PMC: 4309519. DOI: 10.1111/mmi.12841. View

19.

Taghbalout A, Rothfield L . RNaseE and the other constituents of the RNA degradosome are components of the bacterial cytoskeleton. Proc Natl Acad Sci U S A. 2007; 104(5):1667-72. PMC: 1785250. DOI: 10.1073/pnas.0610491104. View

20.

Vohradsky J, Ramsden J . Genome resource utilization during prokaryotic development. FASEB J. 2001; 15(11):2054-6. DOI: 10.1096/fj.00-0889fje. View