Glucocorticoids modulate gastrointestinal microbiome in a wild bird

Noguera, José C.; Aira, Manuel; Pérez‐Losada, Marcos; Domínguez, Jorge; Velando, Alberto

doi:10.1098/rsos.171743

Cited by 99 publications

(105 citation statements)

References 46 publications

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“…GCs have been shown to alter the composition of gut microbes, which are linked to changes in gut and brain function. (31,32,102,113) For example, stress, which elevates serum corticosteroid levels, alters the microbiome and reduces levels of intestinal lactobacilli and increases the growth of E. coli and pseudomonas. (102,113) Stress also increases intestinal bacterial expression of virulence genes.…”

Section: Discussionmentioning

confidence: 99%

“…In addition to the direct effects of GC on bone, GCs also affect other organ systems that can further influence bone health. Especially relevant to the present study, GCs can alter intestinal microbiota composition in animal models …”

Section: Introductionmentioning

confidence: 94%

“…Especially relevant to the present study, GCs can alter intestinal microbiota composition in animal models. (31,32) The microbiome, defined as the collective genetic material of the microbiota, contains an estimated 3 to 8 million unique genes, >100-fold larger than the human genome. (33,34) The intestinal microbiota contains bacteria as well as fungi, viruses, and archaea.…”

mentioning

confidence: 99%

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Involvement of the Gut Microbiota and Barrier Function in Glucocorticoid-Induced Osteoporosis

Schepper

Collins

Rios‐Arce

et al. 2019

Journal of Bone and Mineral Research

135

119

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Glucocorticoids (GCs) are potent immune‐modulating drugs with significant side effects, including glucocorticoid‐induced osteoporosis (GIO). GCs directly induce osteoblast and osteocyte apoptosis but also alter intestinal microbiota composition. Although the gut microbiota is known to contribute to the regulation of bone density, its role in GIO has never been examined. To test this, male C57/Bl6J mice were treated for 8 weeks with GC (prednisolone, GC‐Tx) in the presence or absence of broad‐spectrum antibiotic treatment (ABX) to deplete the microbiota. Long‐term ABX prevented GC‐Tx‐induced trabecular bone loss, showing the requirement of gut microbiota for GIO. Treatment of GC‐Tx mice with a probiotic (Lactobacillus reuteri [LR]) prevented trabecular bone loss. Microbiota analyses indicated that GC‐Tx changed the abundance of Verrucomicobiales and Bacteriodales phyla and random forest analyses indicated significant differences in abundance of Porphyromonadaceae and Clostridiales operational taxonomic units (OTUs) between groups. Furthermore, transplantation of GC‐Tx mouse fecal material into recipient naïve, untreated WT mice caused bone loss, supporting a functional role for microbiota in GIO. We also report that GC caused intestinal barrier breaks, as evidenced by increased serum endotoxin level (2.4‐fold), that were prevented by LR and ABX treatments. Enhancement of barrier function with a mucus supplement prevented both GC‐Tx–induced barrier leakage and trabecular GIO. In bone, treatment with ABX, LR or a mucus supplement reduced GC‐Tx–induced osteoblast and osteocyte apoptosis. GC‐Tx suppression of Wnt10b in bone was restored by the LR and high‐molecular‐weight polymer (MDY) treatments as well as microbiota depletion. Finally, we identified that bone‐specific Wnt10b overexpression prevented GIO. Taken together, our data highlight the previously unappreciated involvement of the gut microbiota and intestinal barrier function in trabecular GIO pathogenesis (including Wnt10b suppression and osteoblast and osteocyte apoptosis) and identify the gut as a novel therapeutic target for preventing GIO. © 2019 American Society for Bone and Mineral Research.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 94%

mentioning

confidence: 99%

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Involvement of the Gut Microbiota and Barrier Function in Glucocorticoid-Induced Osteoporosis

