Analysis of global human gut metagenomes shows that metabolic resilience potential for short-chain fatty acid production is strongly influenced by lifestyle

Jacobson, David P.; Honap, Tanvi P.; Ozga, Andrew T.; Méda, Nicolas; Kagoné, Thérèse; Carabin, Hélène; Spicer, Paul; Tito, Raúl Y.; Obregón-Tito, Alexandra J.; Reyes, Luis Marin; Troncoso-Corzo, Luzmila; Guija-Poma, Emilio; Sankaranarayanan, Krithivasan; Lewis, Cecil M.

doi:10.1038/s41598-021-81257-w

Cited by 11 publications

(11 citation statements)

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“…As expected, we identified higher relative abundances of butyrate production pathways in nonindustrialized populations compared with industrialized populations. Similar patterns have been previously reported by studies examining both the taxonomic composition and function of the human microbiome ( Schnorr et al 2014 ; Smits et al 2017 ; Jacobson et al 2021 ). The gut microbiomes of nonindustrialized human populations generally have increased fiber degradation and SCFA production potential.…”

Section: Discussionsupporting

confidence: 88%

“…The gut microbiomes of nonindustrialized human populations generally have increased fiber degradation and SCFA production potential. For example, a study of variation in the terminal buk and but enzymes of the butyrate synthesis pathways reported lower relative abundances in industrialized populations ( Jacobson et al 2021 ). Given that industrialized diets typically incorporate much lower amounts of fiber than nonindustrialized populations, these findings are not surprising.…”

Section: Discussionmentioning

confidence: 99%

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Butyrate Production Pathway Abundances Are Similar in Human and Nonhuman Primate Gut Microbiomes

Mallott

Amato

2021

Molecular Biology and Evolution

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Over the course of human evolution, shifts in dietary practices such as meat-eating and cooking, have resulted in reduced fiber intake, a trend that has been exaggerated more recently in industrialized populations. Reduced fiber consumption is associated with a loss of gut microbial taxa that degrade fiber, particularly butyrate. Therefore, this dietary shift in humans may have altered the abundance of microbial genes involved in butyrate production. This study uses a gene-targeted alignment approach to quantify the abundance of butyrate production pathway genes from published wild nonhuman primate and human gut metagenomes. Surprisingly, humans have higher diversity and relative abundances of butyrate production pathways compared with all groups of nonhuman primates except cercopithecoids. Industrialized populations of humans also differ only slightly in butyrate pathway abundance from non-industrialized populations. This apparent resilience of butyrate-production pathways to shifts in human diet across both evolutionary and modern populations may signal an evolutionary shift in host-microbe interactions in humans that increased SCFA production. Such a shift could have contributed to meeting the increased energy requirements of humans relative to nonhuman primates.

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Section: Discussionsupporting

confidence: 88%

Section: Discussionmentioning

confidence: 99%

Butyrate Production Pathway Abundances Are Similar in Human and Nonhuman Primate Gut Microbiomes

Mallott

Amato

2021

Molecular Biology and Evolution

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“…Build-up of a trophic network of fibre degraders, acetate and lactate producers combined with butyrate producers ( F. prausnitzii ) appears to be essential for healthy immune system development in children in industrialized counties 12 . Addition of the P. stercorea trophic network in our African cohort (alongside P. copri ) probably helps explain why higher levels of short-chain fatty acid production are seen in African people with non-industrialized gut microbiomes 18 , 19 .…”

Section: Discussionmentioning

confidence: 94%

Gut microbiomes from Gambian infants reveal the development of a non-industrialized Prevotella-based trophic network

et al. 2021

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Distinct bacterial trophic networks exist in the gut microbiota of individuals in industrialized and non-industrialized countries. In particular, non-industrialized gut microbiomes tend to be enriched with Prevotella species. To study the development of these Prevotella-rich compositions, we investigated the gut microbiota of children aged between 7 and 37 months living in rural Gambia (616 children, 1,389 stool samples, stratified by 3-month age groups). These infants, who typically eat a high-fibre, low-protein diet, were part of a double-blind, randomized iron intervention trial (NCT02941081) and here we report the secondary outcome. We found that child age was the largest discriminating factor between samples and that anthropometric indices (collection time points, season, geographic collection site, and iron supplementation) did not significantly influence the gut microbiome. Prevotella copri, Faecalibacterium prausnitzii and Prevotella stercorea were, on average, the most abundant species in these 1,389 samples (35%, 11% and 7%, respectively). Distinct bacterial trophic network clusters were identified, centred around either P.stercorea or F.prausnitzii and were found to develop steadily with age, whereas P.copri, independently of other species, rapidly became dominant after weaning. This dataset, set within a critical gut microbial developmental time frame, provides insights into the development of Prevotella-rich gut microbiomes, which are typically understudied and are underrepresented in western populations.

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“…In the colon, this ratio is 60:25:15, respectively, and it varies in individual sections of the intestine depending on factors such as diet, age and disease. The importance of SCFA in the human body may be proven by the fact that 95% of these compounds are absorbed by intestinal epithelial cells, and only 5% is excreted from the body with the feces [ 30 ].…”

Section: The Process Of Immune Modulation By Human Gut Microbiotamentioning

confidence: 99%

A Link between Chronic Kidney Disease and Gut Microbiota in Immunological and Nutritional Aspects

et al. 2021

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Chronic kidney disease (CKD) is generally progressive and irreversible, structural or functional renal impairment for 3 or more months affecting multiple metabolic pathways. Recently, the composition, dynamics, and stability of a patient’s microbiota has been noted to play a significant role during disease onset or progression. Increasing urea concentration during CKD can lead to an acceleration of the process of kidney injury leading to alterations in the intestinal microbiota that can increase the production of gut-derived toxins and alter the intestinal epithelial barrier. A detailed analysis of the relationship between the role of intestinal microbiota and the development of inflammation within the symbiotic and dysbiotic intestinal microbiota showed significant changes in kidney dysfunction. Several recent studies have determined that dietary factors can significantly influence the activation of immune cells and their mediators. Moreover, dietary changes can profoundly affect the balance of gut microbiota. The aim of this review is to present the importance and factors influencing the differentiation of the human microbiota in the progression of kidney diseases, such as CKD, IgA nephropathy, idiopatic nephropathy, and diabetic kidney disease, with particular emphasis on the role of the immune system. Moreover, the effects of nutrients, bioactive compounds on the immune system in development of chronic kidney disease were reviewed.

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Analysis of global human gut metagenomes shows that metabolic resilience potential for short-chain fatty acid production is strongly influenced by lifestyle

Cited by 11 publications

References 50 publications

Butyrate Production Pathway Abundances Are Similar in Human and Nonhuman Primate Gut Microbiomes

Butyrate Production Pathway Abundances Are Similar in Human and Nonhuman Primate Gut Microbiomes

Gut microbiomes from Gambian infants reveal the development of a non-industrialized Prevotella-based trophic network

A Link between Chronic Kidney Disease and Gut Microbiota in Immunological and Nutritional Aspects

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