Literature DB >> 26957597

Human symbionts inject and neutralize antibacterial toxins to persist in the gut.

Aaron G Wexler1, Yiqiao Bao1, John C Whitney2, Louis-Marie Bobay3, Joao B Xavier4, Whitman B Schofield1, Natasha A Barry1, Alistair B Russell2, Bao Q Tran5, Young Ah Goo5, David R Goodlett5, Howard Ochman3, Joseph D Mougous6, Andrew L Goodman7.   

Abstract

The human gut microbiome is a dynamic and densely populated microbial community that can provide important benefits to its host. Cooperation and competition for nutrients among its constituents only partially explain community composition and interpersonal variation. Notably, certain human-associated Bacteroidetes--one of two major phyla in the gut--also encode machinery for contact-dependent interbacterial antagonism, but its impact within gut microbial communities remains unknown. Here we report that prominent human gut symbionts persist in the gut through continuous attack on their immediate neighbors. Our analysis of just one of the hundreds of species in these communities reveals 12 candidate antibacterial effector loci that can exist in 32 combinations. Through the use of secretome studies, in vitro bacterial interaction assays and multiple mouse models, we uncover strain-specific effector/immunity repertoires that can predict interbacterial interactions in vitro and in vivo, and find that some of these strains avoid contact-dependent killing by accumulating immunity genes to effectors that they do not encode. Effector transmission rates in live animals can exceed 1 billion events per minute per gram of colonic contents, and multiphylum communities of human gut commensals can partially protect sensitive strains from these attacks. Together, these results suggest that gut microbes can determine their interactions through direct contact. An understanding of the strategies human gut symbionts have evolved to target other members of this community may provide new approaches for microbiome manipulation.

Entities:  

Keywords:  gut microbiome; microbial ecology; symbiosis; type VI secretion

Mesh:

Substances:

Year:  2016        PMID: 26957597      PMCID: PMC4822603          DOI: 10.1073/pnas.1525637113

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


  39 in total

1.  SignalP 4.0: discriminating signal peptides from transmembrane regions.

Authors:  Thomas Nordahl Petersen; Søren Brunak; Gunnar von Heijne; Henrik Nielsen
Journal:  Nat Methods       Date:  2011-09-29       Impact factor: 28.547

2.  Quantitative single-cell characterization of bacterial interactions reveals type VI secretion is a double-edged sword.

Authors:  Michele LeRoux; Justin A De Leon; Nathan J Kuwada; Alistair B Russell; Delia Pinto-Santini; Rachel D Hood; Danielle M Agnello; Stephen M Robertson; Paul A Wiggins; Joseph D Mougous
Journal:  Proc Natl Acad Sci U S A       Date:  2012-11-12       Impact factor: 11.205

3.  Tit-for-tat: type VI secretion system counterattack during bacterial cell-cell interactions.

Authors:  Marek Basler; Brian T Ho; John J Mekalanos
Journal:  Cell       Date:  2013-02-14       Impact factor: 41.582

4.  The long-term stability of the human gut microbiota.

Authors:  Jeremiah J Faith; Janaki L Guruge; Mark Charbonneau; Sathish Subramanian; Henning Seedorf; Andrew L Goodman; Jose C Clemente; Rob Knight; Andrew C Heath; Rudolph L Leibel; Michael Rosenbaum; Jeffrey I Gordon
Journal:  Science       Date:  2013-07-05       Impact factor: 47.728

5.  MAFFT multiple sequence alignment software version 7: improvements in performance and usability.

Authors:  Kazutaka Katoh; Daron M Standley
Journal:  Mol Biol Evol       Date:  2013-01-16       Impact factor: 16.240

6.  Intestinal inflammation targets cancer-inducing activity of the microbiota.

Authors:  Janelle C Arthur; Ernesto Perez-Chanona; Marcus Mühlbauer; Sarah Tomkovich; Joshua M Uronis; Ting-Jia Fan; Barry J Campbell; Turki Abujamel; Belgin Dogan; Arlin B Rogers; Jonathan M Rhodes; Alain Stintzi; Kenneth W Simpson; Jonathan J Hansen; Temitope O Keku; Anthony A Fodor; Christian Jobin
Journal:  Science       Date:  2012-08-16       Impact factor: 47.728

Review 7.  Structure and regulation of the type VI secretion system.

