Maternal Gut Dysbiosis Alters Offspring Microbiota and Social Interactions
Abstract
:1. Introduction
2. Materials and Methods
2.1. Ethical Approval Statement
2.2. Mice and Antibiotics Administration
2.3. Test of Sociability and Preference for Social Novelty
2.4. DNA Extraction
2.5. Bioinformatic Analysis
2.6. Data Analysis
3. Results
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Data Availability Statement
Conflicts of Interest
References
- Strzępa, A.; Majewska-Szczepanik, M.; Lobo, F.M.; Wen, L.; Szczepanik, M. Broad spectrum antibiotic enrofloxacin modulates contact sensitivity through gut microbiota in a murine model. J. Allergy Clin. Immunol. 2017, 140, 121–133. [Google Scholar] [CrossRef] [Green Version]
- Dethlefsen, L.; Relman, D.A. Incomplete recovery and individualized responses of the human distal gut microbiota to repeated anti-biotic perturbation. Proc. Natl. Acad. Sci. USA 2011, 108, 4554–4561. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Arentsen, T.; Raith, H.; Qian, Y.; Forssberg, H.; Heijtz, R.D. Host microbiota modulates development of social preference in mice. Microb. Ecol. Health Dis. 2015, 26, 29719. [Google Scholar] [CrossRef]
- Jakobsson, E.H.; Abrahamsson, T.R.; Jenmalm, M.C.; Harris, K.; Quince, C.; Jernberg, C.; Björkstén, B.; Engstrand, L.; Andersson, A.; Filion, K.B.; et al. Decreased gut microbiota diversity, delayed Bacteroidetes colonisation and reduced Th1 responses in infants delivered by Caesarean section. Gut 2014, 63, 559–566. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Nicholson, J.K.; Holmes, E.; Kinross, J.; Burcelin, R.; Gibson, G.; Jia, W.; Pettersson, S. Host-Gut Microbiota Metabolic Interactions. Science 2012, 336, 1262–1267. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Nobel, Y.; Cox, L.; Kirigin, F.F.; Bokulich, N.A.; Yamanishi, S.; Teitler, I.; Chung, J.; Sohn, J.; Barber, C.M.; Goldfarb, D.; et al. Metabolic and metagenomic outcomes from early-life pulsed antibiotic treatment. Nat. Commun. 2015, 6, 7486. [Google Scholar] [CrossRef] [PubMed]
- Minter, M.R.; Hinterleitner, R.; Meisel, M.; Zhang, C.; Leone, V.; Zhang, X.; Oyler-Castrillo, P.; Zhang, X.; Musch, M.W.; Shen, X.; et al. Antibiotic-induced perturbations in microbial diversity during post-natal development alters amyloid pathology in an aged APPSWE/PS1ΔE9 murine model of Alzheimer’s disease. Sci. Rep. 2017, 7, 10411. [Google Scholar] [CrossRef]
- Miyoshi, J.; Bobe, A.M.; Miyoshi, S.; Huang, Y.; Hubert, N.; Delmont, T.O.; Eren, A.M.; Leone, V.; Chang, E.B. Peripartum exposure to antibiotics promotes persistent gut dysbiosis, immune imbalance, and inflammatory bowel disease in genetically prone offspring. Cell Rep. 2017, 20, 87–92. [Google Scholar] [CrossRef] [Green Version]
- Sommer, F.; Bäckhed, F. The gut microbiota—Masters of host development and physiology. Nat. Rev. Microbiol. 2013, 11, 227–238. [Google Scholar] [CrossRef] [PubMed]
- Olson, C.A.; Vuong, H.E.; Yano, J.M.; Liang, Q.Y.; Nusbaum, D.; Hsiao, E.Y. The Gut Microbiota Mediates the Anti-Seizure Effects of the Ketogenic Diet. Cell 2018, 173, 1728–1741.e13. [Google Scholar] [CrossRef] [Green Version]
- Blacher, E.; Bashiardes, S.; Shapiro, H.; Rothschild, D.; Mor, U.; Dori-Bachash, M.; Kleimayer, C.; Moresi, C.; Harnik, Y.; Zur, M.; et al. Potential roles of gut microbiome and me-tabolites in modulating ALS in mice. Nature 2019, 572, 474–480. [Google Scholar] [CrossRef] [PubMed]
- Chu, C.; Murdock, M.H.; Jing, D.; Won, T.H.; Chung, H.; Kressel, A.; Tsaava, T.; Addorisio, M.E.; Putzel, G.G.; Zhou, L.; et al. The microbiota regulate neuronal function and fear extinction learning. Nat. Cell Biol. 2019, 574, 543–548. [Google Scholar] [CrossRef] [PubMed]
