Transgenerational effects of early life stress on the fecal microbiota in mice.
Journal
Communications biology
ISSN: 2399-3642
Titre abrégé: Commun Biol
Pays: England
ID NLM: 101719179
Informations de publication
Date de publication:
31 May 2024
31 May 2024
Historique:
received:
09
11
2023
accepted:
02
05
2024
medline:
1
6
2024
pubmed:
1
6
2024
entrez:
31
5
2024
Statut:
epublish
Résumé
Stress in early life can affect the progeny and increase the risk to develop psychiatric and cardiometabolic diseases across generations. The cross-generational effects of early life stress have been modeled in mice and demonstrated to be associated with epigenetic factors in the germline. While stress is known to affect gut microbial features, whether its effects can persist across life and be passed to the progeny is not well defined. Here we show that early postnatal stress in mice shifts the fecal microbial composition (binary Jaccard index) throughout life, including abundance of eight amplicon sequencing variants (ASVs). Further effects on fecal microbial composition, structure (weighted Jaccard index), and abundance of 16 ASVs are detected in the progeny across two generations. These effects are not accompanied by changes in bacterial metabolites in any generation. These results suggest that changes in the fecal microbial community induced by early life traumatic stress can be perpetuated from exposed parent to the offspring.
Identifiants
pubmed: 38822061
doi: 10.1038/s42003-024-06279-2
pii: 10.1038/s42003-024-06279-2
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
670Subventions
Organisme : Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung (Swiss National Science Foundation)
ID : 31003A_175742/1
Organisme : Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung (Swiss National Science Foundation)
ID : 182880/Phase 2
Organisme : Eidgenössische Technische Hochschule Zürich (Federal Institute of Technology Zurich)
ID : ETH-10 15-2
Organisme : Eidgenössische Technische Hochschule Zürich (Federal Institute of Technology Zurich)
ID : ETH-17 13-2
Organisme : EC | Horizon 2020 Framework Programme (EU Framework Programme for Research and Innovation H2020)
ID : 848158
Informations de copyright
© 2024. The Author(s).
Références
Nelson, C. A., Zeanah, C. H. & Fox, N. A. How early experience shapes human development: the case of psychosocial deprivation. Neural. Plast. 2019, 1–12 (2019).
doi: 10.1155/2019/1676285
Ratsika, A., Codagnone, M. C., O’Mahony, S., Stanton, C. & Cryan, J. F. Priming for life: early life nutrition and the microbiota-gut-brain axis. Nutrients 13, 423 (2021).
pubmed: 33525617
pmcid: 7912058
doi: 10.3390/nu13020423
Gershon, A., Sudheimer, K., Tirouvanziam, R., Williams, L. M. & O’Hara, R. The long-term impact of early adversity on late-life psychiatric disorders. Curr. Psychiatry Rep. 15, 352 (2013).
pubmed: 23443532
doi: 10.1007/s11920-013-0352-9
McEwen, B. S. Understanding the potency of stressful early life experiences on brain and body function. Metabolism 57, 11–15 (2008).
doi: 10.1016/j.metabol.2008.07.006
Bowers, M. E. & Yehuda, R. Intergenerational transmission of stress in humans. Neuropsychopharmacology 41, 232–244 (2016).
pubmed: 26279078
doi: 10.1038/npp.2015.247
Jawaid, A., Jehle, K.-L. & Mansuy, I. M. Impact of parental exposure on offspring health in humans. Trends Genet. 37, 373–388 (2021).
pubmed: 33189388
doi: 10.1016/j.tig.2020.10.006
Weaver, I. C. G. et al. Epigenetic programming by maternal behavior. Nat. Neurosci. 7, 847–854 (2004).
pubmed: 15220929
doi: 10.1038/nn1276
Boscardin, C., Manuella, F. & Mansuy, I. M. Paternal transmission of behavioural and metabolic traits induced by postnatal stress to the 5th generation in mice. Environ. Epigenet. 8, dvac024 (2022).
pubmed: 36518875
pmcid: 9730319
doi: 10.1093/eep/dvac024
van Steenwyk, G., Roszkowski, M., Manuella, F., Franklin, T. B. & Mansuy, I. M. Transgenerational inheritance of behavioral and metabolic effects of paternal exposure to traumatic stress in early postnatal life: evidence in the 4th generation. Environ. Epigenet 4, dvy023 (2018).