Authors:  Julie M Silverman; Yannick R Brunet; Eric Cascales; Joseph D Mougous
Journal:  Annu Rev Microbiol       Date:  2012-06-28       Impact factor: 15.500

8.  Predicting and manipulating cardiac drug inactivation by the human gut bacterium Eggerthella lenta.

Authors:  Henry J Haiser; David B Gootenberg; Kelly Chatman; Gopal Sirasani; Emily P Balskus; Peter J Turnbaugh
Journal:  Science       Date:  2013-07-19       Impact factor: 47.728

9.  Identifying genetic determinants needed to establish a human gut symbiont in its habitat.

Authors:  Andrew L Goodman; Nathan P McNulty; Yue Zhao; Douglas Leip; Robi D Mitra; Catherine A Lozupone; Rob Knight; Jeffrey I Gordon
Journal:  Cell Host Microbe       Date:  2009-09-17       Impact factor: 21.023

10.  Pfam: the protein families database.

Authors:  Robert D Finn; Alex Bateman; Jody Clements; Penelope Coggill; Ruth Y Eberhardt; Sean R Eddy; Andreas Heger; Kirstie Hetherington; Liisa Holm; Jaina Mistry; Erik L L Sonnhammer; John Tate; Marco Punta
Journal:  Nucleic Acids Res       Date:  2013-11-27       Impact factor: 16.971

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  84 in total

1.  Strain competition restricts colonization of an enteric pathogen and prevents colitis.

Authors:  Aaron L Hecht; Benjamin W Casterline; Zachary M Earley; Young Ah Goo; David R Goodlett; Juliane Bubeck Wardenburg
Journal:  EMBO Rep       Date:  2016-07-18       Impact factor: 8.807

2.  Microbial herd protection mediated by antagonistic interaction in polymicrobial communities.

Authors:  Megan Wong; Xiaoye Liang; Matt Smart; Le Tang; Richard Moore; Brian Ingalls; Tao G Dong
Journal:  Appl Environ Microbiol       Date:  2016-09-16       Impact factor: 4.792

Review 3.  Pathogen Colonization Resistance in the Gut and Its Manipulation for Improved Health.

Authors:  Joseph M Pickard; Gabriel Núñez
Journal:  Am J Pathol       Date:  2019-05-14       Impact factor: 4.307

4.  Type VI secretion TssK baseplate protein exhibits structural similarity with phage receptor-binding proteins and evolved to bind the membrane complex.

Authors:  Van Son Nguyen; Laureen Logger; Silvia Spinelli; Pierre Legrand; Thi Thanh Huyen Pham; Thi Trang Nhung Trinh; Yassine Cherrak; Abdelrahim Zoued; Aline Desmyter; Eric Durand; Alain Roussel; Christine Kellenberger; Eric Cascales; Christian Cambillau
Journal:  Nat Microbiol       Date:  2017-06-26       Impact factor: 17.745

Review 5.  An insider's perspective: Bacteroides as a window into the microbiome.

Authors:  Aaron G Wexler; Andrew L Goodman
Journal:  Nat Microbiol       Date:  2017-04-25       Impact factor: 17.745

6.  Evolutionary and ecological consequences of gut microbial communities.

Authors:  Nancy A Moran; Howard Ochman; Tobin J Hammer
Journal:  Annu Rev Ecol Evol Syst       Date:  2019-08-29       Impact factor: 13.915

7.  Mechanism of Kin-Discriminatory Demarcation Line Formation between Colonies of Swarming Bacteria.

Authors:  Pintu Patra; Christopher N Vassallo; Daniel Wall; Oleg A Igoshin
Journal:  Biophys J       Date:  2017-12-05       Impact factor: 4.033

8.  Engineered Regulatory Systems Modulate Gene Expression of Human Commensals in the Gut.

Authors:  Bentley Lim; Michael Zimmermann; Natasha A Barry; Andrew L Goodman
Journal:  Cell       Date:  2017-04-20       Impact factor: 41.582

9.  Nanaerobic growth enables direct visualization of dynamic cellular processes in human gut symbionts.

Authors:  Leonor García-Bayona; Michael J Coyne; Noam Hantman; Paula Montero-Llopis; Salena S Von; Takeshi Ito; Michael H Malamy; Marek Basler; Blanca Barquera; Laurie E Comstock
Journal:  Proc Natl Acad Sci U S A       Date:  2020-09-16       Impact factor: 11.205

10.  The Pseudomonas aeruginosa T6SS-VgrG1b spike is topped by a PAAR protein eliciting DNA damage to bacterial competitors.

Authors:  Panayiota Pissaridou; Luke P Allsopp; Sarah Wettstadt; Sophie A Howard; Despoina A I Mavridou; Alain Filloux
Journal:  Proc Natl Acad Sci U S A       Date:  2018-11-19       Impact factor: 11.205

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