- Burberry, A.; Limone, F.; Wells, M.F.; Couto, A.; Smith, K.S.; Keaney, J.; Gillet, G.; Van Gastel, N.; Wang, J.-Y.; Pietilainen, O.; et al. C9orf72 suppresses systemic and neural inflammation induced by gut microbes. Nature 2020, 582, 89–94. [Google Scholar] [CrossRef]
- Dinan, T.G.; Stilling, R.; Stanton, C.; Cryan, J. Collective unconscious: How gut microbes shape human behavior. J. Psychiatr. Res. 2015, 63, 1–9. [Google Scholar] [CrossRef] [Green Version]
- Finegold, S.M.; Dowd, S.E.; Gontcharova, V.; Liu, C.; Henley, K.E.; Wolcott, R.D.; Youn, E.; Summanen, P.H.; Granpeesheh, D.; Dixson, D.; et al. Pyrosequencing study of fecal microflora of autistic and control children. Anaerobe 2010, 16, 444–453. [Google Scholar] [CrossRef] [PubMed]
- Foster, J.A.; Neufeld, K.-A.M. Gut–brain axis: How the microbiome influences anxiety and depression. Trends Neurosci. 2013, 36, 305–312. [Google Scholar] [CrossRef] [PubMed]
- Cryan, J.F.; Dinan, T.G. Mind-altering microorganisms: The impact of the gut microbiota on brain and behaviour. Nat. Rev. Neurosci. 2012, 13, 701–712. [Google Scholar] [CrossRef]
- Mulligan, C.M.; Friedman, E.J. Maternal modifiers of the infant gut microbiota: Metabolic consequences. J. Endocrinol. 2017, 235, R1–R12. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Clapcote, S.J.; Lipina, T.V.; Millar, J.K.; Mackie, S.; Christie, S.; Ogawa, F.; Lerch, J.P.; Trimble, K.; Uchiyama, M.; Sakuraba, Y.; et al. Behavioral Phenotypes of Disc1 Missense Mutations in Mice. Neuron 2007, 54, 387–402. [Google Scholar] [CrossRef] [Green Version]
- Moy, S.S.; Nadler, J.J.; Perez, A.; Barbaro, R.; Johns, J.M.; Magnuson, T.R.; Piven, J.; Crawley, J.N. Sociability and preference for social novelty in five inbred strains: An approach to assess autistic-like behavior in mice. Genes Brain Behav. 2004, 3, 287–302. [Google Scholar] [CrossRef]
- Nadler, J.J.; Moy, S.S.; Dold, G.; Simmons, N.; Perez, A.; Young, N.B.; Barbaro, R.P.; Piven, J.; Magnuson, T.R.; Crawley, J.N. Automated apparatus for quantitation of social approach behaviors in mice. Genes Brain Behav. 2004, 3, 303–314. [Google Scholar] [CrossRef] [PubMed]
- Yang, M.; Silverman, J.L.; Crawley, J.N. Automated Three-Chambered Social Approach Task for Mice. Curr. Protoc. Neurosci. 2011, 56, 1–8. [Google Scholar] [CrossRef] [PubMed]
- Reyon, D.; Tsai, S.Q.; Khayter, C.; Foden, A.J.; Sander, J.D.; Joung, J.K. FLASH assembly of TALENs for high-throughput genome editing. Nat. Biotechnol. 2012, 30, 460–465. [Google Scholar] [CrossRef]
- Caporaso, J.G.; Kuczynski, J.; Stombaugh, J.; Bittinger, K.; Bushman, F.D.; Costello, E.K.; Fierer, N.; Peña, A.G.; Goodrich, J.K.; Gordon, J.I.; et al. QIIME allows analysis of high-throughput community sequencing data. Nat. Methods 2010, 7, 335–336. [Google Scholar] [CrossRef] [Green Version]
- Rognes, T.; Flouri, T.; Nichols, B.; Quince, C.; Mahé, F. VSEARCH: A versatile open source tool for metagenomics. PeerJ 2016, 4, e2584. [Google Scholar] [CrossRef]
- Wong, A.C.-N.; Wang, Q.-P.; Morimoto, J.; Senior, A.M.; Lihoreau, M.; Neely, G.; Simpson, S.J.; Ponton, F. Gut Microbiota Modifies Olfactory-Guided Microbial Preferences and Foraging Decisions in Drosophila. Curr. Biol. 2017, 27, 2397–2404.e4. [Google Scholar] [CrossRef] [PubMed]
- Segata, N.; Izard, J.; Waldron, L.; Gevers, D.; Miropolsk, L.; Wendy, S.G.; Curtis, H. Metagenomic biomarker discovery and explanation. Genome Biol. 2011, 12, 1–18. [Google Scholar] [CrossRef] [Green Version]
- R Core Team. R: A Language and Environment for Statistical Computing; R Foundation for Statistical Computing: Vienna, Austria, 2020; Available online: https://www.R-project.org/ (accessed on 1 April 2021).
