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Lactobacillus bile salt hydrolase substrate specificity governs bacterial fitness and host colonization.

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Title: Lactobacillus bile salt hydrolase substrate specificity governs bacterial fitness and host colonization.
Authors: Foley, Matthew H.1, O'Flaherty, Sarah2, Allen, Garrison1, Rivera, Alissa J.1, Stewart, Allison K.3, Barrangou, Rodolphe2 rbarran@ncsu.edu, Theriot, Casey M.1 cmtherio@ncsu.edu
Source: Proceedings of the National Academy of Sciences of the United States of America. 2/9/2021, Vol. 118 Issue 6, p1-10. 10p.
Subjects: Bile salts, Lactobacillus, Lactobacillus acidophilus, Colonization, Bile acids
Abstract: Primary bile acids (BAs) are a collection of host-synthesized metabolites that shape physiology and metabolism. BAs transit the gastrointestinal tract and are subjected to a variety of chemical transformations encoded by indigenous bacteria. The resulting microbiota-derived BA pool is a mediator of host-microbiota interactions. Bacterial bile salt hydrolases (BSHs) cleave the conjugated glycine or taurine from BAs, an essential upstream step for the production of deconjugated and secondary BAs. Probiotic lactobacilli harbor a considerable number and diversity of BSHs; however, their contribution to Lactobacillus fitness and colonization remains poorly understood. Here, we define and compare the functions of multiple BSHs encoded by Lactobacillus acidophilus and Lactobacillus gasseri. Our genetic and biochemical characterization of lactobacilli BSHs lend to a model of Lactobacillus adaptation to the gut. These findings deviate from previous notions that BSHs generally promote colonization and detoxify bile. Rather, we show that BSH enzymatic preferences and the intrinsic chemical features of various BAs determine the toxicity of these molecules during Lactobacillus growth. BSHs were able to alter the Lactobacillus transcriptome in a BA-dependent manner. Finally, BSHs were able to dictate differences in bacterial competition in vitro and in vivo, defining their impact on BSH-encoding bacteria within the greater gastrointestinal tract ecosystem. This work emphasizes the importance of considering the enzymatic preferences of BSHs alongside the conjugated/deconjugated BA-bacterial interaction. These results deepen our understanding of the BA-microbiome axis and provide a framework to engineer lactobacilli with improved bile resistance and use probiotics as BA-altering therapeutics. [ABSTRACT FROM AUTHOR]
Copyright of Proceedings of the National Academy of Sciences of the United States of America is the property of National Academy of Sciences and its content may not be copied or emailed to multiple sites without the copyright holder's express written permission. Additionally, content may not be used with any artificial intelligence tools or machine learning technologies. However, users may print, download, or email articles for individual use. This abstract may be abridged. No warranty is given about the accuracy of the copy. Users should refer to the original published version of the material for the full abstract. (Copyright applies to all Abstracts.)
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DbLabel: Engineering Source
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  Data: Lactobacillus bile salt hydrolase substrate specificity governs bacterial fitness and host colonization.
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  Data: <searchLink fieldCode="AR" term="%22Foley%2C+Matthew+H%2E%22">Foley, Matthew H.</searchLink><relatesTo>1</relatesTo><br /><searchLink fieldCode="AR" term="%22O'Flaherty%2C+Sarah%22">O'Flaherty, Sarah</searchLink><relatesTo>2</relatesTo><br /><searchLink fieldCode="AR" term="%22Allen%2C+Garrison%22">Allen, Garrison</searchLink><relatesTo>1</relatesTo><br /><searchLink fieldCode="AR" term="%22Rivera%2C+Alissa+J%2E%22">Rivera, Alissa J.</searchLink><relatesTo>1</relatesTo><br /><searchLink fieldCode="AR" term="%22Stewart%2C+Allison+K%2E%22">Stewart, Allison K.</searchLink><relatesTo>3</relatesTo><br /><searchLink fieldCode="AR" term="%22Barrangou%2C+Rodolphe%22">Barrangou, Rodolphe</searchLink><relatesTo>2</relatesTo><i> rbarran@ncsu.edu</i><br /><searchLink fieldCode="AR" term="%22Theriot%2C+Casey+M%2E%22">Theriot, Casey M.</searchLink><relatesTo>1</relatesTo><i> cmtherio@ncsu.edu</i>
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  Data: <searchLink fieldCode="DE" term="%22Bile+salts%22">Bile salts</searchLink><br /><searchLink fieldCode="DE" term="%22Lactobacillus%22">Lactobacillus</searchLink><br /><searchLink fieldCode="DE" term="%22Lactobacillus+acidophilus%22">Lactobacillus acidophilus</searchLink><br /><searchLink fieldCode="DE" term="%22Colonization%22">Colonization</searchLink><br /><searchLink fieldCode="DE" term="%22Bile+acids%22">Bile acids</searchLink>
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  Data: Primary bile acids (BAs) are a collection of host-synthesized metabolites that shape physiology and metabolism. BAs transit the gastrointestinal tract and are subjected to a variety of chemical transformations encoded by indigenous bacteria. The resulting microbiota-derived BA pool is a mediator of host-microbiota interactions. Bacterial bile salt hydrolases (BSHs) cleave the conjugated glycine or taurine from BAs, an essential upstream step for the production of deconjugated and secondary BAs. Probiotic lactobacilli harbor a considerable number and diversity of BSHs; however, their contribution to Lactobacillus fitness and colonization remains poorly understood. Here, we define and compare the functions of multiple BSHs encoded by Lactobacillus acidophilus and Lactobacillus gasseri. Our genetic and biochemical characterization of lactobacilli BSHs lend to a model of Lactobacillus adaptation to the gut. These findings deviate from previous notions that BSHs generally promote colonization and detoxify bile. Rather, we show that BSH enzymatic preferences and the intrinsic chemical features of various BAs determine the toxicity of these molecules during Lactobacillus growth. BSHs were able to alter the Lactobacillus transcriptome in a BA-dependent manner. Finally, BSHs were able to dictate differences in bacterial competition in vitro and in vivo, defining their impact on BSH-encoding bacteria within the greater gastrointestinal tract ecosystem. This work emphasizes the importance of considering the enzymatic preferences of BSHs alongside the conjugated/deconjugated BA-bacterial interaction. These results deepen our understanding of the BA-microbiome axis and provide a framework to engineer lactobacilli with improved bile resistance and use probiotics as BA-altering therapeutics. [ABSTRACT FROM AUTHOR]
– Name: AbstractSuppliedCopyright
  Label:
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  Data: <i>Copyright of Proceedings of the National Academy of Sciences of the United States of America is the property of National Academy of Sciences and its content may not be copied or emailed to multiple sites without the copyright holder's express written permission. Additionally, content may not be used with any artificial intelligence tools or machine learning technologies. However, users may print, download, or email articles for individual use. This abstract may be abridged. No warranty is given about the accuracy of the copy. Users should refer to the original published version of the material for the full abstract.</i> (Copyright applies to all Abstracts.)
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        Value: 10.1073/pnas.2017709118
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        Text: English
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      – SubjectFull: Bile salts
        Type: general
      – SubjectFull: Lactobacillus
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      – SubjectFull: Lactobacillus acidophilus
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      – SubjectFull: Colonization
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      – SubjectFull: Bile acids
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      – TitleFull: Lactobacillus bile salt hydrolase substrate specificity governs bacterial fitness and host colonization.
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            NameFull: Stewart, Allison K.
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              Text: 2/9/2021
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              Y: 2021
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