Transition of Bacterial Diversity and Composition in Tongue Microbiota during the First Two Years of Life

ABSTRACT Newborns are constantly exposed to various microbes from birth; hence, diverse commensal bacteria colonize the oral cavity. However, how or when these bacteria construct a complex and stable ecosystem remains unclear. This prospective cohort study examined the temporal changes in bacterial...

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Autores principales: Shinya Kageyama, Mikari Asakawa, Toru Takeshita, Yukari Ihara, Shunsuke Kanno, Toshiro Hara, Ichiro Takahashi, Yoshihisa Yamashita
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Publicado: American Society for Microbiology 2019
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spelling oai:doaj.org-article:a58555be762f402c88830ad5c7b705b82021-11-15T15:22:20ZTransition of Bacterial Diversity and Composition in Tongue Microbiota during the First Two Years of Life10.1128/mSphere.00187-192379-5042https://doaj.org/article/a58555be762f402c88830ad5c7b705b82019-06-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSphere.00187-19https://doaj.org/toc/2379-5042ABSTRACT Newborns are constantly exposed to various microbes from birth; hence, diverse commensal bacteria colonize the oral cavity. However, how or when these bacteria construct a complex and stable ecosystem remains unclear. This prospective cohort study examined the temporal changes in bacterial diversity and composition in tongue microbiota during infancy. We longitudinally collected a total of 464 tongue swab samples from 8 infants (age of <6 months at baseline) for approximately 2 years. We also collected samples from 32 children (aged 0 to 2 years) and 73 adults (aged 20 to 29 years) cross-sectionally as control groups. Bacterial diversities and compositions were determined by 16S rRNA gene sequencing. The tongue bacterial diversity in infancy, measured as the number of observed operational taxonomic units (OTUs), rapidly increased and nearly reached the same level as that in adults by around 80 weeks. The overall tongue bacterial composition in the transitional phase, 80 to 120 weeks, was more similar to that of adults than to that of the early exponential phase (EEP), 10 to 29 weeks, according to analysis of similarities. Dominant OTUs in the EEP corresponding to Streptococcus peroris and Streptococcus lactarius exponentially decreased immediately after EEP, around 30 to 49 weeks, whereas several OTUs corresponding to Granulicatella adiacens, Actinomyces odontolyticus, and Fusobacterium periodonticum reciprocally increased during the same period. These results suggest that a drastic compositional shift of tongue microbiota occurs before the age of 1 year, and then bacterial diversity and overall bacterial composition reach levels comparable to those in adults by the age of 2 years. IMPORTANCE Evaluating the development of oral microbiota during infancy is important for understanding the subsequent colonization of bacterial species and the process of formation of mature microbiota in the oral cavity. We examined tongue microbiota longitudinally collected from 8 infants and found that drastic compositional shifts in tongue microbiota occur before the age of 1 year, and then bacterial diversity and overall bacterial composition reach levels comparable to those in adults by the age of 2 years. These results may be helpful for preventing the development of various diseases associated with oral microbiota throughout life.Shinya KageyamaMikari AsakawaToru TakeshitaYukari IharaShunsuke KannoToshiro HaraIchiro TakahashiYoshihisa YamashitaAmerican Society for Microbiologyarticledevelopmentinfancyoral microbiotatongueMicrobiologyQR1-502ENmSphere, Vol 4, Iss 3 (2019)
institution DOAJ
collection DOAJ
language EN
topic development
infancy
oral microbiota
tongue
Microbiology
QR1-502
spellingShingle development
infancy
oral microbiota
tongue
Microbiology
QR1-502
Shinya Kageyama
Mikari Asakawa
Toru Takeshita
Yukari Ihara
Shunsuke Kanno
Toshiro Hara
Ichiro Takahashi
Yoshihisa Yamashita
Transition of Bacterial Diversity and Composition in Tongue Microbiota during the First Two Years of Life
description ABSTRACT Newborns are constantly exposed to various microbes from birth; hence, diverse commensal bacteria colonize the oral cavity. However, how or when these bacteria construct a complex and stable ecosystem remains unclear. This prospective cohort study examined the temporal changes in bacterial diversity and composition in tongue microbiota during infancy. We longitudinally collected a total of 464 tongue swab samples from 8 infants (age of <6 months at baseline) for approximately 2 years. We also collected samples from 32 children (aged 0 to 2 years) and 73 adults (aged 20 to 29 years) cross-sectionally as control groups. Bacterial diversities and compositions were determined by 16S rRNA gene sequencing. The tongue bacterial diversity in infancy, measured as the number of observed operational taxonomic units (OTUs), rapidly increased and nearly reached the same level as that in adults by around 80 weeks. The overall tongue bacterial composition in the transitional phase, 80 to 120 weeks, was more similar to that of adults than to that of the early exponential phase (EEP), 10 to 29 weeks, according to analysis of similarities. Dominant OTUs in the EEP corresponding to Streptococcus peroris and Streptococcus lactarius exponentially decreased immediately after EEP, around 30 to 49 weeks, whereas several OTUs corresponding to Granulicatella adiacens, Actinomyces odontolyticus, and Fusobacterium periodonticum reciprocally increased during the same period. These results suggest that a drastic compositional shift of tongue microbiota occurs before the age of 1 year, and then bacterial diversity and overall bacterial composition reach levels comparable to those in adults by the age of 2 years. IMPORTANCE Evaluating the development of oral microbiota during infancy is important for understanding the subsequent colonization of bacterial species and the process of formation of mature microbiota in the oral cavity. We examined tongue microbiota longitudinally collected from 8 infants and found that drastic compositional shifts in tongue microbiota occur before the age of 1 year, and then bacterial diversity and overall bacterial composition reach levels comparable to those in adults by the age of 2 years. These results may be helpful for preventing the development of various diseases associated with oral microbiota throughout life.
format article
author Shinya Kageyama
Mikari Asakawa
Toru Takeshita
Yukari Ihara
Shunsuke Kanno
Toshiro Hara
Ichiro Takahashi
Yoshihisa Yamashita
author_facet Shinya Kageyama
Mikari Asakawa
Toru Takeshita
Yukari Ihara
Shunsuke Kanno
Toshiro Hara
Ichiro Takahashi
Yoshihisa Yamashita
author_sort Shinya Kageyama
title Transition of Bacterial Diversity and Composition in Tongue Microbiota during the First Two Years of Life
title_short Transition of Bacterial Diversity and Composition in Tongue Microbiota during the First Two Years of Life
title_full Transition of Bacterial Diversity and Composition in Tongue Microbiota during the First Two Years of Life
title_fullStr Transition of Bacterial Diversity and Composition in Tongue Microbiota during the First Two Years of Life
title_full_unstemmed Transition of Bacterial Diversity and Composition in Tongue Microbiota during the First Two Years of Life
title_sort transition of bacterial diversity and composition in tongue microbiota during the first two years of life
publisher American Society for Microbiology
publishDate 2019
url https://doaj.org/article/a58555be762f402c88830ad5c7b705b8
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