- Kohl, K.D.; Stengel, A.; Dearing, M.D. Inoculation of tannin-degrading bacteria into novel hosts increases performance on tannin-rich diets. Environ. Microbiol. 2015, 18, 1720–1729. [Google Scholar] [CrossRef] [PubMed]
- Yi, X.; Guo, J.; Wang, M.; Xue, C.; Ju, M. Inter-trophic Interaction of Gut Microbiota in a Tripartite System. Microb. Ecol. 2021, 81, 1075–1087. [Google Scholar] [CrossRef]
- Dominguez-Bello, M.G.; Costello, E.K.; Contreras, M.; Magris, M.; Hidalgo, G.; Fierer, N.; Knight, R. Delivery mode shapes the acquisition and structure of the initial microbiota across multiple body habitats in newborns. Proc. Natl. Acad. Sci. USA 2010, 107, 11971–11975. [Google Scholar] [CrossRef] [Green Version]
- Geva-Zatorsky, N.; Sefik, E.; Kua, L.; Pasman, L.; Tan, T.G.; Ortiz-Lopez, A.; Yanortsang, T.B.; Yang, L.; Jupp, R.; Mathis, D.; et al. Mining the Human Gut Microbiota for Immunomodulatory Organisms. Cell 2017, 168, 928–943. [Google Scholar] [CrossRef] [Green Version]
- Pannaraj, P.S.; Li, F.; Cerini, C.; Bender, J.M.; Yang, S.; Rollie, A.; Adisetiyo, H.; Zabih, S.; Lincez, P.J.; Bittinger, K.; et al. Association Between Breast Milk Bacterial Communities and Establishment and Development of the Infant Gut Microbiome. JAMA Pediatr. 2017, 171, 647–654. [Google Scholar] [CrossRef] [PubMed]
- Bäckhed, F.; Roswall, J.; Peng, Y.; Feng, Q.; Jia, H.; Kovatcheva-Datchary, P.; Li, Y.; Xia, Y.; Xie, H.; Zhong, H.; et al. Dynamics and Stabilization of the Human Gut Microbiome during the First Year of Life. Cell Host Microbe 2015, 17, 690–703. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Carmen, C.M.; Samuli, R.; Juhani, A.; Erika, I.; Seppo, S. Human gut colonisation may be initiated in Utero by distinct microbial communities in the placenta and amniotic fluid. Sci. Rep. 2016, 6, 23129. [Google Scholar]
- Planer, J.D.; Peng, Y.; Kau, A.L.; Blanton, L.V.; Ndao, I.M.; Tarr, P.I.; Warner, B.B.; Gordon, J.I. Development of the gut microbiota and mucosal IgA responses in twins and gnotobiotic mice. Nat. Cell Biol. 2016, 534, 263–266. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Nuriel-Ohayon, M.; Neuman, H.; Koren, O. Microbial Changes during Pregnancy, Birth, and Infancy. Front. Microbiol. 2016, 7, 1031. [Google Scholar] [CrossRef] [Green Version]
- Desbonnet, L.; Clarke, G.; Shanahan, F.; Dinan, T.G.; Cryan, J.F. Microbiota is essential for social development in the mouse. Mol. Psychiatry 2014, 19, 146–148. [Google Scholar] [CrossRef] [PubMed]
- Nyangahu, D.D.; Lennard, K.S.; Brown, B.; Darby, M.; Wendoh, J.M.; Havyarimana, E.; Smith, P.; Butcher, J.; Stintzi, A.; Mulder, N.J.; et al. Disruption of maternal gut microbiota during gestation alters offspring microbiota and immunity. Microbiome 2018, 6, 1–10. [Google Scholar] [CrossRef] [Green Version]
- Shin, N.-R.; Whon, T.W.; Bae, J.-W. Proteobacteria: Microbial signature of dysbiosis in gut microbiota. Trends Biotechnol. 2015, 33, 496–503. [Google Scholar] [CrossRef]
- Schloss, P.D.; Schubert, A.M.; Zackular, J.; Iverson, K.D.; Young, V.B.; Petrosino, J.F. Stabilization of the murine gut microbiome following weaning. Gut Microbes 2012, 3, 383–393. [Google Scholar] [CrossRef] [PubMed]
