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A secondary metabolite drives intraspecies antagonism in a gut symbiont that is inhibited by peptidoglycan acetylation

Mustafa Özçam, Jee-Hwan Oh, Restituto Tocmo, Deepa Acharya, Shenwei Zhang, Silvette Ruiz-Ramírez, Fuyong Li, Christopher C. Cheng, Eugenio Vivas, Federico E. Rey, Jan Claesen, Tim Bugni, Jens Walter, View ORCID ProfileJan-Peter van Pijkeren
doi: https://doi.org/10.1101/2021.06.11.448121
Mustafa Özçam
1Department of Food Science, University of Wisconsin-Madison, Madison, WI, 53706, USA
2Division of Gastroenterology, Department of Medicine, University of California San Francisco, CA, 94141, USA.
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Jee-Hwan Oh
1Department of Food Science, University of Wisconsin-Madison, Madison, WI, 53706, USA
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Restituto Tocmo
1Department of Food Science, University of Wisconsin-Madison, Madison, WI, 53706, USA
3Department of Pharmacy Practice, University of Illinois at Chicago, Chicago, IL, 60612, USA
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Deepa Acharya
4Department of Pharmacy, University of Wisconsin-Madison, Madison, WI, 53706, USA
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Shenwei Zhang
1Department of Food Science, University of Wisconsin-Madison, Madison, WI, 53706, USA
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Silvette Ruiz-Ramírez
1Department of Food Science, University of Wisconsin-Madison, Madison, WI, 53706, USA
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Fuyong Li
5Department of Agriculture, Food and Nutritional Science, University of Alberta, Edmonton, AB T6G 2P5, Canada
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Christopher C. Cheng
6Department of Biological Sciences, University of Alberta, Edmonton, AB T6G 2P5, Canada;
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Eugenio Vivas
7Department of Bacteriology, University of Wisconsin-Madison, Madison, WI, 53706, USA
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Federico E. Rey
7Department of Bacteriology, University of Wisconsin-Madison, Madison, WI, 53706, USA
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Jan Claesen
8Department of Cardiovascular and Metabolic Sciences and Center for Microbiome and Human Health, Lerner Research Institute, Cleveland Clinic, Cleveland, OH, 44195, USA
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Tim Bugni
4Department of Pharmacy, University of Wisconsin-Madison, Madison, WI, 53706, USA
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Jens Walter
5Department of Agriculture, Food and Nutritional Science, University of Alberta, Edmonton, AB T6G 2P5, Canada
6Department of Biological Sciences, University of Alberta, Edmonton, AB T6G 2P5, Canada;
9Department of Medicine and APC Microbiome Ireland, University College Cork, Cork T12 K8AF, Ireland
10School of Microbiology, University College Cork, Cork T12 YT20, Ireland
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Jan-Peter van Pijkeren
1Department of Food Science, University of Wisconsin-Madison, Madison, WI, 53706, USA
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  • ORCID record for Jan-Peter van Pijkeren
  • For correspondence: vanpijkeren@wisc.edu
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SUMMARY

The mammalian microbiome encodes numerous secondary metabolite biosynthetic gene clusters, yet their role in microbe-microbe interactions is unclear. Here, we characterized two polyketide synthase gene clusters (fun and pks) in the gut symbiont Limosilactobacillus reuteri. The pks, but not the fun cluster, encodes antimicrobial activity. Forty-one out of 51 L. reuteri strains tested are sensitive to Pks products, which was independent of strains’ host origin. The sensitivity to Pks was also established in intraspecies competition experiments in gnotobiotic mice. Comparative genome analyses between Pks-resistant and sensitive strains identified an acyltransferase gene (act) that is unique to Pks-resistant strains. Subsequent peptidoglycan analysis of the wild-type and the act mutant strains showed that Act acetylates peptidoglycan. The pks mutants lost their competitive advantage and act mutants lost their Pks resistance in vivo. Thus, our findings provide mechanistic insights into how closely related gut symbionts can compete and co-exist in the gastrointestinal tract.

Competing Interest Statement

JPVP received unrestricted funds from BioGaia, AB, a probiotic-producing company. JPVP is the founder of the consulting company Next-Gen Probiotics, LLC. JW has received grants and honoraria from several food and ingredient companies, including companies that produce probiotics. JW is a co-owner of Synbiotic Solutions, LLC, and is on the Scientific Advisory Board of Alimentary Health. M.O. was an employee of DuPont Nutrition and Biosciences. JC is a Scientific Advisor for Seed Health, Inc.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. All rights reserved. No reuse allowed without permission.
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Posted June 12, 2021.
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A secondary metabolite drives intraspecies antagonism in a gut symbiont that is inhibited by peptidoglycan acetylation
Mustafa Özçam, Jee-Hwan Oh, Restituto Tocmo, Deepa Acharya, Shenwei Zhang, Silvette Ruiz-Ramírez, Fuyong Li, Christopher C. Cheng, Eugenio Vivas, Federico E. Rey, Jan Claesen, Tim Bugni, Jens Walter, Jan-Peter van Pijkeren
bioRxiv 2021.06.11.448121; doi: https://doi.org/10.1101/2021.06.11.448121
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A secondary metabolite drives intraspecies antagonism in a gut symbiont that is inhibited by peptidoglycan acetylation
Mustafa Özçam, Jee-Hwan Oh, Restituto Tocmo, Deepa Acharya, Shenwei Zhang, Silvette Ruiz-Ramírez, Fuyong Li, Christopher C. Cheng, Eugenio Vivas, Federico E. Rey, Jan Claesen, Tim Bugni, Jens Walter, Jan-Peter van Pijkeren
bioRxiv 2021.06.11.448121; doi: https://doi.org/10.1101/2021.06.11.448121

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