Association between the oral microbiome and brain resting state connectivity in smokers
Recent studies have shown a critical role of the gastrointestinal microbiome in brain and behavior via the complex gut–microbiome–brain axis. However, the influence of the oral microbiome in neurological processes is much less studied, especially in response to the stimuli, such as smoking, within t...
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Published in | NeuroImage (Orlando, Fla.) Vol. 200; pp. 121 - 131 |
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Main Authors | , , , , , , , , |
Format | Journal Article |
Language | English |
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United States
Elsevier Inc
15.10.2019
Elsevier Limited |
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Abstract | Recent studies have shown a critical role of the gastrointestinal microbiome in brain and behavior via the complex gut–microbiome–brain axis. However, the influence of the oral microbiome in neurological processes is much less studied, especially in response to the stimuli, such as smoking, within the oral microenvironment. Additionally, given the complex structural and functional networks in brain, our knowledge about the relationship between microbiome and brain function through specific brain circuits is still very limited. In this pilot study, we leveraged next generation sequencing for microbiome and functional neuroimaging technique to enable the delineation of microbiome-brain network links as well as their relationship to cigarette smoking. Thirty smokers and 30 age- and sex-matched nonsmokers were recruited for 16S sequencing of their oral microbial community. Among them, 56 subjects were scanned by resting-state functional magnetic resonance imaging to derive brain functional networks. Statistical analyses were performed to demonstrate the influence of smoking on the oral microbial composition, functional network connectivity, and the associations between microbial shifts and functional network connectivity alternations. Compared to nonsmokers, we found a significant decrease of beta diversity (P = 6 × 10−3) in smokers and identified several classes (Betaproteobacteria, Spirochaetia, Synergistia, and Mollicutes) with significant alterations in microbial abundance. Pathway analysis on the predicted KEGG pathways shows that the microbiota with altered abundance are mainly involved in pathways related to cell processes, DNA repair, immune system, and neurotransmitters signaling. One brain functional network connectivity component was identified to have a significant difference between smokers and nonsmokers (P = 0.032), mainly including connectivity between brain default network and other task-positive networks. This brain functional component was also significantly associated with smoking related microbiota, suggesting a correlated cross-individual pattern between smoking-induced oral microbiome dysbiosis and brain functional connectivity alternation, possibly involving immunological and neurotransmitter signaling pathways. This work is the first attempt to link oral microbiome and brain functional networks, and provides support for future work in characterizing the role of oral microbiome in mediating smoking effects on brain activity.
•Link the microbiome-brain network in relation to smoking.•Decreased beta diversity, abundance changes in taxa and pathways by smoking.•Alternations of connectivity between DMN and task-positive networks in smokers.•Oral microbiome-brain association involving immune and neurotransmitter pathways. |
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AbstractList | Recent studies have shown a critical role of the gastrointestinal microbiome in brain and behavior via the complex gut–microbiome–brain axis. However, the influence of the oral microbiome in neurological processes is much less studied, especially in response to the stimuli, such as smoking, within the oral microenvironment. Additionally, given the complex structural and functional networks in brain, our knowledge about the relationship between microbiome and brain function through specific brain circuits is still very limited. In this pilot study, we leveraged next generation sequencing for microbiome and functional neuroimaging technique to enable the delineation of microbiome-brain network links as well as their relationship to cigarette smoking. Thirty smokers and 30 age- and sex-matched nonsmokers were recruited for 16S sequencing of their oral microbial community. Among them, 56 subjects were scanned by resting-state functional magnetic resonance imaging to derive brain functional networks. Statistical analyses were performed to demonstrate the influence of