Literature DB >> 30082394

Cargo transport shapes the spatial organization of a microbial community.

Abhishek Shrivastava1,2,3, Visha K Patel4, Yisha Tang4, Susan Connolly Yost2, Floyd E Dewhirst2, Howard C Berg1,3.   

Abstract

The human microbiome is an assemblage of diverse bacteria that interact with one another to form communities. Bacteria in a given community are arranged in a 3D matrix with many degrees of freedom. Snapshots of the community display well-defined structures, but the steps required for their assembly are not understood. Here, we show that this construction is carried out with the help of gliding bacteria. Gliding is defined as the motion of cells over a solid or semisolid surface without the necessity of growth or the aid of pili or flagella. Genomic analysis suggests that gliding bacteria are present in human microbial communities. We focus on Capnocytophaga gingivalis, which is present in abundance in the human oral microbiome. Tracking of fluorescently labeled single cells and of gas bubbles carried by fluid flow shows that swarms of C. gingivalis are layered, with cells in the upper layers moving more rapidly than those in the lower layers. Thus, cells also glide on top of one another. Cells of nonmotile bacterial species attach to the surface of C. gingivalis and are propelled as cargo. The cargo cell moves along the length of a C. gingivalis cell, looping from one pole to the other. Multicolor fluorescent spectral imaging of cells of different live but nonmotile bacterial species reveals their long-range transport in a polymicrobial community. A swarm of C. gingivalis transports some nonmotile bacterial species more efficiently than others and helps to shape the spatial organization of a polymicrobial community.

Entities:  

Keywords:  cargo transport; gliding; microbiome; polymicrobial biofilm; swarm

Mesh:

Year:  2018        PMID: 30082394      PMCID: PMC6112710          DOI: 10.1073/pnas.1808966115

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


  33 in total

1.  The human oral microbiome.

Authors:  Floyd E Dewhirst; Tuste Chen; Jacques Izard; Bruce J Paster; Anne C R Tanner; Wen-Han Yu; Abirami Lakshmanan; William G Wade
Journal:  J Bacteriol       Date:  2010-07-23       Impact factor: 3.490

2.  A rotary motor drives Flavobacterium gliding.

Authors:  Abhishek Shrivastava; Pushkar P Lele; Howard C Berg
Journal:  Curr Biol       Date:  2015-01-22       Impact factor: 10.834

3.  Swimming bacteria promote dispersal of non-motile staphylococcal species.

Authors:  Tahoura Samad; Nicole Billings; Alona Birjiniuk; Thomas Crouzier; Patrick S Doyle; Katharina Ribbeck
Journal:  ISME J       Date:  2017-04-11       Impact factor: 10.302

4.  Oligotyping analysis of the human oral microbiome.

Authors:  A Murat Eren; Gary G Borisy; Susan M Huse; Jessica L Mark Welch
Journal:  Proc Natl Acad Sci U S A       Date:  2014-06-25       Impact factor: 11.205

5.  Lautropia mirabilis gen. nov., sp. nov., a gram-negative motile coccus with unusual morphology isolated from the human mouth.

Authors:  P Gerner-Smidt; H Keiser-Nielsen; M Dorsch; E Stackebrandt; J Ursing; J Blom; A C Christensen; J J Christensen; W Frederiksen; S Hoffmann
Journal:  Microbiology       Date:  1994-07       Impact factor: 2.777

6.  Obesity alters gut microbial ecology.

Authors:  Ruth E Ley; Fredrik Bäckhed; Peter Turnbaugh; Catherine A Lozupone; Robin D Knight; Jeffrey I Gordon
Journal:  Proc Natl Acad Sci U S A       Date:  2005-07-20       Impact factor: 11.205

7.  Structure, function and diversity of the healthy human microbiome.

Authors: 
Journal:  Nature       Date:  2012-06-13       Impact factor: 49.962

8.  Bacterial swarms recruit cargo bacteria to pave the way in toxic environments.

Authors:  Alin Finkelshtein; Dalit Roth; Eshel Ben Jacob; Colin J Ingham
Journal:  MBio       Date:  2015-05-12       Impact factor: 7.867

9.  The mechanism of force transmission at bacterial focal adhesion complexes.

Authors:  Laura M Faure; Jean-Bernard Fiche; Leon Espinosa; Adrien Ducret; Vivek Anantharaman; Jennifer Luciano; Sébastien Lhospice; Salim T Islam; Julie Tréguier; Mélanie Sotes; Erkin Kuru; Michael S Van Nieuwenhze; Yves V Brun; Olivier Théodoly; L Aravind; Marcelo Nollmann; Tâm Mignot
Journal:  Nature       Date:  2016-10-05       Impact factor: 49.962

