Commensal Enterobacteriaceae Protect against Salmonella Colonization through Oxygen Competition

Yael Litvak; Khin K.Z. Mon; Henry Nguyen; Ganrea Chanthavixay; Megan Liou; Eric M. Velazquez; Laura Kutter; Monique A. Alcantara; Mariana X. Byndloss; Connor R. Tiffany; Gregory T. Walker; Franziska Faber; Yuhua Zhu; Denise N. Bronner; Austin J. Byndloss; Renée M. Tsolis; Huaijun Zhou; Andreas J. Bäumler

doi:10.1016/j.chom.2018.12.003

Commensal Enterobacteriaceae Protect against Salmonella Colonization through Oxygen Competition

Yael Litvak, Khin K.Z. Mon, Henry Nguyen, Ganrea Chanthavixay, Megan Liou, Eric M. Velazquez, Laura Kutter, Monique A. Alcantara, Mariana X. Byndloss, Connor R. Tiffany, Gregory T. Walker, Franziska Faber, Yuhua Zhu, Denise N. Bronner, Austin J. Byndloss, Renée M. Tsolis, Huaijun Zhou, Andreas J. Bäumler^*

^*Corresponding author for this work

Research output: Contribution to journal › Article › peer-review

113 Scopus citations

Abstract

Neonates are highly susceptible to infection with enteric pathogens, but the underlying mechanisms are not resolved. We show that neonatal chick colonization with Salmonella enterica serovar Enteritidis requires a virulence-factor-dependent increase in epithelial oxygenation, which drives pathogen expansion by aerobic respiration. Co-infection experiments with an Escherichia coli strain carrying an oxygen-sensitive reporter suggest that S. Enteritidis competes with commensal Enterobacteriaceae for oxygen. A combination of Enterobacteriaceae and spore-forming bacteria, but not colonization with either community alone, confers colonization resistance against S. Enteritidis in neonatal chicks, phenocopying germ-free mice associated with adult chicken microbiota. Combining spore-forming bacteria with a probiotic E. coli isolate protects germ-free mice from pathogen colonization, but the protection is lost when the ability to respire oxygen under micro-aerophilic conditions is genetically ablated in E. coli. These results suggest that commensal Enterobacteriaceae contribute to colonization resistance by competing with S. Enteritidis for oxygen, a resource critical for pathogen expansion.

Original language	American English
Pages (from-to)	128-139.e5
Journal	Cell Host and Microbe
Volume	25
Issue number	1
DOIs	https://doi.org/10.1016/j.chom.2018.12.003
State	Published - 9 Jan 2019
Externally published	Yes

Bibliographical note

Funding Information:
Y.L. was supported by Vaadia-BARD Postdoctoral Fellowship FI-505-2014. Work in H.Z.'s laboratory is supported by the California Agricultural Experimental Station and USDA/NIFA Multistate Research Project NE1334. This work was supported by USDA/NIFA award 2015-67015-22930 (A.J. Bäumler and H.Z.) and by Public Health Service Grants AI060555 (E.M.V. and G.T.W.), AI044170 (A.J. Bäumler), AI096528 (A.J. Bäumler), AI112445 (A.J. Bäumler), and AI112949 (A.J. Bäumler and R.M.T.).

Funding Information:
Y.L. was supported by Vaadia-BARD Postdoctoral Fellowship FI-505-2014. Work in H.Z.?s laboratory is supported by the California Agricultural Experimental Station and USDA/NIFA Multistate Research Project NE1334. This work was supported by USDA/NIFA award 2015-67015-22930 (A.J. B?umler and H.Z.) and by Public Health Service Grants AI060555 (E.M.V. and G.T.W.), AI044170 (A.J. B?umler), AI096528 (A.J. B?umler), AI112445 (A.J. B?umler), and AI112949 (A.J. B?umler and R.M.T.).

