Literature DB >> 30136358

The model squid-vibrio symbiosis provides a window into the impact of strain- and species-level differences during the initial stages of symbiont engagement.

Sabrina Koehler1, Roxane Gaedeke1, Cecilia Thompson2, Clotilde Bongrand1, Karen L Visick2, Edward Ruby1, Margaret McFall-Ngai1.   

Abstract

Among horizontally acquired symbioses, the mechanisms underlying microbial strain- and species-level specificity remain poorly understood. Here, confocal-microscopy analyses and genetic manipulation of the squid-vibrio association revealed quantitative differences in a symbiont's capacity to interact with the host during initial engagement. Specifically, dominant strains of Vibrio fischeri, 'D-type', previously named for their dominant, single-strain colonization of the squid's bioluminescent organ, were compared with 'S-type', or 'sharing', strains, which can co-colonize the organ. These D-type strains typically: (i) formed aggregations of 100s-1000s of cells on the light-organ surface, up to 3 orders of magnitude larger than those of S-type strains; (ii) showed dominance in co-aggregation experiments, independent of inoculum size or strain proportion; (iii) perturbed larger areas of the organ's ciliated surface; and, (iv) appeared at the pore of the organ approximately 4×s more quickly than S-type strains. At least in part, genes responsible for biofilm synthesis control the hyperaggregation phenotype of a D-type strain. Other marine vibrios produced relatively small aggregations, while an array of marine Gram-positive and -negative species outside of the Vibrionaceae did not attach to the organ's surface. These studies provide insight into the impact of strain variation on early events leading to establishment of an environmentally acquired symbiosis.
© 2018 Society for Applied Microbiology and John Wiley & Sons Ltd.

Entities:  

Year:  2018        PMID: 30136358      PMCID: PMC6386636          DOI: 10.1111/1462-2920.14392

Source DB:  PubMed          Journal:  Environ Microbiol        ISSN: 1462-2912            Impact factor:   5.491


  74 in total

1.  New rfp- and pES213-derived tools for analyzing symbiotic Vibrio fischeri reveal patterns of infection and lux expression in situ.

Authors:  Anne K Dunn; Deborah S Millikan; Dawn M Adin; Jeffrey L Bose; Eric V Stabb
Journal:  Appl Environ Microbiol       Date:  2006-01       Impact factor: 4.792

Review 2.  Leeches and their microbiota: naturally simple symbiosis models.

Authors:  Joerg Graf; Yoshitomo Kikuchi; Rita V M Rio
Journal:  Trends Microbiol       Date:  2006-07-14       Impact factor: 17.079

3.  Marine tubeworm metamorphosis induced by arrays of bacterial phage tail-like structures.

Authors:  Nicholas J Shikuma; Martin Pilhofer; Gregor L Weiss; Michael G Hadfield; Grant J Jensen; Dianne K Newman
Journal:  Science       Date:  2014-01-09       Impact factor: 47.728

4.  Construction of a Vibrio splendidus mutant lacking the metalloprotease gene vsm by use of a novel counterselectable suicide vector.

Authors:  Frédérique Le Roux; Johan Binesse; Denis Saulnier; Didier Mazel
Journal:  Appl Environ Microbiol       Date:  2006-11-22       Impact factor: 4.792

Review 5.  Gut microbial communities of social bees.

Authors:  Waldan K Kwong; Nancy A Moran
Journal:  Nat Rev Microbiol       Date:  2016-05-03       Impact factor: 60.633

6.  The first engagement of partners in the Euprymna scolopes-Vibrio fischeri symbiosis is a two-step process initiated by a few environmental symbiont cells.

Authors:  Melissa A Altura; Elizabeth A C Heath-Heckman; Amani Gillette; Natacha Kremer; Anne-Marie Krachler; Caitlin Brennan; Edward G Ruby; Kim Orth; Margaret J McFall-Ngai
Journal:  Environ Microbiol       Date:  2013-07-03       Impact factor: 5.491

Review 7.  High-resolution characterization of the human microbiome.

Authors:  Cecilia Noecker; Colin P McNally; Alexander Eng; Elhanan Borenstein
Journal:  Transl Res       Date:  2016-07-25       Impact factor: 7.012

Review 8.  Beyond 16S rRNA Community Profiling: Intra-Species Diversity in the Gut Microbiota.

Authors:  Kirsten M Ellegaard; Philipp Engel
Journal:  Front Microbiol       Date:  2016-09-21       Impact factor: 5.640

9.  Impact of Salt and Nutrient Content on Biofilm Formation by Vibrio fischeri.

Authors:  Anne E Marsden; Kevin Grudzinski; Jakob M Ondrey; Cindy R DeLoney-Marino; Karen L Visick
Journal:  PLoS One       Date:  2017-01-25       Impact factor: 3.240

10.  A single regulatory gene is sufficient to alter bacterial host range.

Authors:  Mark J Mandel; Michael S Wollenberg; Eric V Stabb; Karen L Visick; Edward G Ruby
Journal:  Nature       Date:  2009-02-01       Impact factor: 49.962

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  18 in total

1.  Squid genomes in a bacterial world.

Authors:  Thomas C G Bosch
Journal:  Proc Natl Acad Sci U S A       Date:  2019-01-23       Impact factor: 11.205

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

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

Review 3.  Compartmentalization drives the evolution of symbiotic cooperation.

Authors:  Guillaume Chomicki; Gijsbert D A Werner; Stuart A West; E Toby Kiers
Journal:  Philos Trans R Soc Lond B Biol Sci       Date:  2020-08-10       Impact factor: 6.237

Review 4.  The impact of Vibrio fischeri strain variation on host colonization.

Authors:  Clotilde Bongrand; Edward G Ruby
Journal:  Curr Opin Microbiol       Date:  2019-10-06       Impact factor: 7.934

Review 5.  Evolutionary "Experiments" in Symbiosis: The Study of Model Animals Provides Insights into the Mechanisms Underlying the Diversity of Host-Microbe Interactions.

Authors:  Thomas C G Bosch; Karen Guillemin; Margaret McFall-Ngai
Journal:  Bioessays       Date:  2019-05-17       Impact factor: 4.345

6.  Tracking the cargo of extracellular symbionts into host tissues with correlated electron microscopy and nanoscale secondary ion mass spectrometry imaging.

Authors:  Stephanie K Cohen; Marie-Stéphanie Aschtgen; Jonathan B Lynch; Sabrina Koehler; Fangmin Chen; Stéphane Escrig; Jean Daraspe; Edward G Ruby; Anders Meibom; Margaret McFall-Ngai
Journal:  Cell Microbiol       Date:  2020-04       Impact factor: 3.715

7.  Genetic Manipulation of Vibrio fischeri.

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

8.  LapG mediates biofilm dispersal in Vibrio fischeri by controlling maintenance of the VCBS-containing adhesin LapV.

Authors:  David G Christensen; Anne E Marsden; Kelsey Hodge-Hanson; Tara Essock-Burns; Karen L Visick
Journal:  Mol Microbiol       Date:  2020-08-03       Impact factor: 3.501

Review 9.  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

10.  MicroRNA-Mediated Regulation of Initial Host Responses in a Symbiotic Organ.

Authors:  Silvia Moriano-Gutierrez; Edward G Ruby; Margaret J McFall-Ngai
Journal:  mSystems       Date:  2021-05-11       Impact factor: 6.496

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