Schepper

Collins

Rios‐Arce

et al. 2019

Journal of Bone and Mineral Research

135

119

View full text Add to dashboard Cite

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“…Although no primate study has yet tested this hypothesis, in wild red squirrels ( Tamiasciurus hudsonicus ) it was found that fecal glucocorticoid metabolites were negatively correlated with bacterial diversity and that there was a positive relationship over time between fecal glucocorticoid metabolite concentrations and bacterial abundance of Pasteurellaceae, a family with known epizootic pathogens (Stothart et al, ). On the contrary, experimentally elevated basal glucocorticoid levels reduced pathogenic bacteria, including Mycoplasma and Microvirga , in the intestines of yellow‐legged gulls ( Larus michahellis ; Noguera, Aira, Pérez‐Losada, Domínguez, & Velando, ).…”

Section: Microbial Endocrinology Of the Stress Responsementioning

confidence: 99%

Primate microbial endocrinology: An uncharted frontier

Benavidez

Iruri‐Tucker

Steiniche

et al. 2019

American J Primatol

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Gut microbial communities communicate bidirectionally with the brain through endocrine, immune, and neural signaling, influencing the physiology and behavior of hosts. The emerging field of microbial endocrinology offers innovative perspectives and methods to analyze host-microbe relationships with relevance to primate ecology, evolution, and conservation. Herein we briefly summarize key findings from microbial endocrinology and explore how applications of a similar framework could inform our understanding of primate stress and reproductive physiology and behavior. We conclude with three guiding hypotheses to further investigate endocrine signaling between gut microbes and the host: (a) host-microbe communication systems promote microbe-mediated stability, in which the microbes are using endocrine signaling from the host to maintain a functioning habitat for their own fitness, (b) host-microbe communication systems promote host-mediated stability, in which the host uses the endocrine system to monitor microbial communities and alter these communities to maintain stability, or (c) host-microbe systems are simply the product of coincidental cross-talk between the host and microbes due to similar molecules from shared ancestry. Utilizing theory and methodology for studying relationships between the microbiome, hormones, and behavior of wild primates is an uncharted frontier with many promising insights when applied to primatology. K E Y W O R D Smicrobe-hormone interactions, neuroendocrine system, reproduction, stress physiology

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“…As the mediator between a vertebrate's perception of its environment and a suite of physiological responses, the HPA axis provides a useful universal measure of how host responses to environmental stimuli could shape the microbiome. Change in the HPA axis has been demonstrated to affect the microbiome in laboratory models [16][17][18] and in free-living wildlife [19][20][21][22]. However, the laboratory approach of comparing control and stressor-exposed animals under highly controlled conditions that lack ecological reality makes extrapolating results to the free-living organisms difficult.…”

Section: Introductionmentioning

confidence: 99%

It's what's on the inside that counts: stress physiology and the bacterial microbiome of a wild urban mammal

2019

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The microbiome's capacity to shape the host phenotype and its mutability underlie theorization that the microbiome might facilitate host acclimation to rapid environmental change. However, when environmental change occurs, it is unclear whether resultant microbiome restructuring is proximately driven by this changing external environment or by the host's physiological response to this change. We leveraged urbanization to compare the ability of host environment (urban or forest) versus multi-scale biological measures of host hypothalamic–pituitary–adrenal (HPA) axis physiology (neutrophil : lymphocyte ratio, faecal glucocorticoid metabolites, hair cortisol) to explain variation in the eastern grey squirrel ( Sciurus carolinensis ) faecal microbiome. Urban and forest squirrels differed across all three of the interpretations of HPA axis activity we measured. Direct consideration of these physiological measures better explained greater phylogenetic turnover between squirrels than environment. This pattern was strongly driven by trade-offs between bacteria which specialize on metabolizing digesta versus host-derived nutrient sources. Drawing on ecological theory to explain patterns in intestinal bacterial communities, we conclude that although environmental change can affect the microbiome, it might primarily do so indirectly by altering host physiology. We demonstrate that the inclusion and careful consideration of dynamic, rather than fixed (e.g. sex), dimensions of host physiology are essential for the study of host–microbe symbioses at the micro-evolutionary scale.

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Glucocorticoids modulate gastrointestinal microbiome in a wild bird

Cited by 99 publications

References 46 publications

Involvement of the Gut Microbiota and Barrier Function in Glucocorticoid-Induced Osteoporosis

Involvement of the Gut Microbiota and Barrier Function in Glucocorticoid-Induced Osteoporosis

Primate microbial endocrinology: An uncharted frontier

It's what's on the inside that counts: stress physiology and the bacterial microbiome of a wild urban mammal

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