Funding Information:
Y.L. was supported by Vaadia-BARD Postdoctoral Fellowship FI-505-2014. Work in H.Z.’s laboratory is supported by the California Agricultural Experimental Station and USDA /NIFA Multistate Research Project NE1334. This work was supported by USDA/NIFA award 2015-67015-22930 (A.J. Bäumler and H.Z.) and by Public Health Service Grants AI060555 (E.M.V. and G.T.W.), AI044170 (A.J. Bäumler), AI096528 (A.J. Bäumler), AI112445 (A.J. Bäumler), and AI112949 (A.J. Bäumler and R.M.T.).

Publisher Copyright:
© 2018 Elsevier Inc.

Keywords

Enterobacteriaceae
Salmonella
colonization resistance
microbiota
neonate
oxygen

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10.1016/j.chom.2018.12.003

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Litvak, Y., Mon, K. K. Z., Nguyen, H., Chanthavixay, G., Liou, M., Velazquez, E. M., Kutter, L., Alcantara, M. A., Byndloss, M. X., Tiffany, C. R., Walker, G. T., Faber, F., Zhu, Y., Bronner, D. N., Byndloss, A. J., Tsolis, R. M., Zhou, H., & Bäumler, A. J. (2019). Commensal Enterobacteriaceae Protect against Salmonella Colonization through Oxygen Competition. Cell Host and Microbe, 25(1), 128-139.e5. https://doi.org/10.1016/j.chom.2018.12.003

@article{276aace12e074e119fb40e845a804518,

title = "Commensal Enterobacteriaceae Protect against Salmonella Colonization through Oxygen Competition",

abstract = "Neonates are highly susceptible to infection with enteric pathogens, but the underlying mechanisms are not resolved. We show that neonatal chick colonization with Salmonella enterica serovar Enteritidis requires a virulence-factor-dependent increase in epithelial oxygenation, which drives pathogen expansion by aerobic respiration. Co-infection experiments with an Escherichia coli strain carrying an oxygen-sensitive reporter suggest that S. Enteritidis competes with commensal Enterobacteriaceae for oxygen. A combination of Enterobacteriaceae and spore-forming bacteria, but not colonization with either community alone, confers colonization resistance against S. Enteritidis in neonatal chicks, phenocopying germ-free mice associated with adult chicken microbiota. Combining spore-forming bacteria with a probiotic E. coli isolate protects germ-free mice from pathogen colonization, but the protection is lost when the ability to respire oxygen under micro-aerophilic conditions is genetically ablated in E. coli. These results suggest that commensal Enterobacteriaceae contribute to colonization resistance by competing with S. Enteritidis for oxygen, a resource critical for pathogen expansion.",

keywords = "Enterobacteriaceae, Salmonella, colonization resistance, microbiota, neonate, oxygen",

author = "Yael Litvak and Mon, {Khin K.Z.} and Henry Nguyen and Ganrea Chanthavixay and Megan Liou and Velazquez, {Eric M.} and Laura Kutter and Alcantara, {Monique A.} and Byndloss, {Mariana X.} and Tiffany, {Connor R.} and Walker, {Gregory T.} and Franziska Faber and Yuhua Zhu and Bronner, {Denise N.} and Byndloss, {Austin J.} and Tsolis, {Ren{\'e}e M.} and Huaijun Zhou and B{\"a}umler, {Andreas J.}",