- Tamburini, S.; Nan, S.; Han, C.W.; Clemente, J.C. The microbiome in early life: Implications for health outcomes. Nat. Med. 2016, 22, 713–722. [Google Scholar] [CrossRef] [PubMed]
- Ferretti, P.; Pasolli, E.; Tett, A.; Asnicar, F.; Gorfer, V.; Fedi, S.; Armanini, F.; Truong, D.T.; Manara, S.; Zolfo, M.; et al. Mother-to-Infant Microbial Transmission from Different Body Sites Shapes the Developing Infant Gut Microbiome. Cell Host Microbe 2018, 24, 133–145. [Google Scholar] [CrossRef] [PubMed]
- Münger, E.; Montiel-Castro, A.J.; Langhans, W.; Pacheco-López, G. Reciprocal Interactions Between Gut Microbiota and Host Social Behavior. Front. Integr. Neurosci. 2018, 12, 21. [Google Scholar] [CrossRef] [PubMed]
- Buffington, S.A.; Di Prisco, G.V.; Auchtung, T.A.; Ajami, N.J.; Petrosino, J.F.; Costa-Mattioli, M. Microbial reconstitution reverses maternal diet-induced social and synaptic deficits in offspring. Cell 2016, 165, 1762–1775. [Google Scholar] [CrossRef] [Green Version]
- Degroote, S.; Hunting, D.J.; Baccarelli, A.A.; Takser, L. Maternal gut and fetal brain connection: Increased anxiety and reduced social interactions in Wistar rat offspring following peri-conceptional antibiotic exposure. Prog. Neuro-Psychopharmacol. Biol. Psychiatry 2016, 71, 76–82. [Google Scholar] [CrossRef]
- Leclercq, S.; Mian, F.M.; Stanisz, A.M.; Bindels, L.B.; Cambier, E.; Ben-Amram, H.; Koren, O.; Forsythe, P.; Bienenstock, J. Low-dose penicillin in early life induces long-term changes in murine gut microbiota, brain cytokines and behavior. Nat. Commun. 2017, 8, 15062. [Google Scholar] [CrossRef]
- Jiang, T.; Wu, H.; Yang, X.; Li, Y.; Zhang, Z.; Chen, F.; Zhao, L.; Zhang, C. Lactobacillus mucosae strain promoted by a high-fiber diet in genetic obese child alleviates lipid metabolism and modifies gut microbiota in apoe-/-mice on a western diet. Microorganisms 2020, 8, 1225. [Google Scholar] [CrossRef] [PubMed]
- Karaduta, O.; Glazko, G.; Dvanajscak, Z.; Arthur, J.; Mackintosh, S.; Orr, L.; Rahmatallah, Y.; Yeruva, L.; Tacket, A.; Zybailov, B. Resistant starch slows the progression of CKD in the 5/6 nephrectomy mouse model. Physiol. Rep. 2020, 8, e14610. [Google Scholar] [CrossRef] [PubMed]
- Hung, L.Y.; Parathan, P.; Boonma, P.; Wu, Q.; Wang, Y.; Haag, A.; Luna, R.A.; Bornstein, J.C.; Savidge, T.C.; Foong, J.P.P. Antibiotic exposure postweaning disrupts the neurochemistry and function of enteric neurons mediating colonic motor activity. Am. J. Physiol. Liver Physiol. 2020, 318, G1042–G1053. [Google Scholar] [CrossRef] [PubMed]
- Gao, X.; Cao, Q.; Cheng, Y.; Zhao, D.; Wang, Z.; Yang, H.; Wu, Q.; You, L.; Wang, Y.; Lin, Y.; et al. Chronic stress promotes colitis by disturbing the gut microbiota and triggering immune system response. Proc. Natl. Acad. Sci. USA 2018, 115, E2960–E2969. [Google Scholar] [CrossRef] [Green Version]