pubmed: 30349741
pmcid: 6190267
Zhou, A. & Ryan, J. Biological embedding of early-life adversity and a scoping review of the evidence for intergenerational epigenetic transmission of stress and trauma in humans. Genes 14, 1639 (2023).
pubmed: 37628690
pmcid: 10454883
doi: 10.3390/genes14081639
Querdasi, F. R. et al. Multigenerational adversity impacts on human gut microbiome composition and socioemotional functioning in early childhood. PNAS 120, e2213768120 (2023).
pubmed: 37463211
pmcid: 10372691
doi: 10.1073/pnas.2213768120
Clarke, G., O’Mahony, S. M., Dinan, T. G. & Cryan, J. F. Priming for health: gut microbiota acquired in early life regulates physiology, brain and behaviour. Acta Paediatr. 103, 812–819 (2014).
pubmed: 24798884
doi: 10.1111/apa.12674
O’Riordan, K. J. et al. Short chain fatty acids: Microbial metabolites for gut-brain axis signalling. Mol. Cell Endocrinol. 546, 111572 (2022).
pubmed: 35066114
doi: 10.1016/j.mce.2022.111572
Mazzoli, R. & Pessione, E. The neuro-endocrinological role of microbial glutamate and GABA signaling. Front. Microbiol 7, 1–17 (2016).
doi: 10.3389/fmicb.2016.01934
Jena, A. et al. Gut-brain axis in the early postnatal years of life: a developmental perspective. Front. Integr. Neurosci. 14, 1–18 (2020).
doi: 10.3389/fnint.2020.00044
De Palma, G. et al. Microbiota and host determinants of behavioural phenotype in maternally separated mice. Nat. Commun. 6, 7735 (2015).
pubmed: 26218677
doi: 10.1038/ncomms8735
Hantsoo, L. & Zemel, B. S. Stress gets into the belly: Early life stress and the gut microbiome. Behav. Brain Res. 414, 113474 (2021).
pubmed: 34280457
pmcid: 8380711
doi: 10.1016/j.bbr.2021.113474
Kemp, K. M., Colson, J., Lorenz, R. G., Maynard, C. L. & Pollock, J. S. Early life stress in mice alters gut microbiota independent of maternal microbiota inheritance. Am. J. Physiol. Integr. Comp. Physiol. 320, R663–R674 (2021).
doi: 10.1152/ajpregu.00072.2020
Coley, E. J. L. et al. Early life adversity predicts brain-gut alterations associated with increased stress and mood. Neurobiol. Stress 15, 100348 (2021).
pubmed: 34113697
pmcid: 8170500
doi: 10.1016/j.ynstr.2021.100348
Callaghan, B. L. et al. Mind and gut: associations between mood and gastrointestinal distress in children exposed to adversity. Dev. Psychopathol. 32, 309–328 (2020).
pubmed: 30919798
doi: 10.1017/S0954579419000087
Flannery, J. E. et al. Gut feelings begin in childhood: the gut metagenome correlates with early environment, caregiving, and behavior. mBio 11, e02780–19 (2020).
pubmed: 31964729
pmcid: 6974564
doi: 10.1128/mBio.02780-19
Franklin, T. B. et al. Epigenetic transmission of the impact of early stress across generations. Biol. Psychiatry 68, 408–415 (2010).
pubmed: 20673872
doi: 10.1016/j.biopsych.2010.05.036
van Steenwyk, G. et al. Involvement of circulating factors in the transmission of paternal experiences through the germline. EMBO J. 39, e104579 (2020).
pubmed: 33034389
pmcid: 7705452
doi: 10.15252/embj.2020104579
Gapp, K. et al. Alterations in sperm long RNA contribute to the epigenetic inheritance of the effects of postnatal trauma. Mol. Psychiatry 25, 2162–2174 (2020).
pubmed: 30374190
doi: 10.1038/s41380-018-0271-6
Gapp, K. et al. Implication of sperm RNAs in transgenerational inheritance of the effects of early trauma in mice. Nat. Neurosci. 17, 667–669 (2014).