note = "Funding Information: Y.L. was supported by Vaadia-BARD Postdoctoral Fellowship FI-505-2014. Work in H.Z.'s laboratory is supported by the California Agricultural Experimental Station and USDA/NIFA Multistate Research Project NE1334. This work was supported by USDA/NIFA award 2015-67015-22930 (A.J. B{\"a}umler and H.Z.) and by Public Health Service Grants AI060555 (E.M.V. and G.T.W.), AI044170 (A.J. B{\"a}umler), AI096528 (A.J. B{\"a}umler), AI112445 (A.J. B{\"a}umler), and AI112949 (A.J. B{\"a}umler and R.M.T.). Funding Information: Y.L. was supported by Vaadia-BARD Postdoctoral Fellowship FI-505-2014. Work in H.Z.?s laboratory is supported by the California Agricultural Experimental Station and USDA/NIFA Multistate Research Project NE1334. This work was supported by USDA/NIFA award 2015-67015-22930 (A.J. B?umler and H.Z.) and by Public Health Service Grants AI060555 (E.M.V. and G.T.W.), AI044170 (A.J. B?umler), AI096528 (A.J. B?umler), AI112445 (A.J. B?umler), and AI112949 (A.J. B?umler and R.M.T.). Funding Information: Y.L. was supported by Vaadia-BARD Postdoctoral Fellowship FI-505-2014. Work in H.Z.{\textquoteright}s laboratory is supported by the California Agricultural Experimental Station and USDA /NIFA Multistate Research Project NE1334. This work was supported by USDA/NIFA award 2015-67015-22930 (A.J. B{\"a}umler and H.Z.) and by Public Health Service Grants AI060555 (E.M.V. and G.T.W.), AI044170 (A.J. B{\"a}umler), AI096528 (A.J. B{\"a}umler), AI112445 (A.J. B{\"a}umler), and AI112949 (A.J. B{\"a}umler and R.M.T.). Publisher Copyright: {\textcopyright} 2018 Elsevier Inc.",

year = "2019",

month = jan,

day = "9",

doi = "10.1016/j.chom.2018.12.003",

language = "American English",

volume = "25",

pages = "128--139.e5",

journal = "Cell Host and Microbe",

issn = "1931-3128",

publisher = "Cell Press",

number = "1",

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Litvak, Y, Mon, KKZ, Nguyen, H, Chanthavixay, G, Liou, M, Velazquez, EM, Kutter, L, Alcantara, MA, Byndloss, MX, Tiffany, CR, Walker, GT, Faber, F, Zhu, Y, Bronner, DN, Byndloss, AJ, Tsolis, RM, Zhou, H & Bäumler, AJ 2019, 'Commensal Enterobacteriaceae Protect against Salmonella Colonization through Oxygen Competition', Cell Host and Microbe, vol. 25, no. 1, pp. 128-139.e5. https://doi.org/10.1016/j.chom.2018.12.003

TY - JOUR

T1 - Commensal Enterobacteriaceae Protect against Salmonella Colonization through Oxygen Competition

AU - Litvak, Yael

AU - Mon, Khin K.Z.

AU - Nguyen, Henry

AU - Chanthavixay, Ganrea

AU - Liou, Megan

AU - Velazquez, Eric M.

AU - Kutter, Laura

AU - Alcantara, Monique A.

AU - Byndloss, Mariana X.

AU - Tiffany, Connor R.

AU - Walker, Gregory T.

AU - Faber, Franziska

AU - Zhu, Yuhua

AU - Bronner, Denise N.

AU - Byndloss, Austin J.

AU - Tsolis, Renée M.

AU - Zhou, Huaijun

AU - Bäumler, Andreas J.

