Prebiotic administration modulates gut microbiota and faecal short-chain fatty acid concentrations but does not prevent chronic intermittent hypoxia-induced apnoea and hypertension in adult rats

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Abstract

Background

Evidence is accruing to suggest that microbiota-gut-brain signalling plays a regulatory role in cardiorespiratory physiology. Chronic intermittent hypoxia (CIH), modelling human sleep apnoea, affects gut microbiota composition and elicits cardiorespiratory morbidity. We investigated if treatment with prebiotics ameliorates cardiorespiratory dysfunction in CIH-exposed rats.

Methods

Adult male rats were exposed to CIH (96 cycles/day, 6.0% O ₂ at nadir) for 14 consecutive days with and without prebiotic supplementation (fructo- and galacto-oligosaccharides) beginning two weeks prior to gas exposures.

Findings

CIH increased apnoea index and caused hypertension. CIH exposure had modest effects on the gut microbiota, decreasing the relative abundance of Lactobacilli species, but had no effect on microbial functional characteristics. Faecal short-chain fatty acid (SCFA) concentrations, plasma and brainstem pro-inflammatory cytokine concentrations and brainstem neurochemistry were unaffected by exposure to CIH. Prebiotic administration modulated gut microbiota composition and diversity, altering gut-metabolic (GMMs) and gut-brain (GBMs) modules and increased faecal acetic and propionic acid concentrations, but did not prevent adverse CIH-induced cardiorespiratory phenotypes.

Interpretation

CIH-induced cardiorespiratory dysfunction is not dependant upon changes in microbial functional characteristics and decreased faecal SCFA concentrations. Prebiotic-related modulation of microbial function and resultant increases in faecal SCFAs were not sufficient to prevent CIH-induced apnoea and hypertension in our model. Our results do not exclude the potential for microbiota-gut-brain axis involvement in OSA-related cardiorespiratory morbidity, but they demonstrate that in a relatively mild model of CIH, sufficient to evoke classic cardiorespiratory dysfunction, such changes are not obligatory for the development of morbidity, but may become relevant in the elaboration and maintenance of cardiorespiratory morbidity with progressive disease.

Funding

Department of Physiology and APC Microbiome Ireland, University College Cork, Ireland. APC Microbiome Ireland is funded by Science Foundation Ireland, through the Government's National Development Plan.

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Most cited references 77

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Alterations of the Gut Microbiome in Hypertension

Qiulong Yan, Yifang Gu, Xiangchun Li … (2017)

Introduction: Human gut microbiota is believed to be directly or indirectly involved in cardiovascular diseases and hypertension. However, the identification and functional status of the hypertension-related gut microbe(s) have not yet been surveyed in a comprehensive manner. Methods: Here we characterized the gut microbiome in hypertension status by comparing fecal samples of 60 patients with primary hypertension and 60 gender-, age-, and body weight-matched healthy controls based on whole-metagenome shotgun sequencing. Results: Hypertension implicated a remarkable gut dysbiosis with significant reduction in within-sample diversity and shift in microbial composition. Metagenome-wide association study (MGWAS) revealed 53,953 microbial genes that differ in distribution between the patients and healthy controls (false discovery rate, 0.05) and can be grouped into 68 clusters representing bacterial species. Opportunistic pathogenic taxa, such as, Klebsiella spp., Streptococcus spp., and Parabacteroides merdae were frequently distributed in hypertensive gut microbiome, whereas the short-chain fatty acid producer, such as, Roseburia spp. and Faecalibacterium prausnitzii, were higher in controls. The number of hypertension-associated species also showed stronger correlation to the severity of disease. Functionally, the hypertensive gut microbiome exhibited higher membrane transport, lipopolysaccharide biosynthesis and steroid degradation, while in controls the metabolism of amino acid, cofactors and vitamins was found to be higher. We further provided the microbial markers for disease discrimination and achieved an area under the receiver operator characteristic curve (AUC) of 0.78, demonstrating the potential of gut microbiota in prediction of hypertension. Conclusion: These findings represent specific alterations in microbial diversity, genes, species and functions of the hypertensive gut microbiome. Further studies on the causality relationship between hypertension and gut microbiota will offer new prospects for treating and preventing the hypertension and its associated diseases.

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Species-function relationships shape ecological properties of the human gut microbiome.