pubmed: 24728267
pmcid: 4333222
doi: 10.1038/nn.3695
Moloney, R. D. et al. Early-life stress induces visceral hypersensitivity in mice. Neurosci. Lett. 512, 99–102 (2012).
pubmed: 22326388
doi: 10.1016/j.neulet.2012.01.066
Skillington, O. et al. The contrasting human gut microbiota in early and late life and implications for host health and disease. Nutr. Healthy Aging 6, 157–178 (2021).
doi: 10.3233/NHA-210129
Salazar, N. et al. Microbiome: effects of ageing and diet. Curr. Issues Mol. Biol. 36, 33–62 (2020).
pubmed: 31558686
doi: 10.21775/cimb.036.033
Bergström, A. et al. Establishment of intestinal microbiota during early life: a longitudinal, explorative study of a large cohort of danish infants. Appl Environ. Microbiol. 80, 2889–2900 (2014).
pubmed: 24584251
pmcid: 3993305
doi: 10.1128/AEM.00342-14
Low, A., Soh, M., Miyake, S. & Seedorf, H. Host age prediction from fecal microbiota composition in male C57BL/6J mice. Microbiol. Spectr. 10, e00735–22 (2022).
pubmed: 35674443
pmcid: 9241839
doi: 10.1128/spectrum.00735-22
Langille, M. G. et al. Microbial shifts in the aging mouse gut. Microbiome 2, 50 (2014).
pubmed: 25520805
pmcid: 4269096
doi: 10.1186/s40168-014-0050-9
You, X., Dadwal, U. C., Lenburg, M. E., Kacena, M. A. & Charles, J. F. Murine gut microbiome meta-analysis reveals alterations in carbohydrate metabolism in response to aging. mSystems 7, e01248–21 (2022).
pubmed: 35400171
pmcid: 9040766
doi: 10.1128/msystems.01248-21
Qu, Q. et al. Effects of heat stress on gut microbiome inrRats. Indian J. Microbiol. 61, 338–347 (2021).
pubmed: 34290462
pmcid: 8263838
doi: 10.1007/s12088-021-00948-0
Zhang, Y. et al. Acute cold water-immersion restraint stress induces intestinal injury and reduces the diversity of gut microbiota in mice. Front. Cell Infect. Microbiol. 11, 706849 (2021).
pubmed: 34722327
pmcid: 8551804
doi: 10.3389/fcimb.2021.706849
Kim, Y.-M. et al. Light-stress influences the composition of the murine gut microbiome, memory function, and plasma metabolome. Front. Mol. Biosci. 6, 108 (2019).
pubmed: 31681796
pmcid: 6813214
doi: 10.3389/fmolb.2019.00108
Bassett, S. A. et al. Metabolome and microbiome profiling of a stress-sensitive rat model of gut-brain axis dysfunction. Sci. Rep. 9, 14026 (2019).
pubmed: 31575902
pmcid: 6773725
doi: 10.1038/s41598-019-50593-3
Rao, J. et al. Fecal microbiota transplantation ameliorates gut microbiota imbalance and intestinal barrier damage in rats with stress‐induced depressive‐like behavior. Eur. J. Neurosci. 53, 3598–3611 (2021).
pubmed: 33742731
doi: 10.1111/ejn.15192
Seewoo, B. J. et al. Changes in the rodent gut microbiome following chronic restraint stress and low-intensity rTMS. Neurobiol. Stress 17, 100430 (2022).
pubmed: 35146078
pmcid: 8819474
doi: 10.1016/j.ynstr.2022.100430
Bridgewater, L. C. et al. Gender-based differences in host behavior and gut microbiota composition in response to high fat diet and stress in a mouse model. Sci. Rep. 7, 10776 (2017).
pubmed: 28883460
pmcid: 5589737
doi: 10.1038/s41598-017-11069-4
Usui, N., Matsuzaki, H. & Shimada, S. Characterization of early life stress-affected gut microbiota. Brain Sci. 11, 913 (2021).
pubmed: 34356147
pmcid: 8306161
doi: 10.3390/brainsci11070913
Reemst, K. et al. The role of the gut microbiota in the effects of early-life stress and dietary fatty acids on later-life central and metabolic outcomes in mice. mSystems 7, e0018022 (2022).
