Circadian oscillations of microbial and functional composition in the human salivary microbiome.
The human microbiomes across the body evidently interact with various signals in response to biogeographical physiological conditions. To understand such interactions in detail, we investigated how the salivary microbiome in the oral cavity would be regulated by host-related signals. Here, we show that the microbial abundance and gene participating in keeping the human salivary microbiome exhibit global circadian rhythm. Analysis of the 16S rRNA sequences of salivary microbial samples of six healthy adults collected at 4-h intervals for three days revealed that the microbial genera accounting for 68.4-89.6% of the total abundance were observed to significantly oscillate with the periodicity of ∼24 h. These oscillation patterns showed high variations amongst individuals, and the extent of circadian variations in individuals was generally lower than that of interindividual variations. Of the microbial categories oscillated, those classified by aerobic/anaerobic growth and Gram staining, Firmicutes including Streptococcus and Gemella, and Bacteroidetes including Prevotella showed high association with the circadian oscillation. The circadian oscillation was completely abolished by incubating the saliva in vitro, suggesting that host's physiological changes mostly contributed to the microbial oscillation. Further metagenomic analysis showed that circadian oscillation enriched the functions of environmental responses such as various transporters and two-component regulatory systems in the evening, and those of metabolisms such as the biosynthesis of vitamins and fatty acids in the morning.
Laboratory of Metagenomics, Department of Computational Biology and Medical Science, Graduate School of Frontier Sciences, The University of Tokyo, 5-1-5, Kashiwanoha, Kashiwa, Chiba 277-8561, Japan.
Lena
L
Takayasu
Laboratory of Metagenomics, Department of Computational Biology and Medical Science, Graduate School of Frontier Sciences, The University of Tokyo, 5-1-5, Kashiwanoha, Kashiwa, Chiba 277-8561, Japan.|Department of Microbiology and Immunology, School of Medicine, Keio University, 35 Shinanomachi, Shinjuku-ku, Tokyo 160-8582, Japan.
Wataru
W
Suda
Laboratory of Metagenomics, Department of Computational Biology and Medical Science, Graduate School of Frontier Sciences, The University of Tokyo, 5-1-5, Kashiwanoha, Kashiwa, Chiba 277-8561, Japan.
Kageyasu
K
Takanashi
Laboratory of Metagenomics, Department of Computational Biology and Medical Science, Graduate School of Frontier Sciences, The University of Tokyo, 5-1-5, Kashiwanoha, Kashiwa, Chiba 277-8561, Japan.
Erica
E
Iioka
Laboratory of Metagenomics, Department of Computational Biology and Medical Science, Graduate School of Frontier Sciences, The University of Tokyo, 5-1-5, Kashiwanoha, Kashiwa, Chiba 277-8561, Japan.
Rina
R
Kurokawa
Laboratory of Metagenomics, Department of Computational Biology and Medical Science, Graduate School of Frontier Sciences, The University of Tokyo, 5-1-5, Kashiwanoha, Kashiwa, Chiba 277-8561, Japan.
Chie
C
Shindo
Laboratory of Metagenomics, Department of Computational Biology and Medical Science, Graduate School of Frontier Sciences, The University of Tokyo, 5-1-5, Kashiwanoha, Kashiwa, Chiba 277-8561, Japan.
Yasue
Y
Hattori
Laboratory of Metagenomics, Department of Computational Biology and Medical Science, Graduate School of Frontier Sciences, The University of Tokyo, 5-1-5, Kashiwanoha, Kashiwa, Chiba 277-8561, Japan.
Naoko
N
Yamashita
Laboratory of Metagenomics, Department of Computational Biology and Medical Science, Graduate School of Frontier Sciences, The University of Tokyo, 5-1-5, Kashiwanoha, Kashiwa, Chiba 277-8561, Japan.
Suguru
S
Nishijima
Laboratory of Metagenomics, Department of Computational Biology and Medical Science, Graduate School of Frontier Sciences, The University of Tokyo, 5-1-5, Kashiwanoha, Kashiwa, Chiba 277-8561, Japan.
Kenshiro
K
Oshima
Laboratory of Metagenomics, Department of Computational Biology and Medical Science, Graduate School of Frontier Sciences, The University of Tokyo, 5-1-5, Kashiwanoha, Kashiwa, Chiba 277-8561, Japan.|Cooperative Major in Advanced Health Science, Graduate School of Advanced Science and Engineering, Faculty of Science and Engineering, Waseda University, 3-4-1 Okubo, Shinjuku-ku, Tokyo 169-8555, Japan.
Masahira
M
Hattori
D000328:Adult; D001419:Bacteria / Q000235:genetics / Q000302:isolation & purification* / Q000378:metabolism; D018407:Bacterial Physiological Phenomena; D002940:Circadian Rhythm; D005227:Fatty Acids / Q000096:biosynthesis; D005260:Female; D000069196:Gastrointestinal Microbiome / Q000235:genetics / Q000502:physiology*; D006801:Humans; D008297:Male; D054892:Metagenome; D012329:RNA, Bacterial; D012336:RNA, Ribosomal, 16S; D012463:Saliva / Q000382:microbiology*; D014815:Vitamins / Q000096:biosynthesis
D005227:Fatty Acids; D012329:RNA, Bacterial; D012336:RNA, Ribosomal, 16S; D014815:Vitamins
16S rRNA gene; circadian rhythm; human; oral; salivary microbiome