Ecological memory of prior nutrient exposure in the human gut microbiome

Letourneau, Jeffrey; Holmes, Zachary C.; Dallow, Eric P.; Durand, Heather K.; Jiang, Sharon; Carrion, Verónica M.; Gupta, Savita K.; Mincey, Adam C.; Muehlbauer, Michael J.; Bain, James R.; David, Lawrence A.

doi:10.1038/s41396-022-01292-x

Cited by 18 publications

(10 citation statements)

References 70 publications

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“…Despite these encouraging trends, a growing number of non-hospitalized adults still develop long-lasting symptoms persisting months after clearing the virus (15,16), highlighting the importance of understanding the mechanisms responsible. Considered in light of emerging evidence that the microbiome can exhibit "ecological memory" of past events (17), we hypothesized that even mild cases of SARS-CoV-2 could still disrupt the gut microbiota, potentially contributing to phenotypes months later.…”

Section: Introductionmentioning

confidence: 99%

Mild SARS-CoV-2 infection results in long-lasting microbiota instability

Upadhyay

Suryawanshi²,

Tasoff³

et al. 2022

Preprint

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Viruses targeting mammalian cells can indirectly alter the gut microbiota, potentially compounding their phenotypic effects. Multiple studies have observed a disrupted gut microbiota in severe cases of SARS-CoV-2 infection that require hospitalization. Yet, despite demographic shifts in disease severity resulting in a large and continuing burden of non-hospitalized infections, we still know very little about the impact of mild SARS-CoV-2 infection on the gut microbiota in the outpatient setting. To address this knowledge gap, we longitudinally sampled 14 SARS-CoV-2 positive subjects who remained outpatient and 4 household controls. SARS-CoV-2 cases exhibited a significantly less stable gut microbiota relative to controls, as long as 154 days after their positive test. These results were confirmed and extended in the K18-hACE2 mouse model, which is susceptible to SARS-CoV-2 infection. All of the tested SARS-CoV-2 variants significantly disrupted the mouse gut microbiota, including USA-WA1/2020 (the original variant detected in the United States), Delta, and Omicron. Surprisingly, despite the fact that the Omicron variant caused the least severe symptoms in mice, it destabilized the gut microbiota and led to a significant depletion in Akkermansia muciniphila. Furthermore, exposure of wild-type C57BL/6J mice to SARS-CoV-2 disrupted the gut microbiota in the absence of severe lung pathology.

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Section: Introductionmentioning

confidence: 99%

Mild SARS-CoV-2 infection results in long-lasting microbiota instability

Upadhyay

Suryawanshi²,

Tasoff³

et al. 2022

Preprint

View full text Add to dashboard Cite

show abstract

“…We also show that high pBMI is associated with diminished remodeling of the gut microbiome during pregnancy, which may reflect a reduced requirement for metabolic adaptations to pregnancy. Overall, these data support a role for the gut microbiota in modulating maternal metabolic adaptations to pregnancy and suggest the gut microbiome may retain an "ecological memory" (Letourneau et al, 2022) of prior pregnancies (Berry et al, 2021). (stars) participants (dot size based on mean abundance, colours correspond to genus colour in a where a differentially abundant genus is among the 20 most abundant genera).…”

Section: Discussionmentioning

confidence: 61%

“…These outcomes are important not only to maternal health, but also to infant health as infants born to multiparous women with excess gestational weight gain show distinct shifts in their microbiota. Finally, our data suggest the human gut microbiome may retain an "ecological memory" 38 of prior pregnancies 44 which may serve as an adaptation that minimizes maternal constraint in subsequent pregnancies.…”

Section: Discussionmentioning

confidence: 77%

“…We also show for the first time in humans that parity modulates the impact of pBMI on pregnancy-associated remodeling of the maternal gut microbiota and also modulates the impact of perinatal antibiotic exposure and GWG on the infant gut microbiota. We now suggest that the maternal gut microbiota may retain a “ecological memory” 38 of previous pregnancies.…”

Section: Discussionmentioning

confidence: 79%

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Parity modulates impact of BMI and Gestational Weight Gain on gut microbiota in human pregnancy

Kennedy

Plagemann

Sommer

et al. 2022

Preprint

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Shifts in the gut microbiome have been implicated in mediating maternal metabolic adaptations to pregnancy. We investigated the impact of pre-pregnancy BMI (pBMI) and gestational weight gain (GWG) on pregnancy-associated remodeling of the maternal gut microbiome and infant colonization, and whether previous pregnancies modulated observed associations. We found that the gut microbiota of participants with higher pBMI changed less over the course of pregnancy in primiparous, but not multiparous participants This suggests that previous pregnancies may have persistent impacts on maternal microbiotal adaptations to pregnancy. This ecological memory appears to be passed to the next generation, as parity impacted infant microbial composition of first-pass meconium and modulated the impact of maternal GWG on the infant gut microbiome. This work supports a role for the gut microbiome in maternal adaptations to pregnancy and highlights parity as a key consideration for studies of the microbiome in pregnancy and infants.

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“…Unlike butyric acid and acetic acid acting as sources of energy for host cells, propionic acid is the precursor for adipogenesis and gluconeogenesis, which plays more important roles in the pathogenesis of NAFLD ( Liu et al., 2021 ). Interestingly, no matter what type of dietary fiber the patients have taken, it will present obvious benefits as soon as it enters the intestinal tract, especially, to those who are already low in dietary fiber intake ( Letourneau et al., 2022 ). Mechanically, SCFAs activate G protein-coupled receptors, such as GPR41 and GPR43, in intestinal and adipose tissues ( Lu et al., 2016 ).…”

Section: Roles Of the Gut Microbiota Dysbiosis On Nafld Occurrence An...mentioning

confidence: 99%

Gut dysbiosis in nonalcoholic fatty liver disease: pathogenesis, diagnosis, and therapeutic implications

Fang

Yu²,

Li³

et al. 2022

Front. Cell. Infect. Microbiol.

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The incidence of nonalcoholic fatty liver disease (NAFLD) is increasing recently and has become one of the most common clinical liver diseases. Since the pathogenesis of NAFLD has not been completely elucidated, few effective therapeutic drugs are available. As the “second genome” of human body, gut microbiota plays an important role in the digestion, absorption and metabolism of food and drugs. Gut microbiota can act as an important driver to advance the occurrence and development of NAFLD, and to accelerate its progression to cirrhosis and hepatocellular carcinoma. Growing evidence has demonstrated that gut microbiota and its metabolites directly affect intestinal morphology and immune response, resulting in the abnormal activation of inflammation and intestinal endotoxemia; gut dysbiosis also causes dysfunction of gut-liver axis via alteration of bile acid metabolism pathway. Because of its composition diversity and disease-specific expression characteristics, gut microbiota holds strong promise as novel biomarkers and therapeutic targets for NAFLD. Intervening intestinal microbiota, such as antibiotic/probiotic treatment and fecal transplantation, has been a novel strategy for preventing and treating NAFLD. In this article, we have reviewed the emerging functions and association of gut bacterial components in different stages of NAFLD progression and discussed its potential implications in NAFLD diagnosis and therapy.

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Ecological memory of prior nutrient exposure in the human gut microbiome

Cited by 18 publications

References 70 publications

Mild SARS-CoV-2 infection results in long-lasting microbiota instability

Mild SARS-CoV-2 infection results in long-lasting microbiota instability

Parity modulates impact of BMI and Gestational Weight Gain on gut microbiota in human pregnancy

Gut dysbiosis in nonalcoholic fatty liver disease: pathogenesis, diagnosis, and therapeutic implications

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