pubmed: 35695433
doi: 10.1128/msystems.00180-22
Louis, P. & Flint, H. J. Formation of propionate and butyrate by the human colonic microbiota. Environ. Microbiol. 19, 29–41 (2017).
pubmed: 27928878
doi: 10.1111/1462-2920.13589
Riba, A. et al. Early life stress in mice is a suitable model for irritable bowel syndrome but does not predispose to colitis nor increase susceptibility to enteric infections. Brain Behav. Immun. 73, 403–415 (2018).
pubmed: 29860025
doi: 10.1016/j.bbi.2018.05.024
Karen, C., Shyu, D. J. H. & Rajan, K. E. Lactobacillus paracasei supplementation prevents early life stress-induced anxiety and depressive-like behavior in maternal separation model-possible involvement of microbiota-gut-brain axis in differential regulation of microRNA124a/132 and glutamate Rec. Front .Neurosci. 15, 719933 (2021).
pubmed: 34531716
pmcid: 8438336
doi: 10.3389/fnins.2021.719933
Enqi, W., Jingzhu, S., Lingpeng, P. & Yaqin, L. Comparison of the gut microbiota disturbance in rat models of irritable bowel syndrome induced by maternal separation and multiple early-life adversity. Front. Cell Infect. Microbiol. 10, 581974 (2021).
pubmed: 33520732
pmcid: 7840688
doi: 10.3389/fcimb.2020.581974
Bidot, W. A., Ericsson, A. C. & Franklin, C. L. Effects of water decontamination methods and bedding material on the gut microbiota. PLoS One 13, e0198305 (2018).
pubmed: 30359379
pmcid: 6201873
doi: 10.1371/journal.pone.0198305
Ericsson, A. C. et al. The influence of caging, bedding, and diet on the composition of the microbiota in different regions of the mouse gut. Sci. Rep. 8, 4065 (2018).
pubmed: 29511208
pmcid: 5840362
doi: 10.1038/s41598-018-21986-7
Franklin, C. L. & Ericsson, A. C. Microbiota and reproducibility of rodent models. Lab Anim. 46, 114–122 (2017).
doi: 10.1038/laban.1222
Nyangahu, D. D. et al. Disruption of maternal gut microbiota during gestation alters offspring microbiota and immunity. Microbiome 6, 124 (2018).
pubmed: 29981583
pmcid: 6035804
doi: 10.1186/s40168-018-0511-7
Francella, C. et al. Microbe–immune–stress interactions impact behaviour during postnatal development. Int. J. Mol. Sci. 23, 15064 (2022).
pubmed: 36499393
pmcid: 9740388
doi: 10.3390/ijms232315064
Li, H. et al. Rifaximin-mediated gut microbiota regulation modulates the function of microglia and protects against CUMS-induced depression-like behaviors in adolescent rat. J. Neuroinflamm. 18, 254 (2021).
doi: 10.1186/s12974-021-02303-y
Kong, Q. et al. The autistic-like behaviors development during weaning and sexual maturation in VPA-induced autistic-like rats is accompanied by gut microbiota dysbiosis. PeerJ 9, e11103 (2021).
pubmed: 33986978
pmcid: 8101471
doi: 10.7717/peerj.11103
Park, H. J., Kim, S. A., Kang, W. S. & Kim, J. W. Early-life stress modulates gut microbiota and peripheral and central inflammation in a sex-dependent manner. Int. J. Mol. Sci. 22, 1899 (2021).
pubmed: 33672958
pmcid: 7918891
doi: 10.3390/ijms22041899
Guida, F. et al. Antibiotic-induced microbiota perturbation causes gut endocannabinoidome changes, hippocampal neuroglial reorganization and depression in mice. Brain Behav. Immun. 67, 230–245 (2018).
pubmed: 28890155
doi: 10.1016/j.bbi.2017.09.001
Smith, B. J. et al. Changes in the gut microbiome and fermentation products concurrent with enhanced longevity in acarbose-treated mice. BMC Microbiol. 19, 130 (2019).
pubmed: 31195972
pmcid: 6567620
doi: 10.1186/s12866-019-1494-7
Moya, A. & Ferrer, M. Functional redundancy-induced stability of gut microbiota subjected to disturbance. Trends Microbiol. 24, 402–413 (2016).
