Literature DB >> 28007984

Microbial competition in porous environments can select against rapid biofilm growth.

Katharine Z Coyte1,2,3,4, Hervé Tabuteau5, Eamonn A Gaffney2, Kevin R Foster6,3, William M Durham6,7.   

Abstract

Microbes often live in dense communities called biofilms, where competition between strains and species is fundamental to both evolution and community function. Although biofilms are commonly found in soil-like porous environments, the study of microbial interactions has largely focused on biofilms growing on flat, planar surfaces. Here, we use microfluidic experiments, mechanistic models, and game theory to study how porous media hydrodynamics can mediate competition between bacterial genotypes. Our experiments reveal a fundamental challenge faced by microbial strains that live in porous environments: cells that rapidly form biofilms tend to block their access to fluid flow and redirect resources to competitors. To understand how these dynamics influence the evolution of bacterial growth rates, we couple a model of flow-biofilm interaction with a game theory analysis. This investigation revealed that hydrodynamic interactions between competing genotypes give rise to an evolutionarily stable growth rate that stands in stark contrast with that observed in typical laboratory experiments: cells within a biofilm can outcompete other genotypes by growing more slowly. Our work reveals that hydrodynamics can profoundly affect how bacteria compete and evolve in porous environments, the habitat where most bacteria live.

Entities:  

Keywords:  adaptive dynamics; bacterial evolution; clogging; game theory; porous media flow

Mesh:

Year:  2016        PMID: 28007984      PMCID: PMC5240682          DOI: 10.1073/pnas.1525228113

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


  73 in total

Review 1.  Community genomics in microbial ecology and evolution.

Authors:  Eric E Allen; Jillian F Banfield
Journal:  Nat Rev Microbiol       Date:  2005-06       Impact factor: 60.633

2.  Physical model for the decay and preservation of marine organic carbon.

Authors:  Daniel H Rothman; David C Forney
Journal:  Science       Date:  2007-06-01       Impact factor: 47.728

3.  Shear stress increases the residence time of adhesion of Pseudomonas aeruginosa.

Authors:  Sigolene Lecuyer; Roberto Rusconi; Yi Shen; Alison Forsyth; Hera Vlamakis; Roberto Kolter; Howard A Stone
Journal:  Biophys J       Date:  2011-01-19       Impact factor: 4.033

Review 4.  Modeling of biofilm systems: a review.

Authors:  Harald Horn; Susanne Lackner
Journal:  Adv Biochem Eng Biotechnol       Date:  2014       Impact factor: 2.635

Review 5.  Spatial structure, cooperation and competition in biofilms.

Authors:  Carey D Nadell; Knut Drescher; Kevin R Foster
Journal:  Nat Rev Microbiol       Date:  2016-07-25       Impact factor: 60.633

6.  Effects of fluid flow conditions on interactions between species in biofilms.

Authors:  Wei Zhang; Tadas Sileika; Aaron I Packman
Journal:  FEMS Microbiol Ecol       Date:  2013-01-24       Impact factor: 4.194

7.  Exopolysaccharide production is required for development of Escherichia coli K-12 biofilm architecture.

Authors:  P N Danese; L A Pratt; R Kolter
Journal:  J Bacteriol       Date:  2000-06       Impact factor: 3.490

Review 8.  Microfluidics expanding the frontiers of microbial ecology.

Authors:  Roberto Rusconi; Melissa Garren; Roman Stocker
Journal:  Annu Rev Biophys       Date:  2014       Impact factor: 12.981

Review 9.  Bacterial competition: surviving and thriving in the microbial jungle.

