Taxonomic and Functional Shifts in the Perinatal Gut Microbiome of Rhesus Macaques

Rhoades, Nicholas S; Cinco, Isaac R; Hendrickson, Sara M; Messaoudi, Ilhem

doi:10.1128/spectrum.00814-22

Cited by 4 publications

(1 citation statement)

References 64 publications

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“…We also found that the gut microbiome of dams that gave birth to infants who experienced diarrhea was both functionally and taxonomically distinct prior to the infants becoming sick, including increased pathogen burden (Campylobacter jejuni and Escherichia coli). Our data align with recent ndings from human cohorts that demonstrated that the maternal microbiome can modulate the infant microbiome composition, immune development, and infant growth [52][53][54] . However, the mechanism by which the maternal microbiome in uences protection and/or vulnerability to disease in the infant deserves further attention as the maternal microbiome is dynamic during the perinatal period.…”

Section: Disscusionsupporting

confidence: 91%

Infant diarrheal disease impedes maturation of the microbiome and is linked to a diverse set of novel yet to be cultured Campylobacter species.

Messaoudi

Rhoades

Cinco

et al. 2023

Preprint

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Diarrheal diseases remain one of the leading causes of death for children under 5 globally, disproportionately impacting those living in low- and middle-income countries (LMIC). Campylobacter spp. is a zoonotic pathogen found in many animal species and is one of the leading causes of food-borne infection in humans, and yet to be cultured Campylobactercontribute to the total burden in diarrheal disease in LMIC children thus hampering interventions. We performed microbiome profiling and metagenomic genome assembly on samples collected from over 100 infant rhesus macaques longitudinally and during cases of clinical diarrhea within the first year of life. Acute diarrhea was associated with taxonomic and functional shifts of the infant gut microbiome and resulted in a chronic state of microbiome immaturity well beyond the resolution of symptoms. One of the major drivers of these changes was the increased relative abundance of Campylobacter which we investigated further using metagenomic assembled genomes (MAGs). We constructed 36 CampylobacterMAGs, many of which fell within 4 yet to be cultured species. Finally, we used the uncultured Campylobacter MAGs assembled from infant macaques with publicly available human metagenomes to show that these uncultured species are also found in human fecal samples from LMIC. These data highlight the importance unculturable Campylobacter spp. as an important target for reducing disease burden in LMIC children.

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Section: Disscusionsupporting

confidence: 91%

Infant diarrheal disease impedes maturation of the microbiome and is linked to a diverse set of novel yet to be cultured Campylobacter species.

Messaoudi

Rhoades

Cinco

et al. 2023

Preprint

Self Cite

View full text Add to dashboard Cite

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Infant diarrheal disease in rhesus macaques impedes microbiome maturation and is linked to uncultured Campylobacter species

Rhoades,

Cinco,

Hendrickson

et al. 2024

Commun Biol

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Diarrheal diseases remain one of the leading causes of death for children under 5 globally, disproportionately impacting those living in low- and middle-income countries (LMIC). Campylobacter spp., a zoonotic pathogen, is one of the leading causes of food-borne infection in humans. Yet to be cultured Campylobacter spp. contribute to the total burden in diarrheal disease in children living in LMIC thus hampering interventions. We performed microbiome profiling and metagenomic genome assembly on samples collected from over 100 infant rhesus macaques longitudinally and during cases of clinical diarrhea within the first year of life. Acute diarrhea was associated with long-lasting taxonomic and functional shifts of the infant gut microbiome indicative of microbiome immaturity. We constructed 36 Campylobacter metagenomic assembled genomes (MAGs), many of which fell within 4 yet to be cultured species. Finally, we compared the uncultured Campylobacter MAGs assembled from infant macaques with publicly available human metagenomes to show that these uncultured species are also found in human fecal samples from LMIC. These data highlight the importance of unculturable Campylobacter spp. as an important target for reducing disease burden in LMIC children.

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Host–gut microbiota interactions during pregnancy

Amato,

Pradhan,

Mallott

et al. 2024

Evolution, Medicine, and Public Health

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Mammalian pregnancy is characterized by a well-known suite of physiological changes that support fetal growth and development, thereby positively affecting both maternal and offspring fitness. However, mothers also experience trade-offs between current and future maternal reproductive success, and maternal responses to these trade-offs can result in mother-offspring fitness conflicts. Knowledge of the mechanisms through which these trade-offs operate, as well as the contexts in which they operate, is critical for understanding the evolution of reproduction. Historically, hormonal changes during pregnancy have been thought to play a pivotal role in these conflicts since they directly and indirectly influence maternal metabolism, immunity, fetal growth, and other aspects of offspring development. However, recent research suggests the gut microbiota may also play an important role. Here, we create a foundation for exploring this role by constructing a mechanistic model linking changes in maternal hormones, immunity, and metabolism during pregnancy to changes in the gut microbiota. We posit that marked changes in hormones alter maternal gut microbiome composition and function both directly and indirectly via impacts on the immune system. The gut microbiota then feeds back to influence maternal immunity and metabolism. We posit that these dynamics are likely to be involved in mediating maternal and offspring fitness as well as trade-offs in different aspects of maternal and offspring health and fitness during pregnancy. We also predict that the interactions we describe are likely to vary across populations in response to maternal environments. Moving forward, empirical studies that combine microbial functional data and maternal physiological data with health and fitness outcomes for both mothers and infants will allow us to test the evolutionary and fitness implications of the gestational microbiota, enriching our understanding of the ecology and evolution of reproductive physiology.

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Taxonomic and Functional Shifts in the Perinatal Gut Microbiome of Rhesus Macaques

Abstract: Pregnancy and the postpartum period are characterized by a myriad of metabolic and physiological adaptations needed to support fetal growth and maternal health. The maternal gut microbiome is believed to play a key role during this period but remains underexplored.

Cited by 4 publications

References 64 publications

Infant diarrheal disease impedes maturation of the microbiome and is linked to a diverse set of novel yet to be cultured Campylobacter species.

Infant diarrheal disease impedes maturation of the microbiome and is linked to a diverse set of novel yet to be cultured Campylobacter species.

Infant diarrheal disease in rhesus macaques impedes microbiome maturation and is linked to uncultured Campylobacter species

Host–gut microbiota interactions during pregnancy

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