pubmed: 26996765
doi: 10.1016/j.tim.2016.02.002
den Besten, G. et al. The role of short-chain fatty acids in the interplay between diet, gut microbiota, and host energy metabolism. J. Lipid Res. 54, 2325–2340 (2013).
doi: 10.1194/jlr.R036012
van de Wouw, M. et al. The role of the microbiota in acute stress-induced myeloid immune cell trafficking. Brain Behav. Immun. 84, 209–217 (2020).
pubmed: 31812778
doi: 10.1016/j.bbi.2019.12.003
Xu, C., Lee, S. K., Zhang, D. & Frenette, P. S. The gut microbiome regulates psychological-stress-induced inflammation. Immunity 53, 417–428.e4 (2020).
pubmed: 32735844
pmcid: 7461158
doi: 10.1016/j.immuni.2020.06.025
Lkhagva, E. et al. The regional diversity of gut microbiome along the GI tract of male C57BL/6 mice. BMC Microbiol. 21, 44 (2021).
pubmed: 33579191
pmcid: 7881553
doi: 10.1186/s12866-021-02099-0
Galley, J. D. et al. The structures of the colonic mucosa-associated and luminal microbial communities are distinct and differentially affected by a prolonged murine stressor. Gut Microbes 5, 748–760 (2014).
pubmed: 25536463
pmcid: 4615309
doi: 10.4161/19490976.2014.972241
Bohacek, J., von Werdt, S. & Mansuy, I. M. Probing the germline-dependence of epigenetic inheritance using artificial insemination in mice. Environ. Epigenet. 2, dvv015–dvv015 (2016).
pubmed: 29492284
pmcid: 5804514
doi: 10.1093/eep/dvv015
Otaru, N. et al. GABA production by human intestinal Bacteroides spp.: prevalence, regulation, and role in acid stress tolerance. Front. Microbiol. 12, 656895 (2021).
pubmed: 33936013
pmcid: 8082179
doi: 10.3389/fmicb.2021.656895
Constancias, F. & Mahé, F. fconstancias/metabaRpipe: v0.9 (v0.9). Zenodo. https://doi.org/10.5281/zenodo.6423397 (2022).
Didion, J. P., Martin, M. & Collins, F. S. Atropos: specific, sensitive, and speedy trimming of sequencing reads. PeerJ 5, e3720 (2017).
pubmed: 28875074
pmcid: 5581536
doi: 10.7717/peerj.3720
Callahan, B. J. et al. DADA2: high-resolution sample inference from Illumina amplicon data. Nat. Methods 13, 581–583 (2016).
pubmed: 27214047
pmcid: 4927377
doi: 10.1038/nmeth.3869
R. Core Team. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria (2022).
Oksanen, J. et al. vegan: community ecology package. https://CRAN.R-project.org/package=vegan (2020).
Paradis, E. & Schliep, K. ape 5.0: an environment for modern phylogenetics and evolutionary analyses in {R}. Bioinformatics 35, 526–528 (2019).
pubmed: 30016406
doi: 10.1093/bioinformatics/bty633
Andersen, K. S., Kirkegaard, R. H., Karst, S. M. & Albertsen, M. ampvis2: an R package to analyse and visualise 16S rRNA amplicon data. bioRxiv (2018).
McLaren, M. speedyseq: faster implementations of phyloseq functions. https://github.com/mikemc/speedyseq (2021).
Mallick, H. et al. Multivariable association discovery in population-scale meta-omics studies. PLoS Comput. Biol. 17, 1–27 (2021).
doi: 10.1371/journal.pcbi.1009442
Constancias, F. & Sundar, S. fconstancias/DivComAnalyses: v0.9 (v0.9). Zenodo. https://doi.org/10.5281/zenodo.6473394 (2022).
Wickham, H. Ggplot2: Elegant Graphics for Data Analysis. (Springer-Verlag New York, 2016).
Gu, Z., Eils, R. & Schlesner, M. Complex heatmaps reveal patterns and correlations in multidimensional genomic data. Bioinformatics 32, 2847–2849 (2016).
pubmed: 27207943
doi: 10.1093/bioinformatics/btw313