smoking on the oral microbial composition, functional network connectivity, and the associations between microbial shifts and functional network connectivity alternations. Compared to nonsmokers, we found a significant decrease of beta diversity (P = 6 × 10−3) in smokers and identified several classes (Betaproteobacteria, Spirochaetia, Synergistia, and Mollicutes) with significant alterations in microbial abundance. Pathway analysis on the predicted KEGG pathways shows that the microbiota with altered abundance are mainly involved in pathways related to cell processes, DNA repair, immune system, and neurotransmitters signaling. One brain functional network connectivity component was identified to have a significant difference between smokers and nonsmokers (P = 0.032), mainly including connectivity between brain default network and other task-positive networks. This brain functional component was also significantly associated with smoking related microbiota, suggesting a correlated cross-individual pattern between smoking-induced oral microbiome dysbiosis and brain functional connectivity alternation, possibly involving immunological and neurotransmitter signaling pathways. This work is the first attempt to link oral microbiome and brain functional networks, and provides support for future work in characterizing the role of oral microbiome in mediating smoking effects on brain activity. Recent studies have shown a critical role of the gastrointestinal microbiome in brain and behavior via the complex gut–microbiome–brain axis. However, the influence of the oral microbiome in neurological processes is much less studied, especially in response to the stimuli, such as smoking, within the oral microenvironment. Additionally, given the complex structural and functional networks in brain, our knowledge about the relationship between microbiome and brain function through specific brain circuits is still very limited. In this pilot study, we leveraged next generation sequencing for microbiome and functional neuroimaging technique to enable the delineation of microbiome-brain network links as well as their relationship to cigarette smoking. Thirty smokers and 30 age- and sex-matched nonsmokers were recruited for 16S sequencing of their oral microbial community. Among them, 56 subjects were scanned by resting-state functional magnetic resonance imaging to derive brain functional networks. Statistical analyses were performed to demonstrate the influence of smoking on the oral microbial composition, functional network connectivity, and the associations between microbial shifts and functional network connectivity alternations. Compared to nonsmokers, we found a significant decrease of beta diversity (P = 6 × 10−3) in smokers and identified several classes (Betaproteobacteria, Spirochaetia, Synergistia, and Mollicutes) with significant alterations in microbial abundance. Pathway analysis on the predicted KEGG pathways shows that the microbiota with altered abundance are mainly involved in pathways related to cell processes, DNA repair, immune system, and neurotransmitters signaling. One brain functional network connectivity component was identified to have a significant difference between smokers and nonsmokers (P = 0.032), mainly including connectivity between brain default network and other task-positive networks. This brain functional component was also significantly associated with smoking related microbiota, suggesting a correlated cross-individual pattern between smoking-induced oral microbiome dysbiosis and brain functional connectivity alternation, possibly involving immunological and neurotransmitter signaling pathways. This work is the first attempt to link oral microbiome and brain functional networks, and provides support for future work in characterizing the role of oral microbiome in mediating smoking effects on brain activity. •Link the microbiome-brain network in relation to smoking.•Decreased beta diversity, abundance changes in taxa and pathways by smoking.•Alternations of connectivity between DMN and task-positive networks in smokers.