Diet and feeding pattern modulate diurnal dynamics of the ileal microbiome and transcriptome

Machado, Ana Carolina Dantas; Brown, Steven D.; Lingaraju, Amulya; Sivaganesh, Vignesh; Martino, Cameron; Chaix, Amandine; Zhao, Peng; Pinto-Duarte, António; Chang, Max W.; Richter, R. Alexander; Saghatelian, Alan; Saltiel, Alan R.; Knight, Rob; Panda, Satchidananda; Zarrinpar, Amir

doi:10.1016/j.celrep.2022.111008

Cited by 53 publications

(37 citation statements)

References 67 publications

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“…A targeted literature review followed by extensive correspondence, led to the acquisition of five previously published datasets in a form suitable for re-analysis ( Fig S1D ) 11,13,27–29 . In addition, we included a recently published dataset from the same mice in one of our circadian studies 13,30 . We also included analysis from an unpublished study that is unique in that it includes two circadian collections over the course of a single experiment.…”

Section: Resultsmentioning

confidence: 99%

“…Though the microbiome of the large and small intestine are quite different 33 , the diurnal dynamics of the latter has only recently been characterized 11,28,30 . We hypothesized that the dynamic response to changes in diet are not the same between gastrointestinal regions.…”

Section: Resultsmentioning

confidence: 99%

“…Moreover, the Zarrinpar, et al study (used for the analysis presented in Fig 2) also had 16S rRNA amplicon sequencing from the ileum of the same mice that was recently published 30 . Similar to the Leone, et al study, these results generally revealed different daily patterns in the ileum ( Fig S4 ) than in the cecum ( Fig 2 ).…”

Section: Resultsmentioning

confidence: 99%

“…For both regions, rarefaction was set to 1,000 reads to control for sequencing effort. Please see source paper for additional details 13,30 .…”

Section: Methodsmentioning

confidence: 99%

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Time of Sample Collection Critical for Microbiome Replicability

Allaband

Lingaraju

Ramos

et al. 2022

Preprint

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Although many aspects of microbiome studies have been standardized to improve experimental replicability, none account for how the daily diurnal fluctuations in the gut lumen cause dynamic changes in 16S amplicon sequencing. Here we show that sample collection time affects the conclusions drawn from microbiome studies and are larger than the effect size of a daily experimental intervention or dietary changes. The timing of divergence of the microbiome composition between experimental and control groups are unique to each experiment. Sample collection times as short as only four hours apart lead to vastly different conclusions. Lack of consistency in the time of sample collection may explain poor cross-study replicability in microbiome research. Without looking at other data, the impact on other fields is unknown but potentially significant.

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Section: Resultsmentioning

confidence: 99%

Section: Resultsmentioning

confidence: 99%

Section: Resultsmentioning

confidence: 99%

“…For both regions, rarefaction was set to 1,000 reads to control for sequencing effort. Please see source paper for additional details 13,30 .…”

Section: Methodsmentioning

confidence: 99%

See 2 more Smart Citations

Time of Sample Collection Critical for Microbiome Replicability

Allaband

Lingaraju

Ramos

et al. 2022

Preprint

Self Cite

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“…The temporal dimension of this relationship warrants serious examination, especially given the ubiquity of circadian rhythms in animal hosts [ 3 – 6 ]. At the very least, because most animal hosts (including humans) eat on a daily schedule, the environment experienced by gut microbiota undergoes approximately 24 h transformation in nutrient availability [ 5 , 7 ]. A gut bacterium that can anticipate the arrival of fresh nutrients might more readily metabolize those resources and thus gain the upper hand over time-ignorant competitors.…”

Section: Introductionmentioning

confidence: 99%

Host circadian behaviors exert only weak selective pressure on the gut microbiome under stable conditions but are critical for recovery from antibiotic treatment

et al. 2022

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The circadian rhythms of hosts dictate an approximately 24 h transformation in the environment experienced by their gut microbiome. The consequences of this cyclic environment on the intestinal microbiota are barely understood and are likely to have medical ramifications. Can daily rhythmicity in the gut act as a selective pressure that shapes the microbial community? Moreover, given that several bacterial species have been reported to exhibit circadian rhythms themselves, we test here whether a rhythmic environment is a selective pressure that favors clock-harboring bacteria that can anticipate and prepare for consistent daily changes in the environment. We observed that the daily rhythmicity of the mouse gut environment is a stabilizing influence that facilitates microbiotal recovery from antibiotic perturbation. The composition of the microbiome recovers to pretreatment conditions when exposed to consistent daily rhythmicity, whereas in hosts whose feeding and activity patterns are temporally disrupted, microbiotal recovery is incomplete and allows potentially unhealthy opportunists to exploit the temporal disarray. Unexpectedly, we found that in the absence of antibiotic perturbation, the gut microbiome is stable to rhythmic versus disrupted feeding and activity patterns. Comparison of our results with those of other studies reveals an intriguing correlation that a stable microbiome may be resilient to one perturbation alone (e.g., disruption of the daily timing of host behavior and feeding), but not to multiple perturbations in combination. However, after a perturbation of the stable microbiome, a regular daily pattern of host behavior/feeding appears to be essential for the microbiome to recover to the original steady state. Given the inconsistency of daily rhythms in modern human life (e.g., shiftwork, social jet-lag, irregular eating habits), these results emphasize the importance of consistent daily rhythmicity to optimal health not only directly to the host, but also indirectly by preserving the host’s microbiome in the face of perturbations.

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The Role of Diet and Gut Microbiota Interactions in Metabolic Homeostasis

Guan

Liu

2023

Advanced Biology

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Diet is a pivotal determinant in shaping the structure and function of resident microorganisms in the gut through different food components, nutritive proportion, and calories. The effects of diet on host metabolism and physiology can be mediated through the gut microbiota. Gut microbiota‐derived metabolites have been shown to regulate glucose and lipid metabolism, energy consumption, and the immune system. On the other hand, emerging evidence indicates that baseline gut microbiota could predict the efficacy of diet intervention, highlighting gut microbiota can be harnessed as a biomarker in personalized nutrition. In this review, the alterations of gut microbiota in different dietary components and dietary patterns, and the potential mechanisms in the diet‐microbiota crosstalk are summarized to understand the interactions of diet and gut microbiota on the impact of metabolic homeostasis.

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Diet and feeding pattern modulate diurnal dynamics of the ileal microbiome and transcriptome

Cited by 53 publications

References 67 publications

Time of Sample Collection Critical for Microbiome Replicability

Time of Sample Collection Critical for Microbiome Replicability

Host circadian behaviors exert only weak selective pressure on the gut microbiome under stable conditions but are critical for recovery from antibiotic treatment

The Role of Diet and Gut Microbiota Interactions in Metabolic Homeostasis

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