The evolution of ecological facilitation within mixed-species biofilms in the mouse gastrointestinal tract

Xiaoxi B. Lin, Tuo Wang, Paul Stothard, Jukka Corander, Jun Wang, John F. Baines, Sarah C.L. Knowles, Laima Baltrūnaitė, Guergana Tasseva, Robert Schmaltz, Stephanie Tollenaar, Liz A. Cody, Theodore Grenier, Wei Wu, Amanda E. Ramer-Tait, Jens Walter

Research output: Contribution to journalArticle

4 Citations (Scopus)

Abstract

The eco-evolutionary interactions among members of the vertebrate gut microbiota that ultimately result in host-specific communities are poorly understood. Here we show that Lactobacillus reuteri coexists with species that belong to the Lactobacillus johnsonii cluster (L. johnsonii, L. gasseri, and L taiwanensis) in a taxonomically wide range of rodents, suggesting cohabitation over evolutionary times. The two dominant Lactobacillus species found in wild mice establish a commensalistic relationship in gastric biofilms when introduced together into germ-free mice in which L. reuteri facilitates colonization of L. taiwanensis. Genomic analysis revealed allopatric diversification in strains of both species that originated from geographically separated locations (Scotland and France). Allopatry of the strains resulted in reduced formation of mixed biofilms in vitro, indicating that interspecies interactions in gastric Lactobacillus-biofilms are the result of an adaptive evolutionary process that occurred in a biogeographical context. In summary, these findings suggest that members within the vertebrate gut microbiota can evolve inter-dependencies through ecological facilitation, which could represent one mechanism by which host-specific bacterial communities assemble across vertebrate species and an explanation for their spatial and biogeographic patterns.

Original languageEnglish (US)
Pages (from-to)2770-2784
Number of pages15
JournalISME Journal
Volume12
Issue number11
DOIs
StatePublished - Nov 1 2018

Fingerprint

facilitation
Biofilms
Lactobacillus johnsonii
Lactobacillus reuteri
biofilm
gastrointestinal system
Vertebrates
Gastrointestinal Tract
vertebrate
vertebrates
Lactobacillus
intestinal microorganisms
Stomach
mice
stomach
Lactobacillus gasseri
allopatry
cohabitation
Scotland
bacterial communities

ASJC Scopus subject areas

  • Microbiology
  • Ecology, Evolution, Behavior and Systematics

Cite this

Lin, X. B., Wang, T., Stothard, P., Corander, J., Wang, J., Baines, J. F., ... Walter, J. (2018). The evolution of ecological facilitation within mixed-species biofilms in the mouse gastrointestinal tract. ISME Journal, 12(11), 2770-2784. https://doi.org/10.1038/s41396-018-0211-0

The evolution of ecological facilitation within mixed-species biofilms in the mouse gastrointestinal tract. / Lin, Xiaoxi B.; Wang, Tuo; Stothard, Paul; Corander, Jukka; Wang, Jun; Baines, John F.; Knowles, Sarah C.L.; Baltrūnaitė, Laima; Tasseva, Guergana; Schmaltz, Robert; Tollenaar, Stephanie; Cody, Liz A.; Grenier, Theodore; Wu, Wei; Ramer-Tait, Amanda E.; Walter, Jens.

In: ISME Journal, Vol. 12, No. 11, 01.11.2018, p. 2770-2784.

Research output: Contribution to journalArticle

Lin, XB, Wang, T, Stothard, P, Corander, J, Wang, J, Baines, JF, Knowles, SCL, Baltrūnaitė, L, Tasseva, G, Schmaltz, R, Tollenaar, S, Cody, LA, Grenier, T, Wu, W, Ramer-Tait, AE & Walter, J 2018, 'The evolution of ecological facilitation within mixed-species biofilms in the mouse gastrointestinal tract', ISME Journal, vol. 12, no. 11, pp. 2770-2784. https://doi.org/10.1038/s41396-018-0211-0
Lin, Xiaoxi B. ; Wang, Tuo ; Stothard, Paul ; Corander, Jukka ; Wang, Jun ; Baines, John F. ; Knowles, Sarah C.L. ; Baltrūnaitė, Laima ; Tasseva, Guergana ; Schmaltz, Robert ; Tollenaar, Stephanie ; Cody, Liz A. ; Grenier, Theodore ; Wu, Wei ; Ramer-Tait, Amanda E. ; Walter, Jens. / The evolution of ecological facilitation within mixed-species biofilms in the mouse gastrointestinal tract. In: ISME Journal. 2018 ; Vol. 12, No. 11. pp. 2770-2784.
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