Sara Vieira-Silva, Gwen Falony, Youssef Darzi … (2016)

Despite recent progress, the organization and ecological properties of the intestinal microbial ecosystem remain under-investigated. Here, using a manually curated metabolic module framework for (meta-)genomic data analysis, we studied species-function relationships in gut microbial genomes and microbiomes. Half of gut-associated species were found to be generalists regarding overall substrate preference, but we observed significant genus-level metabolic diversification linked to bacterial life strategies. Within each genus, metabolic consistency varied significantly, being low in Firmicutes genera and higher in Bacteroides. Differentiation of fermentable substrate degradation potential contributed to metagenomic functional repertoire variation between individuals, with different enterotypes showing distinct saccharolytic/proteolytic/lipolytic profiles. Finally, we found that module-derived functional redundancy was reduced in the low-richness Bacteroides enterotype, potentially indicating a decreased resilience to perturbation, in line with its frequent association to dysbiosis. These results provide insights into the complex structure of gut microbiome-encoded metabolic properties and emphasize the importance of functional and ecological assessment of gut microbiome variation in clinical studies.

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bioBakery: a meta’omic analysis environment

Lauren Mciver, Galeb Abu-Ali, Eric Franzosa … (2017)

Abstract Summary bioBakery is a meta’omic analysis environment and collection of individual software tools with the capacity to process raw shotgun sequencing data into actionable microbial community feature profiles, summary reports, and publication-ready figures. It includes a collection of pre-configured analysis modules also joined into workflows for reproducibility. Availability and implementation bioBakery (http://huttenhower.sph.harvard.edu/biobakery) is publicly available for local installation as individual modules and as a virtual machine image. Each individual module has been developed to perform a particular task (e.g. quantitative taxonomic profiling or statistical analysis), and they are provided with source code, tutorials, demonstration data, and validation results; the bioBakery virtual image includes the entire suite of modules and their dependencies pre-installed. Images are available for both Amazon EC2 and Google Compute Engine. All software is open source under the MIT license. bioBakery is actively maintained with a support group at biobakery-users@googlegroups.com and new tools being added upon their release. Supplementary information Supplementary data are available at Bioinformatics online.

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Author and article information

Contributors

Ken D. O'Halloran

Journal

Journal ID (nlm-ta): EBioMedicine

Journal ID (iso-abbrev): EBioMedicine

Title: EBioMedicine

Publisher: Elsevier

ISSN (Electronic): 2352-3964

Publication date PMC-release: 30 August 2020

Publication date Collection: September 2020

Publication date (Electronic): 30 August 2020

Volume: 59

Electronic Location Identifier: 102968

Affiliations

[a ]Department of Physiology, School of Medicine, College of Medicine & Health, University College Cork, Cork, Ireland

[b ]Department of Anatomy & Neuroscience, School of Medicine, College of Medicine & Health, University College Cork, Cork, Ireland

[c ]APC Microbiome Ireland, University College Cork, Cork, Ireland

[d ]Teagasc Food Research Centre, Moorepark, Fermoy, County Cork, Ireland

[e ]Department of Psychiatry and Neurobehavioural Science, School of Medicine, College of Medicine & Health, University College Cork, Cork, Ireland

Author notes

[* ]Corresponding author : Ken D. O'Halloran, Department of Physiology, University College Cork, Western Gateway Building, Western Road, Cork, Ireland. k.ohalloran@ 123456ucc.ie

Article

Publisher ID: S2352-3964(20)30344-3 Publisher ID: 102968

DOI: 10.1016/j.ebiom.2020.102968

PMC ID: 7475129

PubMed ID: 32861200

SO-VID: 35ac5955-e0d9-4acb-b7ee-000b6b380f82

License:

This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/).