Authors:  Michael E Hibbing; Clay Fuqua; Matthew R Parsek; S Brook Peterson
Journal:  Nat Rev Microbiol       Date:  2010-01       Impact factor: 60.633

10.  Psl trails guide exploration and microcolony formation in Pseudomonas aeruginosa biofilms.

Authors:  Kun Zhao; Boo Shan Tseng; Bernard Beckerman; Fan Jin; Maxsim L Gibiansky; Joe J Harrison; Erik Luijten; Matthew R Parsek; Gerard C L Wong
Journal:  Nature       Date:  2013-05-08       Impact factor: 49.962

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  26 in total

1.  Challenges of biofilm control and utilization: lessons from mathematical modelling.

Authors:  Paulina A Dzianach; Gary A Dykes; Norval J C Strachan; Ken J Forbes; Francisco J Pérez-Reche
Journal:  J R Soc Interface       Date:  2019-06-12       Impact factor: 4.118

Review 2.  Soil Aggregate Microbial Communities: Towards Understanding Microbiome Interactions at Biologically Relevant Scales.

Authors:  Regina L Wilpiszeski; Jayde A Aufrecht; Scott T Retterer; Matthew B Sullivan; David E Graham; Eric M Pierce; Olivier D Zablocki; Anthony V Palumbo; Dwayne A Elias
Journal:  Appl Environ Microbiol       Date:  2019-07-01       Impact factor: 4.792

3.  Reply to Baveye and Darnault: Useful models are simple and extendable.

Authors:  Katharine Z Coyte; Hervé Tabuteau; Eamonn A Gaffney; Kevin R Foster; William M Durham
Journal:  Proc Natl Acad Sci U S A       Date:  2017-03-24       Impact factor: 11.205

4.  Microbial competition and evolution in natural porous environments: Not that simple.

Authors:  Philippe C Baveye; Christophe Darnault
Journal:  Proc Natl Acad Sci U S A       Date:  2017-03-24       Impact factor: 11.205

Review 5.  Emergent Properties of Microbial Activity in Heterogeneous Soil Microenvironments: Different Research Approaches Are Slowly Converging, Yet Major Challenges Remain.

Authors:  Philippe C Baveye; Wilfred Otten; Alexandra Kravchenko; María Balseiro-Romero; Éléonore Beckers; Maha Chalhoub; Christophe Darnault; Thilo Eickhorst; Patricia Garnier; Simona Hapca; Serkan Kiranyaz; Olivier Monga; Carsten W Mueller; Naoise Nunan; Valérie Pot; Steffen Schlüter; Hannes Schmidt; Hans-Jörg Vogel
Journal:  Front Microbiol       Date:  2018-08-27       Impact factor: 5.640

6.  Optically Accessible Microfluidic Flow Channels for Noninvasive High-Resolution Biofilm Imaging Using Lattice Light Sheet Microscopy.

Authors:  Ji Zhang; Mingxing Zhang; Yibo Wang; Eric Donarski; Andreas Gahlmann
Journal:  J Phys Chem B       Date:  2021-10-29       Impact factor: 2.991

7.  Competition between growth and shear stress drives intermittency in preferential flow paths in porous medium biofilms.

Authors:  Dorothee L Kurz; Eleonora Secchi; Francisco J Carrillo; Ian C Bourg; Roman Stocker; Joaquin Jimenez-Martinez
Journal:  Proc Natl Acad Sci U S A       Date:  2022-07-18       Impact factor: 12.779

8.  Sharp turns and gyrotaxis modulate surface accumulation of microorganisms.

Authors:  Li Zeng; Weiquan Jiang; Timothy J Pedley
Journal:  Proc Natl Acad Sci U S A       Date:  2022-10-11       Impact factor: 12.779

9.  Bacterial predation transforms the landscape and community assembly of biofilms.

Authors:  Benjamin R Wucher; Mennat Elsayed; James S Adelman; Daniel E Kadouri; Carey D Nadell
Journal:  Curr Biol       Date:  2021-04-06       Impact factor: 10.900

10.  Flow environment and matrix structure interact to determine spatial competition in Pseudomonas aeruginosa biofilms.

Authors:  Carey D Nadell; Deirdre Ricaurte; Jing Yan; Knut Drescher; Bonnie L Bassler
Journal:  Elife       Date:  2017-01-13       Impact factor: 8.140

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