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Microbiome and Metabolome Variation as Indicator of Social Stress in Female Prairie Voles

Social isolation is detrimental to the health of social mammals inducing neurochemical and hormonal changes related to depression and anxiety, as well as impairments of cardiovascular and immune functioning. Likewise, perceptions of loneliness are increasingly recognized as detrimental to human psyc...

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Autores principales: Nuccio, Daniel A., Normann, Marigny C., Zhou, Haiming, Grippo, Angela J., Singh, Pallavi
Formato: Online Artículo Texto
Lenguaje:English
Publicado: MDPI 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9861106/
https://www.ncbi.nlm.nih.gov/pubmed/36675193
http://dx.doi.org/10.3390/ijms24021677
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author Nuccio, Daniel A.
Normann, Marigny C.
Zhou, Haiming
Grippo, Angela J.
Singh, Pallavi
author_facet Nuccio, Daniel A.
Normann, Marigny C.
Zhou, Haiming
Grippo, Angela J.
Singh, Pallavi
author_sort Nuccio, Daniel A.
collection PubMed
description Social isolation is detrimental to the health of social mammals inducing neurochemical and hormonal changes related to depression and anxiety, as well as impairments of cardiovascular and immune functioning. Likewise, perceptions of loneliness are increasingly recognized as detrimental to human psychological well-being, cognitive functioning, and physical health. Few studies, however, have examined the impact of social isolation on the intestinal microbiome and metabolome. To better understand the impact of social isolation on these systems, intestinal microbiota, and the systemic impact via the gut–brain axis, we employed prairie voles. Physiological stress on female prairie voles (n = 22) either with a same-sex sibling (n = 11) or in isolation (n = 11) for four weeks demonstrated behavioral indicators of increased anxiety and depression in isolated voles (p ≤ 0.01). Bacterial DNA from fecal and colon samples, collected at five time points (T(0–4)), were sequenced for all nine hypervariable regions of the 16S rRNA gene. Microbiome analyses revealed several differences in gut communities of paired and isolated voles with greater differences at T(4). Notably, several taxa associated with host health including Anaerostipes and Lactobacillaceae were more prevalent in paired voles, whereas several taxa associated with known pathogens (e.g., Staphylococcaceae and Enterococcus) or disease were elevated in isolated animals. Similarly, metabolome analyses suggested isolated voles, when compared to paired animals, exhibited differences in metabolites associated with diabetes and colitis. These findings further contribute to our understanding of the harmful effects of social isolation, which cause perturbations in the gut microbiome and serum metabolites.
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spelling pubmed-98611062023-01-22 Microbiome and Metabolome Variation as Indicator of Social Stress in Female Prairie Voles Nuccio, Daniel A. Normann, Marigny C. Zhou, Haiming Grippo, Angela J. Singh, Pallavi Int J Mol Sci Article Social isolation is detrimental to the health of social mammals inducing neurochemical and hormonal changes related to depression and anxiety, as well as impairments of cardiovascular and immune functioning. Likewise, perceptions of loneliness are increasingly recognized as detrimental to human psychological well-being, cognitive functioning, and physical health. Few studies, however, have examined the impact of social isolation on the intestinal microbiome and metabolome. To better understand the impact of social isolation on these systems, intestinal microbiota, and the systemic impact via the gut–brain axis, we employed prairie voles. Physiological stress on female prairie voles (n = 22) either with a same-sex sibling (n = 11) or in isolation (n = 11) for four weeks demonstrated behavioral indicators of increased anxiety and depression in isolated voles (p ≤ 0.01). Bacterial DNA from fecal and colon samples, collected at five time points (T(0–4)), were sequenced for all nine hypervariable regions of the 16S rRNA gene. Microbiome analyses revealed several differences in gut communities of paired and isolated voles with greater differences at T(4). Notably, several taxa associated with host health including Anaerostipes and Lactobacillaceae were more prevalent in paired voles, whereas several taxa associated with known pathogens (e.g., Staphylococcaceae and Enterococcus) or disease were elevated in isolated animals. Similarly, metabolome analyses suggested isolated voles, when compared to paired animals, exhibited differences in metabolites associated with diabetes and colitis. These findings further contribute to our understanding of the harmful effects of social isolation, which cause perturbations in the gut microbiome and serum metabolites. MDPI 2023-01-14 /pmc/articles/PMC9861106/ /pubmed/36675193 http://dx.doi.org/10.3390/ijms24021677 Text en © 2023 by the authors. https://creativecommons.org/licenses/by/4.0/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/).
spellingShingle Article
Nuccio, Daniel A.
Normann, Marigny C.
Zhou, Haiming
Grippo, Angela J.
Singh, Pallavi
Microbiome and Metabolome Variation as Indicator of Social Stress in Female Prairie Voles
title Microbiome and Metabolome Variation as Indicator of Social Stress in Female Prairie Voles
title_full Microbiome and Metabolome Variation as Indicator of Social Stress in Female Prairie Voles
title_fullStr Microbiome and Metabolome Variation as Indicator of Social Stress in Female Prairie Voles
title_full_unstemmed Microbiome and Metabolome Variation as Indicator of Social Stress in Female Prairie Voles
title_short Microbiome and Metabolome Variation as Indicator of Social Stress in Female Prairie Voles
title_sort microbiome and metabolome variation as indicator of social stress in female prairie voles
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9861106/
https://www.ncbi.nlm.nih.gov/pubmed/36675193
http://dx.doi.org/10.3390/ijms24021677
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