History

Date received : 10 April 2020

Date revision received : 22 May 2020

Date accepted : 6 August 2020

Categories

Subject: Research paper

Keywords: chronic intermittent hypoxia,prebiotics,apnoea,hypertension,autonomic dysfunction,neurochemistry,short-chain fatty acids,vagus,microbiota,auc, area under the curve,bh, benjamini-hochberg,cih, chronic intermittent hypoxia,da, dopamine,dopac, 3,4-dihydroxyphenylacetic acid,dia, diaphragm,emg, electromyogram,etco2, end-tidal carbon dioxide,fdr, false discovery rate,fr, respiratory frequency,fico2, fractional inspired carbon dioxide concentration,fio2, fractional inspired oxygen concentration,gaba, gamma-aminobutyric acid,gbm, gut-brain modules,gmm, gut-metabolic modules,hfd, high-fat diet,hsd, high-salt diet,hva, homovanillic acid,ifn, interferon,il, interleukin,kc/gro, keratinocytechemoattractant/growth-related oncogene,kegg, kyoto encyclopedia of genes and genomes,l-dopa, l-3,4-dihydroxyphenylalanine,lsd, least significant difference,na, noradrenaline,nacn, sodium cyanide,nts, nucleus tractus solitarius,osa, obstructive sleep apnoea,pbg, phenylbiguanide,pca, principal component analysis,pcoa, principal coordinates analysis,paco2, partial pressure of arterial carbon dioxide,pao2, partial pressure of arterial oxygen,preb, prebiotic,sao2, arterial oxygen saturation,sdb, sleep-disordered breathing,sd1, short-term respiratory timing variability,sd2, long-term respiratory timing variability,te, expiratory time,ti, inspiratory time,tmao, trimethylamine n-oxide,tnf-α, tumor necrosis factor-α,ttot, total breath duration,vco2, carbon dioxide production,vi, minute ventilation,vi/vco2, ventilatory equivalent for co2,vo2, oxygen consumption,vt, tidal volume,vt/ti, mean inspiratory flow,5-hiaa, 5-hydroindoleacetic acid,5-ht, 5-hydroxytryptamine (serotonin),5-ht3, 5-hydroxytryptamine type 3

Data availability:

Keywords: chronic intermittent hypoxia, prebiotics, apnoea, hypertension, autonomic dysfunction, neurochemistry, short-chain fatty acids, vagus, microbiota, auc, area under the curve, bh, benjamini-hochberg, cih, chronic intermittent hypoxia, da, dopamine, dopac, 3,4-dihydroxyphenylacetic acid, dia, diaphragm, emg, electromyogram, etco2, end-tidal carbon dioxide, fdr, false discovery rate, fr, respiratory frequency, fico2, fractional inspired carbon dioxide concentration, fio2, fractional inspired oxygen concentration, gaba, gamma-aminobutyric acid, gbm, gut-brain modules, gmm, gut-metabolic modules, hfd, high-fat diet, hsd, high-salt diet, hva, homovanillic acid, ifn, interferon, il, interleukin, kc/gro, keratinocytechemoattractant/growth-related oncogene, kegg, kyoto encyclopedia of genes and genomes, l-dopa, l-3,4-dihydroxyphenylalanine, lsd, least significant difference, na, noradrenaline, nacn, sodium cyanide, nts, nucleus tractus solitarius, osa, obstructive sleep apnoea, pbg, phenylbiguanide, pca, principal component analysis, pcoa, principal coordinates analysis, paco2, partial pressure of arterial carbon dioxide, pao2, partial pressure of arterial oxygen, preb, prebiotic, sao2, arterial oxygen saturation, sdb, sleep-disordered breathing, sd1, short-term respiratory timing variability, sd2, long-term respiratory timing variability, te, expiratory time, ti, inspiratory time, tmao, trimethylamine n-oxide, tnf-α, tumor necrosis factor-α, ttot, total breath duration, vco2, carbon dioxide production, vi, minute ventilation, vi/vco2, ventilatory equivalent for co2, vo2, oxygen consumption, vt, tidal volume, vt/ti, mean inspiratory flow, 5-hiaa, 5-hydroindoleacetic acid, 5-ht, 5-hydroxytryptamine (serotonin), 5-ht3, 5-hydroxytryptamine type 3

Prebiotic administration modulates gut microbiota and faecal short-chain fatty acid concentrations but does not prevent chronic intermittent hypoxia-induced apnoea and hypertension in adult rats

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Abstract

Background

Methods

Findings

Interpretation

Funding

Related collections

Tick microbiome

Most cited references 77

Alterations of the Gut Microbiome in Hypertension

Species-function relationships shape ecological properties of the human gut microbiome.

bioBakery: a meta’omic analysis environment

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Contributors

Journal

Affiliations

Author notes

Article

History

Categories

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