Chellappa, Sarah L. ORCID: 0000-0002-6190-464X, Engen, Phillip A., Naqib, Ankur ORCID: 0000-0003-0832-5646, Qian, Jingyi, Vujovic, Nina, Rahman, Nishath, Green, Stefan J., Garaulet, Marta ORCID: 0000-0002-4066-3509, Keshavarzian, Ali and Scheer, Frank A. J. L. (2022). Proof-of-principle demonstration of endogenous circadian system and circadian misalignment effects on human oral microbiota. Faseb J., 36 (1). HOBOKEN: WILEY. ISSN 1530-6860

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Abstract

Circadian misalignment-the misalignment between the central circadian clock and behavioral and environmental cycles (including sleep/wake, fasting/eating, dark/light)-results in adverse cardiovascular and metabolic effects. Potential underlying mechanisms for these adverse effects include alterations in the orogastrointestinal microbiota. However, it remains unknown whether human oral microbiota has endogenous circadian rhythms (i.e., independent of sleep/wake, fasting/eating, and dark/light cycles) and whether circadian misalignment influences oral microbiota community composition. Healthy young individuals [27.3 +/- 2.3 years (18-35 years), 4 men and 2 women, body-mass index range: 18-28 kg/m(2)] were enrolled in a stringently controlled 14-day circadian laboratory protocol. This included a 32-h constant routine (CR) protocol (endogenous circadian baseline assessment), a forced desynchrony protocol with four 28-h days under similar to 3 lx to induce circadian misalignment, and a post-misalignment 40-h CR protocol. Microbiota assessments were performed on saliva samples collected every 4 h throughout both CR protocols. Total DNA was extracted and processed using high-throughput 16S ribosomal RNA gene amplicon sequencing. The relative abundance of specific oral microbiota populations, i.e., one of the five dominant phyla, and three of the fourteen dominant genera, exhibited significant endogenous circadian rhythms. Importantly, circadian misalignment dramatically altered the oral microbiota landscape, such that four of the five dominant phyla and eight of the fourteen dominant genera exhibited significant circadian misalignment effects. Moreover, circadian misalignment significantly affected the metagenome functional content of oral microbiota (inferred gene content analysis), as indicated by changes in specific functional pathways associated with metabolic control and immunity. Collectively, our proof-of-concept study provides evidence for endogenous circadian rhythms in human oral microbiota and show that even relatively short-term experimental circadian misalignment can dramatically affect microbiota community composition and functional pathways involved in metabolism and immune function. These proof-of-principle findings have translational relevance to individuals typically exposed to circadian misalignment, including night shift workers and frequent flyers.

Item Type: Journal Article
Creators:
CreatorsEmailORCIDORCID Put Code
Chellappa, Sarah L.UNSPECIFIEDorcid.org/0000-0002-6190-464XUNSPECIFIED
Engen, Phillip A.UNSPECIFIEDUNSPECIFIEDUNSPECIFIED
Naqib, AnkurUNSPECIFIEDorcid.org/0000-0003-0832-5646UNSPECIFIED
Qian, JingyiUNSPECIFIEDUNSPECIFIEDUNSPECIFIED
Vujovic, NinaUNSPECIFIEDUNSPECIFIEDUNSPECIFIED
Rahman, NishathUNSPECIFIEDUNSPECIFIEDUNSPECIFIED
Green, Stefan J.UNSPECIFIEDUNSPECIFIEDUNSPECIFIED
Garaulet, MartaUNSPECIFIEDorcid.org/0000-0002-4066-3509UNSPECIFIED
Keshavarzian, AliUNSPECIFIEDUNSPECIFIEDUNSPECIFIED
Scheer, Frank A. J. L.UNSPECIFIEDUNSPECIFIEDUNSPECIFIED
URN: urn:nbn:de:hbz:38-685155
DOI: 10.1096/fj.202101153R
Journal or Publication Title: Faseb J.
Volume: 36
Number: 1
Date: 2022
Publisher: WILEY
Place of Publication: HOBOKEN
ISSN: 1530-6860
Language: English
Faculty: Unspecified
Divisions: Unspecified
Subjects: no entry
Uncontrolled Keywords:
KeywordsLanguage
NIGHT-SHIFT WORK; IMPACT; RISK; CELL; OSCILLATIONS; METABOLISM; DIVERSITY; BACTERIAL; DISEASE; HEALTHMultiple languages
Biochemistry & Molecular Biology; Biology; Cell BiologyMultiple languages
URI: http://kups.ub.uni-koeln.de/id/eprint/68515

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