N1 - Funding Information: Y.L. was supported by Vaadia-BARD Postdoctoral Fellowship FI-505-2014. Work in H.Z.'s laboratory is supported by the California Agricultural Experimental Station and USDA/NIFA Multistate Research Project NE1334. This work was supported by USDA/NIFA award 2015-67015-22930 (A.J. Bäumler and H.Z.) and by Public Health Service Grants AI060555 (E.M.V. and G.T.W.), AI044170 (A.J. Bäumler), AI096528 (A.J. Bäumler), AI112445 (A.J. Bäumler), and AI112949 (A.J. Bäumler and R.M.T.). Funding Information: Y.L. was supported by Vaadia-BARD Postdoctoral Fellowship FI-505-2014. Work in H.Z.?s laboratory is supported by the California Agricultural Experimental Station and USDA/NIFA Multistate Research Project NE1334. This work was supported by USDA/NIFA award 2015-67015-22930 (A.J. B?umler and H.Z.) and by Public Health Service Grants AI060555 (E.M.V. and G.T.W.), AI044170 (A.J. B?umler), AI096528 (A.J. B?umler), AI112445 (A.J. B?umler), and AI112949 (A.J. B?umler and R.M.T.). Funding Information: Y.L. was supported by Vaadia-BARD Postdoctoral Fellowship FI-505-2014. Work in H.Z.’s laboratory is supported by the California Agricultural Experimental Station and USDA /NIFA Multistate Research Project NE1334. This work was supported by USDA/NIFA award 2015-67015-22930 (A.J. Bäumler and H.Z.) and by Public Health Service Grants AI060555 (E.M.V. and G.T.W.), AI044170 (A.J. Bäumler), AI096528 (A.J. Bäumler), AI112445 (A.J. Bäumler), and AI112949 (A.J. Bäumler and R.M.T.). Publisher Copyright: © 2018 Elsevier Inc.

PY - 2019/1/9

Y1 - 2019/1/9

N2 - Neonates are highly susceptible to infection with enteric pathogens, but the underlying mechanisms are not resolved. We show that neonatal chick colonization with Salmonella enterica serovar Enteritidis requires a virulence-factor-dependent increase in epithelial oxygenation, which drives pathogen expansion by aerobic respiration. Co-infection experiments with an Escherichia coli strain carrying an oxygen-sensitive reporter suggest that S. Enteritidis competes with commensal Enterobacteriaceae for oxygen. A combination of Enterobacteriaceae and spore-forming bacteria, but not colonization with either community alone, confers colonization resistance against S. Enteritidis in neonatal chicks, phenocopying germ-free mice associated with adult chicken microbiota. Combining spore-forming bacteria with a probiotic E. coli isolate protects germ-free mice from pathogen colonization, but the protection is lost when the ability to respire oxygen under micro-aerophilic conditions is genetically ablated in E. coli. These results suggest that commensal Enterobacteriaceae contribute to colonization resistance by competing with S. Enteritidis for oxygen, a resource critical for pathogen expansion.

AB - Neonates are highly susceptible to infection with enteric pathogens, but the underlying mechanisms are not resolved. We show that neonatal chick colonization with Salmonella enterica serovar Enteritidis requires a virulence-factor-dependent increase in epithelial oxygenation, which drives pathogen expansion by aerobic respiration. Co-infection experiments with an Escherichia coli strain carrying an oxygen-sensitive reporter suggest that S. Enteritidis competes with commensal Enterobacteriaceae for oxygen. A combination of Enterobacteriaceae and spore-forming bacteria, but not colonization with either community alone, confers colonization resistance against S. Enteritidis in neonatal chicks, phenocopying germ-free mice associated with adult chicken microbiota. Combining spore-forming bacteria with a probiotic E. coli isolate protects germ-free mice from pathogen colonization, but the protection is lost when the ability to respire oxygen under micro-aerophilic conditions is genetically ablated in E. coli. These results suggest that commensal Enterobacteriaceae contribute to colonization resistance by competing with S. Enteritidis for oxygen, a resource critical for pathogen expansion.

KW - Enterobacteriaceae

KW - Salmonella

KW - colonization resistance

KW - microbiota

KW - neonate

KW - oxygen

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U2 - 10.1016/j.chom.2018.12.003

DO - 10.1016/j.chom.2018.12.003

M3 - Article

C2 - 30629913

AN - SCOPUS:85059128262

SN - 1931-3128

VL - 25

SP - 128-139.e5

JO - Cell Host and Microbe

JF - Cell Host and Microbe

IS - 1

ER -

Commensal Enterobacteriaceae Protect against Salmonella Colonization through Oxygen Competition

Abstract

Bibliographical note

Keywords

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