Metabolic reconstitution of germ-free mice by a gnotobiotic microbiota varies over the circadian cycle.
Journal
PLoS biology
ISSN: 1545-7885
Titre abrégé: PLoS Biol
Pays: United States
ID NLM: 101183755
Informations de publication
Date de publication:
09 2022
09 2022
Historique:
received:
14
12
2021
accepted:
06
07
2022
entrez:
20
9
2022
pubmed:
21
9
2022
medline:
24
9
2022
Statut:
epublish
Résumé
The capacity of the intestinal microbiota to degrade otherwise indigestible diet components is known to greatly improve the recovery of energy from food. This has led to the hypothesis that increased digestive efficiency may underlie the contribution of the microbiota to obesity. OligoMM12-colonized gnotobiotic mice have a consistently higher fat mass than germ-free (GF) or fully colonized counterparts. We therefore investigated their food intake, digestion efficiency, energy expenditure, and respiratory quotient using a novel isolator-housed metabolic cage system, which allows long-term measurements without contamination risk. This demonstrated that microbiota-released calories are perfectly balanced by decreased food intake in fully colonized versus gnotobiotic OligoMM12 and GF mice fed a standard chow diet, i.e., microbiota-released calories can in fact be well integrated into appetite control. We also observed no significant difference in energy expenditure after normalization by lean mass between the different microbiota groups, suggesting that cumulative small differences in energy balance, or altered energy storage, must underlie fat accumulation in OligoMM12 mice. Consistent with altered energy storage, major differences were observed in the type of respiratory substrates used in metabolism over the circadian cycle: In GF mice, the respiratory exchange ratio (RER) was consistently lower than that of fully colonized mice at all times of day, indicative of more reliance on fat and less on glucose metabolism. Intriguingly, the RER of OligoMM12-colonized gnotobiotic mice phenocopied fully colonized mice during the dark (active/eating) phase but phenocopied GF mice during the light (fasting/resting) phase. Further, OligoMM12-colonized mice showed a GF-like drop in liver glycogen storage during the light phase and both liver and plasma metabolomes of OligoMM12 mice clustered closely with GF mice. This implies the existence of microbiota functions that are required to maintain normal host metabolism during the resting/fasting phase of circadian cycle and which are absent in the OligoMM12 consortium.
Identifiants
pubmed: 36126044
doi: 10.1371/journal.pbio.3001743
pii: PBIOLOGY-D-21-03250
pmc: PMC9488797
doi:
Substances chimiques
Liver Glycogen
0
Glucose
IY9XDZ35W2
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
e3001743Commentaires et corrections
Type : CommentIn
Déclaration de conflit d'intérêts
The authors have declared that no competing interests exist.
Références
Biochem Biophys Res Commun. 2008 Dec 19;377(3):987-91
pubmed: 18952058
Proc Natl Acad Sci U S A. 2014 May 20;111(20):7421-6
pubmed: 24799697
Mol Syst Biol. 2008;4:219
pubmed: 18854818
Obes Res. 2004 Jan;12(1):150-60
pubmed: 14742854
Diabetes. 2010 Feb;59(2):323-9
pubmed: 20103710
Mol Metab. 2012 Aug 03;1(1-2):21-31
pubmed: 24024115
Sci Rep. 2018 Jan 23;8(1):1395
pubmed: 29362450
Nat Methods. 2011 Dec 28;9(1):57-63
pubmed: 22205519
Science. 2013 Sep 6;341(6150):1241214
pubmed: 24009397
Environ Microbiol. 2016 May;18(5):1403-14
pubmed: 26271760
Nat Commun. 2021 Aug 5;12(1):4725
pubmed: 34354051
Nat Med. 2015 Dec;21(12):1497-1501
pubmed: 26569380
Microbiome. 2019 Dec 12;7(1):158
pubmed: 31831058
Nature. 2006 Dec 21;444(7122):1027-31
pubmed: 17183312
Cell Metab. 2013 Feb 5;17(2):225-35
pubmed: 23395169
J Exp Biol. 2005 May;208(Pt 9):1611-9
pubmed: 15855392
Diabetes. 2011 Jan;60(1):17-23
pubmed: 21193735
Proc Natl Acad Sci U S A. 2007 Jan 16;104(3):979-84
