Synchrony and idiosyncrasy in the gut microbiome of wild baboons

Björk, Johannes; Dasari, Mauna; Roche, Kim; Grieneisen, Laura; Gould, Trevor; Grenier, Jean; Yotova, Vania; Gottel, Neil; Jansen, David; Gesquiere, Laurence R.; Gordon, Jacob B.; Learn, Niki H.; Wango, Tim L.; Mututua, Raphael S.; Warutere, J. Kinyua; Siodi, L.I.; Mukherjee, Sayan; Barreiro, Luis B.; Alberts, Susan C.; Gilbert, Jack A.; Tung, Jenny; Blekhman, Ran; Archie, Elizabeth A.

doi:10.1038/s41559-022-01773-4

Cited by 25 publications

(57 citation statements)

References 61 publications

(151 reference statements)

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“…Our findings of weak long-term contributions of individual identity to gut microbial composition, an exponential decay in microbiota similarity within individuals over time, and increases in taxon repeatability with age, all align closely with those found in a decade long study of baboons [8,25], suggesting that such dynamics may be consistent across host species. These patterns in longitudinal dynamics may resolve the conflicting reports of the major drivers of gut microbiota dynamics across different species, with different findings being due to variable sampling intervals and designs rather than inherent differences among species.…”

Section: Discussionsupporting

confidence: 86%

“…Nevertheless, this does not preclude the possibility of differences in gut microbiota stability and associated drivers between host species. For example, individual host traits such as age, sex and social dominance rank generate individualized microbial signatures that are stable over short time frames in baboons [25], yet these traits do not have a strong stabilizing effect in meerkats [9].…”

Section: Discussionmentioning

confidence: 99%

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Gut microbiota individuality is contingent on temporal scale and age in wild meerkats

et al. 2022

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Inter-individual differences in gut microbiota composition are hypothesized to generate variation in host fitness—a premise for the evolution of host–gut microbe symbioses. However, recent evidence suggests that gut microbial communities are highly dynamic, challenging the notion that individuals harbour unique gut microbial phenotypes. Leveraging a long-term dataset of wild meerkats, we reconcile these concepts by demonstrating that the relative importance of identity for shaping gut microbiota phenotypes depends on the temporal scale. Across meerkat lifespan, year-to-year variation overshadowed the effects of identity and social group in predicting gut microbiota composition, with identity explaining on average less than 2% of variation. However, identity was the strongest predictor of microbial phenotypes over short sampling intervals (less than two months), predicting on average 20% of variation. The effect of identity was also dependent on meerkat age, with the gut microbiota becoming more individualized and stable as meerkats aged. Nevertheless, while the predictive power of identity was negligible after two months, gut microbiota composition remained weakly individualized compared to that of other meerkats for up to 1 year. These findings illuminate the degree to which individualized gut microbial signatures can be expected, with important implications for the time frames over which gut microbial phenotypes may mediate host physiology, behaviour and fitness in natural populations.

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Section: Discussionsupporting

confidence: 86%

Section: Discussionmentioning

confidence: 99%

Gut microbiota individuality is contingent on temporal scale and age in wild meerkats

et al. 2022

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“…Another recent study examined the gut microbiomes of baboons ( Papio spp.) over a 14-year period and concluded that although all gut microbiomes exhibited cyclical seasonal shifts in composition, microbiome dynamics across baboons were only weakly synchronized (14). Instead, baboons exhibited largely individualized gut microbiomes over their lifespans, despite their shared diets, environments, and opportunities for between-host microbial dispersal (14).…”

Section: Introductionmentioning

confidence: 99%

“…over a 14-year period and concluded that although all gut microbiomes exhibited cyclical seasonal shifts in composition, microbiome dynamics across baboons were only weakly synchronized (14). Instead, baboons exhibited largely individualized gut microbiomes over their lifespans, despite their shared diets, environments, and opportunities for between-host microbial dispersal (14). Findings from the two studies suggest that gut microbiome dynamics may be species-specific and influenced by host behavior, temporal factors, and habitat characteristics.…”

Section: Introductionmentioning

confidence: 99%

Taxonomic, genomic, and functional variation in the gut microbiomes of wild spotted hyenas across two decades of study

