Literature DB >> 33826904

Bacterial predation transforms the landscape and community assembly of biofilms.

Benjamin R Wucher1, Mennat Elsayed2, James S Adelman3, Daniel E Kadouri2, Carey D Nadell4.   

Abstract

The bacterium Bdellovibrio bacteriovorus attaches to the exterior of a Gram-negative prey cell, enters the periplasm, and harvests resources to replicate before lysing the host to find new prey.1-7 Predatory bacteria such as this are common in many natural environments,8-13 as are groups of matrix-bound prey cell clusters, termed biofilms.14-16 Despite the ubiquity of both predatory bacteria and biofilm-dwelling prey, the interaction between B. bacteriovorus and prey inside biofilms has received little attention and has not yet been studied at the micrometer scale. Filling this knowledge gap is critical to understanding bacterial predator-prey interaction in nature. Here we show that B. bacteriovorus is able to attack biofilms of the pathogen Vibrio cholerae, but only up until a critical maturation threshold past which the prey biofilms are protected from their predators. Using high-resolution microscopy and detailed spatial analysis, we determine the relative contributions of matrix secretion and cell-cell packing of the prey biofilm toward this protection mechanism. Our results demonstrate that B. bacteriovorus predation in the context of this protection threshold fundamentally transforms the sub-millimeter-scale landscape of biofilm growth, as well as the process of community assembly as new potential biofilm residents enter the system. We conclude that bacterial predation can be a key factor influencing the spatial community ecology of microbial biofilms.
Copyright © 2021 The Authors. Published by Elsevier Inc. All rights reserved.

Entities:  

Keywords:  Bdellovibrio bacteriovorus; Vibrio cholerae; architecture; biofilm; collective behavior; community assembly; competition; extracellular matrix; predation; spatial ecology

Mesh:

Year:  2021        PMID: 33826904      PMCID: PMC8588571          DOI: 10.1016/j.cub.2021.03.036

Source DB:  PubMed          Journal:  Curr Biol        ISSN: 0960-9822            Impact factor:   10.900


  82 in total

1.  Recovery of bdellovibrios from submerged surfaces and other aquatic habitats.

Authors:  H N Williams; A J Schoeffield; D Guether; J Kelley; D Shah; W A Falkler
Journal:  Microb Ecol       Date:  1995-01       Impact factor: 4.552

2.  Extracellular matrix structure governs invasion resistance in bacterial biofilms.

Authors:  Carey D Nadell; Knut Drescher; Ned S Wingreen; Bonnie L Bassler
Journal:  ISME J       Date:  2015-01-20       Impact factor: 10.302

Review 3.  Biofilms: an emergent form of bacterial life.

Authors:  Hans-Curt Flemming; Jost Wingender; Ulrich Szewzyk; Peter Steinberg; Scott A Rice; Staffan Kjelleberg
Journal:  Nat Rev Microbiol       Date:  2016-08-11       Impact factor: 60.633

Review 4.  The biogeography of polymicrobial infection.

Authors:  Apollo Stacy; Luke McNally; Sophie E Darch; Sam P Brown; Marvin Whiteley
Journal:  Nat Rev Microbiol       Date:  2015-12-30       Impact factor: 60.633

5.  Visualizing Bdellovibrio bacteriovorus by Using the tdTomato Fluorescent Protein.

Authors:  Somdatta Mukherjee; Kimberly M Brothers; Robert M Q Shanks; Daniel E Kadouri
Journal:  Appl Environ Microbiol       Date:  2015-12-28       Impact factor: 4.792

6.  Vibrio cholerae biofilm growth program and architecture revealed by single-cell live imaging.

Authors:  Jing Yan; Andrew G Sharo; Howard A Stone; Ned S Wingreen; Bonnie L Bassler
Journal:  Proc Natl Acad Sci U S A       Date:  2016-08-23       Impact factor: 11.205

7.  Biofilm formation and phenotypic variation enhance predation-driven persistence of Vibrio cholerae.

Authors:  Carsten Matz; Diane McDougald; Ana Maria Moreno; Pui Yi Yung; Fitnat H Yildiz; Staffan Kjelleberg
Journal:  Proc Natl Acad Sci U S A       Date:  2005-11-02       Impact factor: 11.205

8.  The extracellular matrix protects Pseudomonas aeruginosa biofilms by limiting the penetration of tobramycin.

Authors:  Boo Shan Tseng; Wei Zhang; Joe J Harrison; Tam P Quach; Jisun Lee Song; Jon Penterman; Pradeep K Singh; David L Chopp; Aaron I Packman; Matthew R Parsek
Journal:  Environ Microbiol       Date:  2013-06-10       Impact factor: 5.491

9.  Molecular insights into Vibrio cholerae's intra-amoebal host-pathogen interactions.

Authors:  Charles Van der Henst; Audrey Sophie Vanhove; Natália Carolina Drebes Dörr; Sandrine Stutzmann; Candice Stoudmann; Stéphanie Clerc; Tiziana Scrignari; Catherine Maclachlan; Graham Knott; Melanie Blokesch
Journal:  Nat Commun       Date:  2018-08-27       Impact factor: 14.919

10.  Breakdown of Vibrio cholerae biofilm architecture induced by antibiotics disrupts community barrier function.

Authors:  Francisco Díaz-Pascual; Raimo Hartmann; Martin Lempp; Lucia Vidakovic; Boya Song; Hannah Jeckel; Kai M Thormann; Fitnat H Yildiz; Jörn Dunkel; Hannes Link; Carey D Nadell; Knut Drescher
Journal:  Nat Microbiol       Date:  2019-10-28       Impact factor: 17.745

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  3 in total

1.  Differential Surface Competition and Biofilm Invasion Strategies of Pseudomonas aeruginosa PA14 and PAO1.

Authors:  Swetha Kasetty; Stefan Katharios-Lanwermeyer; George A O'Toole; Carey D Nadell
Journal:  J Bacteriol       Date:  2021-09-13       Impact factor: 3.490

2.  Social evolution of shared biofilm matrix components.

Authors:  Jung-Shen B Tai; Saikat Mukherjee; Thomas Nero; Rich Olson; Jeffrey Tithof; Carey D Nadell; Jing Yan
Journal:  Proc Natl Acad Sci U S A       Date:  2022-06-30       Impact factor: 12.779

3.  VxrB Influences Antagonism within Biofilms by Controlling Competition through Extracellular Matrix Production and Type 6 Secretion.

Authors:  Jennifer K Teschler; Eva Jiménez-Siebert; Hannah Jeckel; Praveen K Singh; Jin Hwan Park; Stefan Pukatzki; Carey D Nadell; Knut Drescher; Fitnat H Yildiz
Journal:  mBio       Date:  2022-07-26       Impact factor: 7.786

  3 in total

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