•Oral microbiome-brain association involving immune and neurotransmitter pathways. Recent studies have shown a critical role of the gastrointestinal microbiome in brain and behavior via the complex gut-microbiome-brain axis. However, the influence of the oral microbiome in neurological processes is much less studied, especially in response to the stimuli, such as smoking, within the oral microenvironment. Additionally, given the complex structural and functional networks in brain, our knowledge about the relationship between microbiome and brain function through specific brain circuits is still very limited. In this pilot study, we leveraged next generation sequencing for microbiome and functional neuroimaging technique to enable the delineation of microbiome-brain network links as well as their relationship to cigarette smoking. Thirty smokers and 30 age- and sex-matched nonsmokers were recruited for 16S sequencing of their oral microbial community. Among them, 56 subjects were scanned by resting-state functional magnetic resonance imaging to derive brain functional networks. Statistical analyses were performed to demonstrate the influence of smoking on the oral microbial composition, functional network connectivity, and the associations between microbial shifts and functional network connectivity alternations. Compared to nonsmokers, we found a significant decrease of beta diversity (P = 6 × 10 ) in smokers and identified several classes (Betaproteobacteria, Spirochaetia, Synergistia, and Mollicutes) with significant alterations in microbial abundance. Pathway analysis on the predicted KEGG pathways shows that the microbiota with altered abundance are mainly involved in pathways related to cell processes, DNA repair, immune system, and neurotransmitters signaling. One brain functional network connectivity component was identified to have a significant difference between smokers and nonsmokers (P = 0.032), mainly including connectivity between brain default network and other task-positive networks. This brain functional component was also significantly associated with smoking related microbiota, suggesting a correlated cross-individual pattern between smoking-induced oral microbiome dysbiosis and brain functional connectivity alternation, possibly involving immunological and neurotransmitter signaling pathways. This work is the first attempt to link oral microbiome and brain functional networks, and provides support for future work in characterizing the role of oral microbiome in mediating smoking effects on brain activity. Recent studies have shown a critical role of the gastrointestinal microbiome in brain and behavior via the complex gut–microbiome–brain axis. However, the influence of the oral microbiome in neurological processes is much less studied, especially in response to the stimuli, such as smoking, within the oral microenvironment. Additionally, given the complex structural and functional networks in brain, our knowledge about the relationship between microbiome and brain function through specific brain circuits is still very limited. In this pilot study, we leveraged next generation sequencing for microbiome and functional neuroimaging technique to enable the delineation of microbiome-brain network links as well as their relationship to cigarette smoking. Thirty smokers and 30 age- and sex-matched nonsmokers were recruited for 16S sequencing of their oral microbial community. Among them, 56 subjects were scanned by resting-state functional magnetic resonance imaging to derive brain functional networks. Statistical analyses were performed to demonstrate the influence of smoking on the oral microbial composition, functional network connectivity, and the associations between microbial shifts and functional network connectivity alternations. Compared to nonsmokers, we found a significant decrease of beta diversity (P = 6 × 10 −3 ) in smokers and identified several classes (Betaproteobacteria, Spirochaetia, Synergistia, and Mollicutes) with significant alterations in microbial abundance. Pathway analysis on the predicted KEGG pathways shows that the microbiota with altered abundance are mainly involved in pathways related to cell processes, DNA repair, immune system, and neurotransmitters signaling. One brain functional network connectivity component was identified to have a significant difference between smokers and nonsmokers (P = 0.032), mainly including connectivity between brain default network and other task-positive networks. This brain functional component was also significantly associated with smoking related microbiota, suggesting a correlated cross-individual pattern between smoking-induced oral microbiome dysbiosis and brain functional connectivity alternation, possibly involving immunological and neurotransmitter signaling pathways. This work is the first attempt to link oral microbiome and brain functional networks, and provides support for future work in characterizing the role of oral microbiome in mediating smoking effects on brain activity. Recent studies have shown a critical role of the gastrointestinal microbiome in brain and behavior via the complex gut-microbiome-brain axis. However, the influence of the oral microbiome in neurological processes is much less studied, especially in response to the stimuli, such as smoking, within the oral microenvironment. Additionally, given