Literature DB >> 27016564

Intraspecific Competition Impacts Vibrio fischeri Strain Diversity during Initial Colonization of the Squid Light Organ.

Yan Sun1, Elijah D LaSota1, Andrew G Cecere1, Kyle B LaPenna1, Jessie Larios-Valencia1, Michael S Wollenberg2, Tim Miyashiro3.   

Abstract

UNLABELLED: Animal development and physiology depend on beneficial interactions with microbial symbionts. In many cases, the microbial symbionts are horizontally transmitted among hosts, thereby making the acquisition of these microbes from the environment an important event within the life history of each host. The light organ symbiosis established between the Hawaiian squid Euprymna scolopes and the bioluminescent bacterium Vibrio fischeri is a model system for examining how hosts acquire horizontally transmitted microbial symbionts. Recent studies have revealed that the light organ of wild-caught E. scolopes squid contains polyclonal populations of V. fischeri bacteria; however, the function and development of such strain diversity in the symbiosis are unknown. Here, we report our phenotypic and phylogenetic characterizations of FQ-A001, which is a V. fischeri strain isolated directly from the light organ of an E. scolopes individual. Relative to the type strain ES114, FQ-A001 exhibits similar growth in rich medium but displays increased bioluminescence and decreased motility in soft agar. FQ-A001 outcompetes ES114 in colonizing the crypt spaces of the light organs. Remarkably, we find that animals cocolonized with FQ-A001 and ES114 harbor singly colonized crypts, in contrast to the cocolonized crypts observed from competition experiments involving single genotypes. The results with our two-strain system suggest that strain diversity within the squid light organ is a consequence of diversity in the single-strain colonization of individual crypt spaces. IMPORTANCE: The developmental programs and overall physiologies of most animals depend on diverse microbial symbionts that are acquired from the environment. However, the basic principles underlying how microbes colonize their hosts remain poorly understood. Here, we report our findings of bacterial strain competition within the coevolved animal-microbe symbiosis composed of the Hawaiian squid and bioluminescent bacterium Vibrio fischeri Using fluorescent proteins to differentially label two distinct V. fischeri strains, we find that the strains are unable to coexist in the same niche within the host. Our results suggest that strain competition for distinct colonization sites dictates the strain diversity associated with the host. Our study provides a platform for studying how strain diversity develops within a host.
Copyright © 2016, American Society for Microbiology. All Rights Reserved.

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Year:  2016        PMID: 27016564      PMCID: PMC4959073          DOI: 10.1128/AEM.04143-15

Source DB:  PubMed          Journal:  Appl Environ Microbiol        ISSN: 0099-2240            Impact factor:   4.792


  43 in total

1.  Shedding light on bioluminescence regulation in Vibrio fischeri.

Authors:  Tim Miyashiro; Edward G Ruby
Journal:  Mol Microbiol       Date:  2012-05-02       Impact factor: 3.501

Review 2.  Models and approaches to dissect host-symbiont specificity.

Authors:  Mark J Mandel
Journal:  Trends Microbiol       Date:  2010-08-21       Impact factor: 17.079

3.  Effect of the Squid Host on the Abundance and Distribution of Symbiotic Vibrio fischeri in Nature.

Authors:  K H Lee; E G Ruby
Journal:  Appl Environ Microbiol       Date:  1994-05       Impact factor: 4.792

Review 4.  Eco-Evo-Devo: developmental symbiosis and developmental plasticity as evolutionary agents.

Authors:  Scott F Gilbert; Thomas C G Bosch; Cristina Ledón-Rettig
Journal:  Nat Rev Genet       Date:  2015-09-15       Impact factor: 53.242

5.  Squid-derived chitin oligosaccharides are a chemotactic signal during colonization by Vibrio fischeri.

Authors:  Mark J Mandel; Amy L Schaefer; Caitlin A Brennan; Elizabeth A C Heath-Heckman; Cindy R Deloney-Marino; Margaret J McFall-Ngai; Edward G Ruby
Journal:  Appl Environ Microbiol       Date:  2012-04-20       Impact factor: 4.792

6.  Complete genome sequence of Vibrio fischeri: a symbiotic bacterium with pathogenic congeners.

Authors:  E G Ruby; M Urbanowski; J Campbell; A Dunn; M Faini; R Gunsalus; P Lostroh; C Lupp; J McCann; D Millikan; A Schaefer; E Stabb; A Stevens; K Visick; C Whistler; E P Greenberg
Journal:  Proc Natl Acad Sci U S A       Date:  2005-02-09       Impact factor: 11.205

7.  Population structure of Vibrio fischeri within the light organs of Euprymna scolopes squid from Two Oahu (Hawaii) populations.

