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Microbial nitrogen limitation in the mammalian large intestine

Microbial nitrogen limitation in the mammalian large intestine
Microbial nitrogen limitation in the mammalian large intestine

Resource limitation is a fundamental factor governing the composition and function of ecological communities. However, the role of resource supply in structuring the intestinal microbiome has not been established and represents a challenge for mammals that rely on microbial symbionts for digestion: too little supply might starve the microbiome while too much might starve the host. We present evidence that microbiota occupy a habitat that is limited in total nitrogen supply within the large intestines of 30 mammal species. Lowering dietary protein levels in mice reduced their faecal concentrations of bacteria. A gradient of stoichiometry along the length of the gut was consistent with the hypothesis that intestinal nitrogen limitation results from host absorption of dietary nutrients. Nitrogen availability is also likely to be shaped by host-microbe interactions: levels of host-secreted nitrogen were altered in germ-free mice and when bacterial loads were reduced via experimental antibiotic treatment. Single-cell spectrometry revealed that members of the phylum Bacteroidetes consumed nitrogen in the large intestine more readily than other commensal taxa did. Our findings support a model where nitrogen limitation arises from preferential host use of dietary nutrients. We speculate that this resource limitation could enable hosts to regulate microbial communities in the large intestine. Commensal microbiota may have adapted to nitrogen-limited settings, suggesting one reason why excess dietary protein has been associated with degraded gut-microbial ecosystems.

Animals, Bacteria/classification, Carbon/metabolism, Diet, Dietary Proteins, Feces/microbiology, Gastrointestinal Microbiome/physiology, Host Microbial Interactions/physiology, Intestine, Large/metabolism, Mammals/microbiology, Mice, Nitrogen/metabolism, RNA, Ribosomal, 16S/genetics, Symbiosis
2058-5276
1441-1450
Reese, Aspen T
1d5bc13a-f94e-4054-b405-08dd7a2e2a44
Pereira, Fátima C
a9396948-26f9-4f13-8f83-a22fec1dd0e0
Schintlmeister, Arno
f759d96e-8895-434c-bf74-5879021635f7
Berry, David
97308fd9-0d70-4014-b085-1c2e64b6ecc5
Wagner, Michael
b1db4f29-c6dc-444b-b750-5f6a7afcfab7
Hale, Laura P
cbc2ad10-2efc-49e1-8c3a-4db26e12b79d
Wu, Anchi
000761b2-a97a-419d-8054-82c7e144501f
Jiang, Sharon
83255769-6692-4288-8be6-c163fdb39162
Durand, Heather K
8fe935ac-bbfe-42de-9daa-e0d10ee49f80
Zhou, Xiyou
54199815-47ff-470d-b95b-24b6ad2364fe
Premont, Richard T
7704286a-0eb5-49ee-a91f-85453cc28c4a
Diehl, Anna Mae
d8d2d629-50e7-47c0-8743-cbbcde2660cb
O'Connell, Thomas M
e12bc520-c4a1-48b8-8625-e1558e0438eb
Alberts, Susan C
592f6631-540a-4fbf-8956-00d1961b0ff9
Kartzinel, Tyler R
1af6c71e-03f7-4cd5-aa31-88b9451d9202
Pringle, Robert M
c3e2ef1c-3f3e-4a69-b09c-4d6af46a2fce
Dunn, Robert R
f0dc2a9a-aa44-491e-88fc-3fb550f2cc02
Wright, Justin P
e012b6bc-d5ef-4455-b574-ce3b86e4f819
David, Lawrence A
6a479e97-9bb7-413a-93ec-553e990fbf9f
Reese, Aspen T
1d5bc13a-f94e-4054-b405-08dd7a2e2a44
Pereira, Fátima C
a9396948-26f9-4f13-8f83-a22fec1dd0e0
Schintlmeister, Arno
f759d96e-8895-434c-bf74-5879021635f7
Berry, David
97308fd9-0d70-4014-b085-1c2e64b6ecc5
Wagner, Michael
b1db4f29-c6dc-444b-b750-5f6a7afcfab7
Hale, Laura P
cbc2ad10-2efc-49e1-8c3a-4db26e12b79d
Wu, Anchi
000761b2-a97a-419d-8054-82c7e144501f
Jiang, Sharon
83255769-6692-4288-8be6-c163fdb39162
Durand, Heather K
8fe935ac-bbfe-42de-9daa-e0d10ee49f80
Zhou, Xiyou
54199815-47ff-470d-b95b-24b6ad2364fe
Premont, Richard T
7704286a-0eb5-49ee-a91f-85453cc28c4a
Diehl, Anna Mae
d8d2d629-50e7-47c0-8743-cbbcde2660cb
O'Connell, Thomas M
e12bc520-c4a1-48b8-8625-e1558e0438eb
Alberts, Susan C
592f6631-540a-4fbf-8956-00d1961b0ff9
Kartzinel, Tyler R
1af6c71e-03f7-4cd5-aa31-88b9451d9202
Pringle, Robert M
c3e2ef1c-3f3e-4a69-b09c-4d6af46a2fce
Dunn, Robert R
f0dc2a9a-aa44-491e-88fc-3fb550f2cc02
Wright, Justin P
e012b6bc-d5ef-4455-b574-ce3b86e4f819
David, Lawrence A
6a479e97-9bb7-413a-93ec-553e990fbf9f