the complex structural and functional networks in brain, our knowledge about the relationship between microbiome and brain function through specific brain circuits is still very limited. In this pilot study, we leveraged next generation sequencing for microbiome and functional neuroimaging technique to enable the delineation of microbiome-brain network links as well as their relationship to cigarette smoking. Thirty smokers and 30 age- and sex-matched nonsmokers were recruited for 16S sequencing of their oral microbial community. Among them, 56 subjects were scanned by resting-state functional magnetic resonance imaging to derive brain functional networks. Statistical analyses were performed to demonstrate the influence of smoking on the oral microbial composition, functional network connectivity, and the associations between microbial shifts and functional network connectivity alternations. Compared to nonsmokers, we found a significant decrease of beta diversity (P = 6 × 10-3) in smokers and identified several classes (Betaproteobacteria, Spirochaetia, Synergistia, and Mollicutes) with significant alterations in microbial abundance. Pathway analysis on the predicted KEGG pathways shows that the microbiota with altered abundance are mainly involved in pathways related to cell processes, DNA repair, immune system, and neurotransmitters signaling. One brain functional network connectivity component was identified to have a significant difference between smokers and nonsmokers (P = 0.032), mainly including connectivity between brain default network and other task-positive networks. This brain functional component was also significantly associated with smoking related microbiota, suggesting a correlated cross-individual pattern between smoking-induced oral microbiome dysbiosis and brain functional connectivity alternation, possibly involving immunological and neurotransmitter signaling pathways. This work is the first attempt to link oral microbiome and brain functional networks, and provides support for future work in characterizing the role of oral microbiome in mediating smoking effects on brain activity.Recent studies have shown a critical role of the gastrointestinal microbiome in brain and behavior via the complex gut-microbiome-brain axis. However, the influence of the oral microbiome in neurological processes is much less studied, especially in response to the stimuli, such as smoking, within the oral microenvironment. Additionally, given the complex structural and functional networks in brain, our knowledge about the relationship between microbiome and brain function through specific brain circuits is still very limited. In this pilot study, we leveraged next generation sequencing for microbiome and functional neuroimaging technique to enable the delineation of microbiome-brain network links as well as their relationship to cigarette smoking. Thirty smokers and 30 age- and sex-matched nonsmokers were recruited for 16S sequencing of their oral microbial community. Among them, 56 subjects were scanned by resting-state functional magnetic resonance imaging to derive brain functional networks. Statistical analyses were performed to demonstrate the influence of smoking on the oral microbial composition, functional network connectivity, and the associations between microbial shifts and functional network connectivity alternations. Compared to nonsmokers, we found a significant decrease of beta diversity (P = 6 × 10-3) in smokers and identified several classes (Betaproteobacteria, Spirochaetia, Synergistia, and Mollicutes) with significant alterations in microbial abundance. Pathway analysis on the predicted KEGG pathways shows that the microbiota with altered abundance are mainly involved in pathways related to cell processes, DNA repair, immune system, and neurotransmitters signaling. One brain functional network connectivity component was identified to have a significant difference between smokers and nonsmokers (P = 0.032), mainly including connectivity between brain default network and other task-positive networks. This brain functional component was also significantly associated with smoking related microbiota, suggesting a correlated cross-individual pattern between smoking-induced oral microbiome dysbiosis and brain functional connectivity alternation, possibly involving immunological and neurotransmitter signaling pathways. This work is the first attempt to link oral microbiome and brain functional networks, and provides support for future work in characterizing the role of oral microbiome in mediating smoking effects on brain activity. |
Author | Hutchison, Kent E. Portillo, Salvador Lin, Dongdong Liu, Jingyu Vegara, Victor Carroll-Portillo, Amanda Krauter, Kenneth S. Ellingson, Jarrod M. Calhoun, Vince D. |