10.  The role of motility and chemotaxis in the bacterial colonization of protected surfaces.

Authors:  Einat Tamar; Moriah Koler; Ady Vaknin
Journal:  Sci Rep       Date:  2016-01-21       Impact factor: 4.379

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  18 in total

1.  Metabolic Signaling and Spatial Interactions in the Oral Polymicrobial Community.

Authors:  D P Miller; Z R Fitzsimonds; R J Lamont
Journal:  J Dent Res       Date:  2019-07-29       Impact factor: 6.116

Review 2.  The Structure of Dental Plaque Microbial Communities in the Transition from Health to Dental Caries and Periodontal Disease.

Authors:  Alex M Valm
Journal:  J Mol Biol       Date:  2019-05-17       Impact factor: 5.469

3.  Recent progress in analyzing the spatial structure of the human microbiome: distinguishing biogeography and architecture in the oral and gut communities.

Authors:  Emmanuel E Adade; Khalid Al Lakhen; Alex A Lemus; Alex M Valm
Journal:  Curr Opin Endocr Metab Res       Date:  2021-04-26

4.  Multispecies biofilm removal by a multisonic irrigation system in mandibular molars.

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Journal:  Int Endod J       Date:  2022-08-30       Impact factor: 5.165

5.  Large-Scale Vortices with Dynamic Rotation Emerged from Monolayer Collective Motion of Gliding Flavobacteria.

Authors:  Daisuke Nakane; Shoko Odaka; Kana Suzuki; Takayuki Nishizaka
Journal:  J Bacteriol       Date:  2021-06-22       Impact factor: 3.490

Review 6.  Spatial scale in analysis of the dental plaque microbiome.

Authors:  Gary G Borisy; Alex M Valm
Journal:  Periodontol 2000       Date:  2021-03-10       Impact factor: 7.589

Review 7.  Roadmap on emerging concepts in the physical biology of bacterial biofilms: from surface sensing to community formation.

Authors:  Gerard C L Wong; Jyot D Antani; Pushkar P Lele; Jing Chen; Beiyan Nan; Marco J Kühn; Alexandre Persat; Jean-Louis Bru; Nina Molin Høyland-Kroghsbo; Albert Siryaporn; Jacinta C Conrad; Francesco Carrara; Yutaka Yawata; Roman Stocker; Yves V Brun; Gregory B Whitfield; Calvin K Lee; Jaime de Anda; William C Schmidt; Ramin Golestanian; George A O'Toole; Kyle A Floyd; Fitnat H Yildiz; Shuai Yang; Fan Jin; Masanori Toyofuku; Leo Eberl; Nobuhiko Nomura; Lori A Zacharoff; Mohamed Y El-Naggar; Sibel Ebru Yalcin; Nikhil S Malvankar; Mauricio D Rojas-Andrade; Allon I Hochbaum; Jing Yan; Howard A Stone; Ned S Wingreen; Bonnie L Bassler; Yilin Wu; Haoran Xu; Knut Drescher; Jörn Dunkel
Journal:  Phys Biol       Date:  2021-06-23       Impact factor: 2.959

8.  Biofilm Spreading by the Adhesin-Dependent Gliding Motility of Flavobacterium johnsoniae: 2. Role of Filamentous Extracellular Network and Cell-to-Cell Connections at the Biofilm Surface.

Authors:  Keiko Sato; Masami Naya; Yuri Hatano; Naoki Kasahata; Yoshio Kondo; Mari Sato; Katsuki Takebe; Mariko Naito; Chikara Sato
Journal:  Int J Mol Sci       Date:  2021-06-27       Impact factor: 5.923

9.  A molecular rack and pinion actuates a cell-surface adhesin and enables bacterial gliding motility.

Authors:  Abhishek Shrivastava; Howard C Berg
Journal:  Sci Adv       Date:  2020-03-04       Impact factor: 14.136

Review 10.  The influence of spaceflight and simulated microgravity on bacterial motility and chemotaxis.

Authors:  Jacqueline M Acres; Myka Jaap Youngapelian; Jay Nadeau
Journal:  NPJ Microgravity       Date:  2021-02-22       Impact factor: 4.415

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