Authors:  M S Wollenberg; E G Ruby
Journal:  Appl Environ Microbiol       Date:  2008-11-07       Impact factor: 4.792

Review 8.  An intricate network of regulators controls biofilm formation and colonization by Vibrio fischeri.

Authors:  Karen L Visick
Journal:  Mol Microbiol       Date:  2009-10-08       Impact factor: 3.501

9.  Design, construction and characterization of a set of insulated bacterial promoters.

Authors:  Joseph H Davis; Adam J Rubin; Robert T Sauer
Journal:  Nucleic Acids Res       Date:  2010-09-15       Impact factor: 16.971

10.  Bacterial colonization factors control specificity and stability of the gut microbiota.

Authors:  S Melanie Lee; Gregory P Donaldson; Zbigniew Mikulski; Silva Boyajian; Klaus Ley; Sarkis K Mazmanian
Journal:  Nature       Date:  2013-08-18       Impact factor: 49.962

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  18 in total

1.  Sulfur availability for Vibrio fischeri growth during symbiosis establishment depends on biogeography within the squid light organ.

Authors:  Nathan P Wasilko; Jessie Larios-Valencia; Caroline H Steingard; Briana M Nunez; Subhash C Verma; Tim Miyashiro
Journal:  Mol Microbiol       Date:  2019-01-02       Impact factor: 3.501

2.  Bacterial type VI secretion system facilitates niche domination.

Authors:  Natália C Drebes Dörr; Melanie Blokesch
Journal:  Proc Natl Acad Sci U S A       Date:  2018-08-24       Impact factor: 11.205

3.  Vibrio fischeri: Laboratory Cultivation, Storage, and Common Phenotypic Assays.

Authors:  David G Christensen; Karen L Visick
Journal:  Curr Protoc Microbiol       Date:  2020-06

4.  Niche-Specific Impact of a Symbiotic Function on the Persistence of Microbial Symbionts within a Natural Host.

Authors:  Subhash C Verma; Tim Miyashiro
Journal:  Appl Environ Microbiol       Date:  2016-09-16       Impact factor: 4.792

5.  Detecting Symbioses in Complex Communities: the Fungal Symbionts of Bark and Ambrosia Beetles Within Asian Pines.

Authors:  James Skelton; Michelle A Jusino; You Li; Craig Bateman; Pham Hong Thai; Chengxu Wu; Daniel L Lindner; Jiri Hulcr
Journal:  Microb Ecol       Date:  2018-02-24       Impact factor: 4.552

Review 6.  The State of the Union Is Strong: a Review of ASM's 6th Conference on Cell-Cell Communication in Bacteria.

Authors:  Sam P Brown; Helen E Blackwell; Brian K Hammer
Journal:  J Bacteriol       Date:  2018-06-25       Impact factor: 3.490

7.  Incompatibility of Vibrio fischeri Strains during Symbiosis Establishment Depends on Two Functionally Redundant hcp Genes.

Authors:  Kirsten R Guckes; Andrew G Cecere; Nathan P Wasilko; Amanda L Williams; Katherine M Bultman; Mark J Mandel; Tim Miyashiro
Journal:  J Bacteriol       Date:  2019-09-06       Impact factor: 3.490

8.  Genetic Manipulation of Vibrio fischeri.

Authors:  David G Christensen; Jovanka Tepavčević; Karen L Visick
Journal:  Curr Protoc Microbiol       Date:  2020-12

9.  The Bacterial Enhancer Binding Protein VasH Promotes Expression of a Type VI Secretion System in Vibrio fischeri during Symbiosis.

Authors:  Kirsten R Guckes; Andrew G Cecere; Amanda L Williams; Anjali E McNeil; Tim Miyashiro
Journal:  J Bacteriol       Date:  2020-03-11       Impact factor: 3.490

Review 10.  A lasting symbiosis: how Vibrio fischeri finds a squid partner and persists within its natural host.

Authors:  Karen L Visick; Eric V Stabb; Edward G Ruby
Journal:  Nat Rev Microbiol       Date:  2021-06-04       Impact factor: 60.633

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