pubmed: 17210919
Anal Chem. 2006 Feb 1;78(3):779-87
pubmed: 16448051
Mol Nutr Food Res. 2015 Nov;59(11):2267-78
pubmed: 26202344
Nat Methods. 2016 Jul;13(7):581-3
pubmed: 27214047
Proc Natl Acad Sci U S A. 2004 Nov 2;101(44):15718-23
pubmed: 15505215
Br J Nutr. 2010 Sep;104(6):919-29
pubmed: 20441670
Cell Rep. 2019 Mar 5;26(10):2720-2737.e5
pubmed: 30840893
J Appl Physiol. 1949 Jul;2(1):1-15
pubmed: 18133122
Science. 2017 Sep 1;357(6354):912-916
pubmed: 28860383
FEMS Microbiol Ecol. 2011 Jul;77(1):107-19
pubmed: 21395623
Microbiome. 2018 Aug 9;6(1):140
pubmed: 30092815
Proc Soc Exp Biol Med. 1968 May;128(1):137-41
pubmed: 5656680
Nat Commun. 2018 Jul 20;9(1):2872
pubmed: 30030441
Elife. 2020 May 01;9:
pubmed: 32356724
J Nutr Biochem. 2018 Jul;57:130-135
pubmed: 29702431
J Biol Chem. 2010 Jul 16;285(29):22114-21
pubmed: 20430893
Curr Protoc Mouse Biol. 2015 Sep 01;5(3):205-222
pubmed: 26331756
Cell Metab. 2018 Oct 2;28(4):656-666.e1
pubmed: 30017358
Nat Methods. 2019 Sep;16(9):797-799
pubmed: 31391589
Cell Metab. 2020 Mar 3;31(3):592-604.e9
pubmed: 32084379
Microbiome. 2018 Dec 17;6(1):226
pubmed: 30558668
Cell. 2014 Oct 23;159(3):514-29
pubmed: 25417104
Nat Commun. 2020 May 22;11(1):2590
pubmed: 32444602
Obesity (Silver Spring). 2017 Mar;25 Suppl 1:S8-S16
pubmed: 28229538
JPEN J Parenter Enteral Nutr. 1978 May;2(2):78-107
pubmed: 575910
Nat Microbiol. 2019 Dec;4(12):2164-2174
pubmed: 31591555
Mol Metab. 2016 Oct 13;5(12):1162-1174
pubmed: 27900259
Eur J Clin Nutr. 2018 May;72(5):698-709
pubmed: 29748653
Nucleic Acids Res. 2013 Jan;41(Database issue):D590-6
pubmed: 23193283
Cell. 2018 Mar 8;172(6):1198-1215
pubmed: 29522742
Nat Rev Endocrinol. 2017 Jan;13(1):11-25
pubmed: 27616451
Front Physiol. 2013 Mar 14;4:34
pubmed: 23504620
Nat Microbiol. 2016 Nov 21;2:16215
pubmed: 27869789
Nature. 2021 Jul;595(7866):272-277
pubmed: 34163067
STAR Protoc. 2021 Jun 12;2(2):100607
pubmed: 34179836
Int J Body Compos Res. 2010 Mar 1;8(1):17-29
pubmed: 21152249
mBio. 2014 Sep 30;5(5):e01530-14
pubmed: 25271283
Life Sci. 1976 Dec 15;19(12):1873-8
pubmed: 826747
J Nutr. 1969 Apr;97(4):542-52
pubmed: 4305338
Biomolecules. 2019 Mar 28;9(4):
pubmed: 30925749
Science. 2019 Sep 27;365(6460):1428-1434
pubmed: 31604271
J Physiol. 1949 Aug;109(1-2):1-9
pubmed: 15394301
Mol Cell. 2020 May 21;78(4):584-596
pubmed: 32234490
J Proteome Res. 2020 Apr 3;19(4):1447-1458
pubmed: 31984744
Nat Protoc. 2016 Aug;11(8):1531-53
pubmed: 27466712
PLoS One. 2012;7(4):e35240
pubmed: 22506074
Int J Obes (Lond). 2006 Sep;30(9):1322-31
pubmed: 16801931
Appl Environ Microbiol. 2004 Oct;70(10):5810-7
pubmed: 15466518
ISME J. 2022 Apr;16(4):1095-1109
pubmed: 34857933
Lab Anim (NY). 2017 Oct 6;46(10):373-377
pubmed: 28984861
Cell Host Microbe. 2021 Apr 14;29(4):650-663.e9
pubmed: 33662276
Front Microbiol. 2020 Jan 10;10:2999
pubmed: 31998276
Cell Rep. 2019 Mar 26;26(13):3772-3783.e6
pubmed: 30917328
Cell Metab. 2015 Oct 6;22(4):658-68
pubmed: 26321659
Cell. 2016 Dec 1;167(6):1495-1510.e12
pubmed: 27912059
Sci Transl Med. 2014 Jan 22;6(220):220ra11
pubmed: 24452263
Gut Microbes. 2021 Jan-Dec;13(1):1-21
pubmed: 33382950
Elife. 2018 Jul 17;7:
pubmed: 30014852
Lab Anim Sci. 1983 Feb;33(1):46-50
pubmed: 6834773
Nat Metab. 2019 Jan;1(1):34-46
pubmed: 32694818
Mol Syst Biol. 2015 Oct 16;11(10):834
pubmed: 26475342
Bacteriol Rev. 1971 Dec;35(4):390-429
pubmed: 4945725
EcoSal Plus. 2008 Sep;3(1):
pubmed: 26443740
Proc Nutr Soc. 2015 Feb;74(1):13-22
pubmed: 25268552
Bioinformatics. 2018 Dec 15;34(24):4313-4314
pubmed: 29955821
Nature. 2016 Jul 06;535(7610):56-64
pubmed: 27383980
Cell Metab. 2014 Dec 2;20(6):1006-17
pubmed: 25470548
Heliyon. 2019 Jun 18;5(6):e01950
pubmed: 31286084
Cell. 2020 Jan 23;180(2):221-232
pubmed: 31978342
J Biol Chem. 2009 Jan 30;284(5):2811-2822
pubmed: 19047060
Gut Microbes. 2011 Jan-Feb;2(1):25-33
pubmed: 21637015
Physiol Rep. 2017 Mar;5(6):
pubmed: 28320888