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Article

Early-Life Adversity Leaves Its Imprint on the Oral Microbiome for More Than 20 Years and Is Associated with Long-Term Immune Changes

by
Eleftheria G. Charalambous
1,2,
Sophie B. Mériaux
1,
Pauline Guebels
1,
Claude P. Muller
1,
Fleur A. D. Leenen
1,
Martha M. C. Elwenspoek
1,
Ines Thiele
3,4,5,6,
Johannes Hertel
3,7 and
Jonathan D. Turner
1,*
1
Immune Endocrine and Epigenetics Research Group, Department of Infection and Immunity, Luxembourg Institute of Health (LIH), 29 Rue Henri Koch, L-4354 Esch-sur-Alzette, Luxembourg
2
Faculty of Science, Technology and Medicine, University of Luxembourg, 2 Avenue de Université, L-4365 Esch-sur-Alzette, Luxembourg
3
School of Medicine, National University of Ireland, H91 YR71 Galway, Ireland
4
Ryan Institute, National University of Galway, H91 TK33 Galway, Ireland
5
Division of Microbiology, National University of Galway, H91 TK33 Galway, Ireland
6
APC Microbiome Ireland, T12 HW58 Cork, Ireland
7
Department of Psychiatry and Psychotherapy, University Medicine Greifswald, 17489 Greifswald, Germany
*
Author to whom correspondence should be addressed.
Int. J. Mol. Sci. 2021, 22(23), 12682; https://doi.org/10.3390/ijms222312682
Submission received: 27 October 2021 / Revised: 19 November 2021 / Accepted: 22 November 2021 / Published: 24 November 2021
(This article belongs to the Special Issue The Interplay of Microbiome and Immune Response in Health and Diseases-2nd Edition)
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Abstract

The early-life microbiome (ELM) interacts with the psychosocial environment, in particular during early-life adversity (ELA), defining life-long health trajectories. The ELM also plays a significant role in the maturation of the immune system. We hypothesised that, in this context, the resilience of the oral microbiomes, despite being composed of diverse and distinct communities, allows them to retain an imprint of the early environment. Using 16S amplicon sequencing on the EpiPath cohort, we demonstrate that ELA leaves an imprint on both the salivary and buccal oral microbiome 24 years after exposure to adversity. Furthermore, the changes in both communities were associated with increased activation, maturation, and senescence of both innate and adaptive immune cells, although the interaction was partly dependent on prior herpesviridae exposure and current smoking. Our data suggest the presence of multiple links between ELA, Immunosenescence, and cytotoxicity that occur through long-term changes in the microbiome.
Keywords: early-life adversity; early experience; microbiome; bacterial community; oral microbiome; developmental origins of health and disease; immune system; host-microbe interactions early-life adversity; early experience; microbiome; bacterial community; oral microbiome; developmental origins of health and disease; immune system; host-microbe interactions

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MDPI and ACS Style

Charalambous, E.G.; Mériaux, S.B.; Guebels, P.; Muller, C.P.; Leenen, F.A.D.; Elwenspoek, M.M.C.; Thiele, I.; Hertel, J.; Turner, J.D. Early-Life Adversity Leaves Its Imprint on the Oral Microbiome for More Than 20 Years and Is Associated with Long-Term Immune Changes. Int. J. Mol. Sci. 2021, 22, 12682. https://doi.org/10.3390/ijms222312682

AMA Style

Charalambous EG, Mériaux SB, Guebels P, Muller CP, Leenen FAD, Elwenspoek MMC, Thiele I, Hertel J, Turner JD. Early-Life Adversity Leaves Its Imprint on the Oral Microbiome for More Than 20 Years and Is Associated with Long-Term Immune Changes. International Journal of Molecular Sciences. 2021; 22(23):12682. https://doi.org/10.3390/ijms222312682

Chicago/Turabian Style

Charalambous, Eleftheria G., Sophie B. Mériaux, Pauline Guebels, Claude P. Muller, Fleur A. D. Leenen, Martha M. C. Elwenspoek, Ines Thiele, Johannes Hertel, and Jonathan D. Turner. 2021. "Early-Life Adversity Leaves Its Imprint on the Oral Microbiome for More Than 20 Years and Is Associated with Long-Term Immune Changes" International Journal of Molecular Sciences 22, no. 23: 12682. https://doi.org/10.3390/ijms222312682

APA Style

Charalambous, E. G., Mériaux, S. B., Guebels, P., Muller, C. P., Leenen, F. A. D., Elwenspoek, M. M. C., Thiele, I., Hertel, J., & Turner, J. D. (2021). Early-Life Adversity Leaves Its Imprint on the Oral Microbiome for More Than 20 Years and Is Associated with Long-Term Immune Changes. International Journal of Molecular Sciences, 22(23), 12682. https://doi.org/10.3390/ijms222312682

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