Reese, Aspen T, Pereira, Fátima C, Schintlmeister, Arno, Berry, David, Wagner, Michael, Hale, Laura P, Wu, Anchi, Jiang, Sharon, Durand, Heather K, Zhou, Xiyou, Premont, Richard T, Diehl, Anna Mae, O'Connell, Thomas M, Alberts, Susan C, Kartzinel, Tyler R, Pringle, Robert M, Dunn, Robert R, Wright, Justin P and David, Lawrence A (2018) Microbial nitrogen limitation in the mammalian large intestine. Nature Microbiology, 3 (12), 1441-1450. (doi:10.1038/s41564-018-0267-7).

Record type: Article

Abstract

Resource limitation is a fundamental factor governing the composition and function of ecological communities. However, the role of resource supply in structuring the intestinal microbiome has not been established and represents a challenge for mammals that rely on microbial symbionts for digestion: too little supply might starve the microbiome while too much might starve the host. We present evidence that microbiota occupy a habitat that is limited in total nitrogen supply within the large intestines of 30 mammal species. Lowering dietary protein levels in mice reduced their faecal concentrations of bacteria. A gradient of stoichiometry along the length of the gut was consistent with the hypothesis that intestinal nitrogen limitation results from host absorption of dietary nutrients. Nitrogen availability is also likely to be shaped by host-microbe interactions: levels of host-secreted nitrogen were altered in germ-free mice and when bacterial loads were reduced via experimental antibiotic treatment. Single-cell spectrometry revealed that members of the phylum Bacteroidetes consumed nitrogen in the large intestine more readily than other commensal taxa did. Our findings support a model where nitrogen limitation arises from preferential host use of dietary nutrients. We speculate that this resource limitation could enable hosts to regulate microbial communities in the large intestine. Commensal microbiota may have adapted to nitrogen-limited settings, suggesting one reason why excess dietary protein has been associated with degraded gut-microbial ecosystems.

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More information

e-pub ahead of print date: 29 October 2018
Published date: 1 December 2018
Keywords: Animals, Bacteria/classification, Carbon/metabolism, Diet, Dietary Proteins, Feces/microbiology, Gastrointestinal Microbiome/physiology, Host Microbial Interactions/physiology, Intestine, Large/metabolism, Mammals/microbiology, Mice, Nitrogen/metabolism, RNA, Ribosomal, 16S/genetics, Symbiosis

Identifiers

Local EPrints ID: 470697
URI: http://eprints.soton.ac.uk/id/eprint/470697
ISSN: 2058-5276
PURE UUID: 1c9c7075-5a4e-47c8-a26e-b25bb44097c6
ORCID for Fátima C Pereira: ORCID iD orcid.org/0000-0002-1288-6481

Catalogue record

Date deposited: 18 Oct 2022 16:41
Last modified: 17 Mar 2024 04:14

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Contributors

Author: Aspen T Reese
Author: Fátima C Pereira ORCID iD
Author: Arno Schintlmeister
Author: David Berry
Author: Michael Wagner
Author: Laura P Hale
Author: Anchi Wu
Author: Sharon Jiang
Author: Heather K Durand
Author: Xiyou Zhou
Author: Richard T Premont
Author: Anna Mae Diehl
Author: Thomas M O'Connell
Author: Susan C Alberts
Author: Tyler R Kartzinel
Author: Robert M Pringle
Author: Robert R Dunn
Author: Justin P Wright
Author: Lawrence A David

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