- Abriouel, H.; Franz, C.M.A.P.; Ben Omar, N.; Galvez, A. Diversity and applications of Bacillus bacteriocins. FEMS Microbiol. Rev. 2011, 35, 201–232. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Chiquette, J.; Allison, M.; Rasmussen, M. Use of Prevotella bryantii 25A and a commercial probiotic during subacute acidosis challenge in midlactation dairy cows. J. Dairy Sci. 2012, 95, 5985–5995. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Dolpady, J.; Sorini, C.; Di Pietro, C.; Cosorich, I.; Ferrarese, R.; Saita, D.; Clementi, M.; Canducci, F.; Falcone, M. Oral probiotic vsl#3 prevents autoimmune diabetes by modulating microbiota and promoting indoleamine 2,3-dioxygenase-enriched tolerogenic intestinal environment. J. Diabetes Res. 2016, 2016, 7569431. [Google Scholar]
- Zhuang, M.; Shang, W.; Ma, Q.; Strappe, P.; Zhou, Z. Abundance of probiotics and butyrate-production microbiome manages consti-pation via short-chain fatty acids production and hormones secretion. Mol. Nutr. Food Res. 2019, 63, 1801187. [Google Scholar] [CrossRef] [PubMed]
- Artwohl, E.J.; Flynn, J.C.; Bunte, R.M.; Angen, O.; Herold, K.C. Outbreak of Pasteurella pneumotropica in a closed colony of STOCK-Cd28(tm1Mak) mice. Contemp. Top. Lab. Anim. Sci. 2000, 39, 39–41. [Google Scholar]
- Garrett, W.S.; Gallini, C.A.; Yatsunenko, T.; Michaud, M.; DuBois, A.; Delaney, M.L.; Punit, S.; Karlsson, M.; Bry, L.; Glickman, J.N.; et al. Enterobacteriaceae Act in Concert with the Gut Microbiota to Induce Spontaneous and Maternally Transmitted Colitis. Cell Host Microbe 2010, 8, 292–300. [Google Scholar] [CrossRef] [Green Version]
- Huffnagle, G.B.; Dickson, R.P.; Lukacs, N.W. The respiratory tract microbiome and lung inflammation: A two-way street. Mucosal Immunol. 2017, 10, 299–306. [Google Scholar] [CrossRef] [Green Version]
- Knoop, K.; McDonald, K.G.; Kulkarni, D.H.; Newberry, R.D. Antibiotics promote inflammation through the translocation of native commensal colonic bacteria. Gut 2016, 65, 1100–1109. [Google Scholar] [CrossRef] [Green Version]
- Singhal, G.; Jaehne, E.J.; Corrigan, F.; Baune, B.T. Cellular and molecular mechanisms of immunomodulation in the brain through environmental enrichment. Front. Cell. Neurosci. 2014, 8, 97. [Google Scholar] [CrossRef] [Green Version]
- Sgritta, M.; Dooling, S.W.; Buffington, S.A.; Momin, E.N.; Francis, M.B.; Britton, R.A.; Costa-Mattioli, M. Mechanisms underlying microbi-al-mediated changes in social behavior in mouse models of autism spectrum disorder. Neuron 2019, 101, 246–259. [Google Scholar] [CrossRef] [Green Version]
- Needham, B.; Tang, W.; Wu, W.-L. Searching for the gut microbial contributing factors to social behavior in rodent models of autism spectrum disorder. Dev. Neurobiol. 2018, 78, 474–499. [Google Scholar] [CrossRef] [PubMed]
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2021 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Zhang, Z.; Xue, C.; Ju, M.; Guo, J.; Wang, M.; Yi, S.; Yi, X. Maternal Gut Dysbiosis Alters Offspring Microbiota and Social Interactions. Microorganisms 2021, 9, 1742. https://doi.org/10.3390/microorganisms9081742
Zhang Z, Xue C, Ju M, Guo J, Wang M, Yi S, Yi X. Maternal Gut Dysbiosis Alters Offspring Microbiota and Social Interactions. Microorganisms. 2021; 9(8):1742. https://doi.org/10.3390/microorganisms9081742
Chicago/Turabian StyleZhang, Zihan, Chao Xue, Mengyao Ju, Jiawei Guo, Minghui Wang, Sijie Yi, and Xianfeng Yi. 2021. "Maternal Gut Dysbiosis Alters Offspring Microbiota and Social Interactions" Microorganisms 9, no. 8: 1742. https://doi.org/10.3390/microorganisms9081742