Rojas

Holekamp

Viladomat

et al. 2022

Preprint

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The gut microbiome provides vital functions for mammalian hosts, yet research on the variability and function of the microbiome across adult lifespans and multiple generations is limited in large mammalian carnivores. Here we use 16S rRNA gene and metagenomic sequencing to profile the taxonomic composition, genomic diversity, and metabolic function of the gut microbiome of 12 wild spotted hyenas (Crocuta crocuta) residing in the Masai Mara National Reserve, Kenya over a 23-year period spanning three generations. We determined the extent to which host factors predict variation in the gut microbiome and identify the core microbes present in the guts of hyenas. We also investigate novel genomic diversity in the mammalian gut by reporting the first metagenome-assembled genomes (MAGs) for hyenas. We found that gut microbiome taxonomic composition was highly variable across the two decades of sampling, but despite this, a core set of 22 bacterial genera and 19 amplicon sequence variants were identified. The strongest predictors of microbiome alpha and beta-diversity were host identity and age, suggesting that hyenas possess individualized microbiomes, and that these may change with age during adulthood. Gut microbiome functional profiles were also individual-specific, and were moderately correlated with antelope prey abundance, indicating that the functions of the gut microbiome vary with host diet. We recovered 149 high-quality MAGs from the hyena gut, spanning 25 bacterial orders and 51 genera. Some MAGs were classified as taxa previously reported for other carnivores, but many were novel and lacked species level matches to genomes in existing reference databases, greatly greatly expanding the microbial genome repertoire known for hyenas, carnivores and wild mammals in general.

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“…We also tested whether pairs of ASVs with especially consistent between-host correlation patterns tend to show large seasonal changes in CLR abundance. To do so, we focused on 13 families that exhibit significant seasonal changes in CLR abundance, based on a previous analysis of the same data set[42]. While ASV pairs in which one member belongs to one of these significantly "seasonal" families are slightly more universal, this effect is small (difference of 0.026, p<0.0001 vs. pairs where 0 or 1 partner were "seasonal"; Fig.S9).…”

mentioning

confidence: 99%

Universal gut microbial relationships in the gut microbiome of wild baboons

Roche

Björk

Dasari

et al. 2022

Preprint

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Ecological relationships between bacteria mediate the services that gut microbiomes provide to their hosts. Knowing the overall direction and strength of these relationships within hosts, and their generalizability across hosts, is essential to learn how microbial ecology scales up to affect microbiome assembly, dynamics, and host health. Here we gain insight into these patterns by inferring thousands of correlations in bacterial abundance between pairs of gut microbiome taxa from extensive time series data, consisting of 5,534 microbiome profiles from 56 wild baboon hosts over a 13-year period. We model these time series using a statistically robust, multinomial logistic-normal modeling framework and test the degree to which bacterial abundance correlations are consistent across hosts (i.e., "univeral") or individualized to each host. We also compare these patterns to two publicly available human data sets. We find that baboon gut microbial relationships are largely universal: correlation patterns within each baboon host reflect a mixture of idiosyncratic and shared patterns, but the shared pattern dominates by almost 2-fold. Surprisingly, the strongest and most consistently correlated bacterial pairs across hosts were overwhelmingly positively correlated and typically belonged to the same family - a 3-fold enrichment compared to pairs drawn from the data set as a whole. The bias towards universal, positive bacterial correlations was also apparent in monthly samples from human infants, and bacterial families that had universal relationships in baboons also tended to be universal in human infants. Together, our results advance our understanding of the relationships that shape gut microbial ecosystems, with implications for microbiome personalization, community assembly and stability, and the feasibility of microbiome interventions to improve host health.

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Synchrony and idiosyncrasy in the gut microbiome of wild baboons

Cited by 25 publications

References 61 publications

Gut microbiota individuality is contingent on temporal scale and age in wild meerkats

Gut microbiota individuality is contingent on temporal scale and age in wild meerkats

Taxonomic, genomic, and functional variation in the gut microbiomes of wild spotted hyenas across two decades of study

Universal gut microbial relationships in the gut microbiome of wild baboons

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