Literature DB >> 28039436

Cell morphology drives spatial patterning in microbial communities.

William P J Smith1, Yohan Davit2, James M Osborne3, Wook Kim4, Kevin R Foster5, Joe M Pitt-Francis6.   

Abstract

The clearest phenotypic characteristic of microbial cells is their shape, but we do not understand how cell shape affects the dense communities, known as biofilms, where many microbes live. Here, we use individual-based modeling to systematically vary cell shape and study its impact in simulated communities. We compete cells with different cell morphologies under a range of conditions and ask how shape affects the patterning and evolutionary fitness of cells within a community. Our models predict that cell shape will strongly influence the fate of a cell lineage: we describe a mechanism through which coccal (round) cells rise to the upper surface of a community, leading to a strong spatial structuring that can be critical for fitness. We test our predictions experimentally using strains of Escherichia coli that grow at a similar rate but differ in cell shape due to single amino acid changes in the actin homolog MreB. As predicted by our model, cell types strongly sort by shape, with round cells at the top of the colony and rod cells dominating the basal surface and edges. Our work suggests that cell morphology has a strong impact within microbial communities and may offer new ways to engineer the structure of synthetic communities.

Entities:  

Keywords:  biofilms; biophysics; cell morphology; self-organization; synthetic biology

Mesh:

Substances:

Year:  2016        PMID: 28039436      PMCID: PMC5255625          DOI: 10.1073/pnas.1613007114

Source DB:  PubMed          Journal:  Proc Natl Acad Sci U S A        ISSN: 0027-8424            Impact factor:   11.205


  52 in total

Review 1.  Bacterial cell shape.

Authors:  Matthew T Cabeen; Christine Jacobs-Wagner
Journal:  Nat Rev Microbiol       Date:  2005-08       Impact factor: 60.633

Review 2.  Morphological plasticity as a bacterial survival strategy.

Authors:  Sheryl S Justice; David A Hunstad; Lynette Cegelski; Scott J Hultgren
Journal:  Nat Rev Microbiol       Date:  2008-02       Impact factor: 60.633

3.  Mechanically-driven phase separation in a growing bacterial colony.

Authors:  Pushpita Ghosh; Jagannath Mondal; Eshel Ben-Jacob; Herbert Levine
Journal:  Proc Natl Acad Sci U S A       Date:  2015-04-13       Impact factor: 11.205

Review 4.  Cutting through the complexity of cell collectives.

Authors:  Carey D Nadell; Vanni Bucci; Knut Drescher; Simon A Levin; Bonnie L Bassler; João B Xavier
Journal:  Proc Biol Sci       Date:  2013-01-30       Impact factor: 5.349

Review 5.  Bacterial diversity: the natural history of selected morphologically unusual bacteria.

Authors:  M P Starr; V B Skerman
Journal:  Annu Rev Microbiol       Date:  1965       Impact factor: 15.500

6.  Spatial organization of intestinal microbiota in the mouse ascending colon.

Authors:  Gerardo M Nava; Hans J Friedrichsen; Thaddeus S Stappenbeck
Journal:  ISME J       Date:  2010-10-28       Impact factor: 10.302

7.  Difference of EGCg adhesion on cell surface between Staphylococcus aureus and Escherichia coli visualized by electron microscopy after novel indirect staining with cerium chloride.

Authors:  Motokazu Nakayama; Naofumi Shigemune; Takashi Tsugukuni; Hajime Tokuda; Takahisa Miyamoto
Journal:  J Microbiol Methods       Date:  2011-04-23       Impact factor: 2.363

Review 8.  Bacterial shape: two-dimensional questions and possibilities.

Authors:  Kevin D Young
Journal:  Annu Rev Microbiol       Date:  2010       Impact factor: 15.500

9.  Importance of positioning for microbial evolution.

Authors:  Wook Kim; Fernando Racimo; Jonas Schluter; Stuart B Levy; Kevin R Foster
Journal:  Proc Natl Acad Sci U S A       Date:  2014-04-08       Impact factor: 11.205

10.  Rapid radiation in bacteria leads to a division of labour.

Authors:  Wook Kim; Stuart B Levy; Kevin R Foster
Journal:  Nat Commun       Date:  2016-02-08       Impact factor: 14.919

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  40 in total

1.  A Dual-Species Biofilm with Emergent Mechanical and Protective Properties.

Authors:  Sarah M Yannarell; Gabrielle M Grandchamp; Shih-Yuan Chen; Karen E Daniels; Elizabeth A Shank
Journal:  J Bacteriol       Date:  2019-08-22       Impact factor: 3.490

2.  Straightening up for life in a biofilm.

Authors:  Heidi A Arjes; Kerwyn Casey Huang
Journal:  Proc Natl Acad Sci U S A       Date:  2020-11-17       Impact factor: 11.205

3.  Cooperation, competition and antibiotic resistance in bacterial colonies.

Authors:  Isabel Frost; William P J Smith; Sara Mitri; Alvaro San Millan; Yohan Davit; James M Osborne; Joe M Pitt-Francis; R Craig MacLean; Kevin R Foster
Journal:  ISME J       Date:  2018-03-21       Impact factor: 10.302

Review 4.  Emergence of evolutionary driving forces in pattern-forming microbial populations.

Authors:  Jona Kayser; Carl F Schreck; QinQin Yu; Matti Gralka; Oskar Hallatschek
Journal:  Philos Trans R Soc Lond B Biol Sci       Date:  2018-05-26       Impact factor: 6.237

5.  Cellular packing, mechanical stress and the evolution of multicellularity.

Authors:  Shane Jacobeen; Jennifer T Pentz; Elyes C Graba; Colin G Brandys; William C Ratcliff; Peter J Yunker
Journal:  Nat Phys       Date:  2018-03       Impact factor: 20.034

6.  Vibrio cholerae adapts to sessile and motile lifestyles by cyclic di-GMP regulation of cell shape.

Authors:  Nicolas L Fernandez; Brian Y Hsueh; Nguyen T Q Nhu; Joshua L Franklin; Yann S Dufour; Christopher M Waters
Journal:  Proc Natl Acad Sci U S A       Date:  2020-11-02       Impact factor: 11.205

7.  Modeling mechanical interactions in growing populations of rod-shaped bacteria.

Authors:  James J Winkle; Oleg A Igoshin; Matthew R Bennett; Krešimir Josić; William Ott
Journal:  Phys Biol       Date:  2017-07-28       Impact factor: 2.583

8.  Entropically driven aggregation of bacteria by host polymers promotes antibiotic tolerance in Pseudomonas aeruginosa.

Authors:  Patrick R Secor; Lia A Michaels; Anina Ratjen; Laura K Jennings; Pradeep K Singh
Journal:  Proc Natl Acad Sci U S A       Date:  2018-10-01       Impact factor: 11.205

Review 9.  The Molecular Basis of Noncanonical Bacterial Morphology.

Authors:  Paul D Caccamo; Yves V Brun
Journal:  Trends Microbiol       Date:  2017-10-19       Impact factor: 17.079

Review 10.  Type IV pili: dynamics, biophysics and functional consequences.

Authors:  Lisa Craig; Katrina T Forest; Berenike Maier
Journal:  Nat Rev Microbiol       Date:  2019-07       Impact factor: 60.633

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