AuthorAffiliation | c Molecular,Cellular,and Developmental Biology, University of Colorado Boulder, Boulder, 80309, USA d University of New Mexico, Department of Electrical and Computer Engineering, Albuquerque, NM, 87106, USA a The Mind Research Network, Albuquerque, NM, 87106, USA e Tri-institutional Center for Translational Research in Neuroimaging and Data Science (TReNDS) [Georgia State University, Georgia Institute of Technology, Emory University], Atlanta, GA, 30303, USA b Department of Psychology and Neuroscience, University of Colorado Boulder, Boulder, 80309, USA |
AuthorAffiliation_xml | – name: c Molecular,Cellular,and Developmental Biology, University of Colorado Boulder, Boulder, 80309, USA – name: a The Mind Research Network, Albuquerque, NM, 87106, USA – name: d University of New Mexico, Department of Electrical and Computer Engineering, Albuquerque, NM, 87106, USA – name: e Tri-institutional Center for Translational Research in Neuroimaging and Data Science (TReNDS) [Georgia State University, Georgia Institute of Technology, Emory University], Atlanta, GA, 30303, USA – name: b Department of Psychology and Neuroscience, University of Colorado Boulder, Boulder, 80309, USA |
Author_xml | – sequence: 1 givenname: Dongdong surname: Lin fullname: Lin, Dongdong email: dlin@mrn.org organization: The Mind Research Network, Albuquerque, NM, 87106, USA – sequence: 2 givenname: Kent E. surname: Hutchison fullname: Hutchison, Kent E. organization: Department of Psychology and Neuroscience, University of Colorado Boulder, Boulder, 80309, USA – sequence: 3 givenname: Salvador surname: Portillo fullname: Portillo, Salvador organization: University of New Mexico, Department of Electrical and Computer Engineering, Albuquerque, NM, 87106, USA – sequence: 4 givenname: Victor surname: Vegara fullname: Vegara, Victor organization: The Mind Research Network, Albuquerque, NM, 87106, USA – sequence: 5 givenname: Jarrod M. surname: Ellingson fullname: Ellingson, Jarrod M. organization: Department of Psychology and Neuroscience, University of Colorado Boulder, Boulder, 80309, USA – sequence: 6 givenname: Jingyu surname: Liu fullname: Liu, Jingyu organization: The Mind Research Network, Albuquerque, NM, 87106, USA – sequence: 7 givenname: Kenneth S. surname: Krauter fullname: Krauter, Kenneth S. organization: Molecular,Cellular,and Developmental Biology, University of Colorado Boulder, Boulder, 80309, USA – sequence: 8 givenname: Amanda surname: Carroll-Portillo fullname: Carroll-Portillo, Amanda organization: University of New Mexico, Department of Electrical and Computer Engineering, Albuquerque, NM, 87106, USA – sequence: 9 givenname: Vince D. surname: Calhoun fullname: Calhoun, Vince D. organization: The Mind Research Network, Albuquerque, NM, 87106, USA |
BackLink | https://www.ncbi.nlm.nih.gov/pubmed/31201984$$D View this record in MEDLINE/PubMed |
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Keywords | Neuroimaging Functional connectivity Saliva Microbiome Smoking |
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Snippet | Recent studies have shown a critical role of the gastrointestinal microbiome in brain and behavior via the complex gut–microbiome–brain axis. However, the... Recent studies have shown a critical role of the gastrointestinal microbiome in brain and behavior via the complex gut-microbiome-brain axis. However, the... |
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SubjectTerms | Adult Alzheimer's disease Animal cognition Antibiotics Bacteria Brain mapping Cerebral Cortex - diagnostic imaging Cerebral Cortex - immunology Cerebral Cortex - physiopathology Cigarette smoking Cognitive ability Connectome DNA repair Dysbacteriosis Dysbiosis - etiology Dysbiosis - microbiology Ecosystems Female Functional connectivity Functional magnetic resonance imaging Humans Immune system Information processing Intestinal microflora Magnetic Resonance Imaging Male Microbiome Microbiomes Microbiota Microbiota - physiology Middle Aged Mouth - microbiology Nerve Net - diagnostic imaging Nerve Net - immunology Nerve Net - physiopathology Neural networks Neurodegeneration Neurogenesis Neuroimaging Neurotransmitters Next-generation sequencing Nicotine Oral hygiene Pilot Projects Saliva Saliva - microbiology Signal transduction Signal Transduction - immunology Signal Transduction - physiology Smoking Smoking - adverse effects Smoking - physiopathology Statistical analysis Structure-function relationships Young Adult |
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Title | Association between the oral microbiome and brain resting state connectivity in smokers |
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