Molecular Characterization of Host-Specific Biofilm Formation in a Vertebrate Gut Symbiont

Steven A. Frese, Donald A. MacKenzie, Daniel A. Peterson, Robert Schmaltz, Teresa Fangman, You Zhou, Chaomei Zhang, Andrew K. Benson, Liz A. Cody, Francis Mulholland, Nathalie Juge, Jens Walter

Research output: Contribution to journalArticle

57 Citations (Scopus)

Abstract

Although vertebrates harbor bacterial communities in their gastrointestinal tract whose composition is host-specific, little is known about the mechanisms by which bacterial lineages become selected. The goal of this study was to characterize the ecological processes that mediate host-specificity of the vertebrate gut symbiont Lactobacillus reuteri, and to systematically identify the bacterial factors that are involved. Experiments with monoassociated mice revealed that the ability of L. reuteri to form epithelial biofilms in the mouse forestomach is strictly dependent on the strain's host origin. To unravel the molecular basis for this host-specific biofilm formation, we applied a combination of transcriptome analysis and comparative genomics and identified eleven genes of L. reuteri 100-23 that were predicted to play a role. We then determined expression and importance of these genes during in vivo biofilm formation in monoassociated mice. This analysis revealed that six of the genes were upregulated in vivo, and that genes encoding for proteins involved in epithelial adherence, specialized protein transport, cell aggregation, environmental sensing, and cell lysis contributed to biofilm formation. Inactivation of a serine-rich surface adhesin with a devoted transport system (the SecA2-SecY2 pathway) completely abrogated biofilm formation, indicating that initial adhesion represented the most significant step in biofilm formation, likely conferring host specificity. In summary, this study established that the epithelial selection of bacterial symbionts in the vertebrate gut can be both specific and highly efficient, resulting in biofilms that are exclusively formed by the coevolved strains, and it allowed insight into the bacterial effectors of this process.

Original languageEnglish (US)
Article numbere1004057
JournalPLoS genetics
Volume9
Issue number12
DOIs
StatePublished - Dec 1 2013

Fingerprint

Biofilms
symbiont
symbionts
biofilm
Vertebrates
vertebrate
digestive system
vertebrates
Lactobacillus reuteri
host specificity
gene
Host Specificity
mice
Bacterial Physiological Phenomena
genes
forestomach
Cell Aggregation
adhesins
protein
protein transport

ASJC Scopus subject areas

  • Ecology, Evolution, Behavior and Systematics
  • Molecular Biology
  • Genetics
  • Genetics(clinical)
  • Cancer Research

Cite this

Frese, S. A., MacKenzie, D. A., Peterson, D. A., Schmaltz, R., Fangman, T., Zhou, Y., ... Walter, J. (2013). Molecular Characterization of Host-Specific Biofilm Formation in a Vertebrate Gut Symbiont. PLoS genetics, 9(12), [e1004057]. https://doi.org/10.1371/journal.pgen.1004057

Molecular Characterization of Host-Specific Biofilm Formation in a Vertebrate Gut Symbiont. / Frese, Steven A.; MacKenzie, Donald A.; Peterson, Daniel A.; Schmaltz, Robert; Fangman, Teresa; Zhou, You; Zhang, Chaomei; Benson, Andrew K.; Cody, Liz A.; Mulholland, Francis; Juge, Nathalie; Walter, Jens.

In: PLoS genetics, Vol. 9, No. 12, e1004057, 01.12.2013.

Research output: Contribution to journalArticle

Frese, SA, MacKenzie, DA, Peterson, DA, Schmaltz, R, Fangman, T, Zhou, Y, Zhang, C, Benson, AK, Cody, LA, Mulholland, F, Juge, N & Walter, J 2013, 'Molecular Characterization of Host-Specific Biofilm Formation in a Vertebrate Gut Symbiont', PLoS genetics, vol. 9, no. 12, e1004057. https://doi.org/10.1371/journal.pgen.1004057
Frese, Steven A. ; MacKenzie, Donald A. ; Peterson, Daniel A. ; Schmaltz, Robert ; Fangman, Teresa ; Zhou, You ; Zhang, Chaomei ; Benson, Andrew K. ; Cody, Liz A. ; Mulholland, Francis ; Juge, Nathalie ; Walter, Jens. / Molecular Characterization of Host-Specific Biofilm Formation in a Vertebrate Gut Symbiont. In: PLoS genetics. 2013 ; Vol. 9, No. 12.
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