Host specificity of the gut microbiome Mallott, Elizabeth K; Amato, Katherine R
Nature reviews. Microbiology,
10/2021, Letnik:
19, Številka:
10
Journal Article
Recenzirano
Developing general principles of host-microorganism interactions necessitates a robust understanding of the eco-evolutionary processes that structure microbiota. Phylosymbiosis, or patterns of ...microbiome composition that can be predicted by host phylogeny, is a unique framework for interrogating these processes. Identifying the contexts in which phylosymbiosis does and does not occur facilitates an evaluation of the relative importance of different ecological processes in shaping the microbial community. In this Review, we summarize the prevalence of phylosymbiosis across the animal kingdom on the basis of the current literature and explore the microbial community assembly processes and related host traits that contribute to phylosymbiosis. We find that phylosymbiosis is less prevalent in taxonomically richer microbiomes and hypothesize that this pattern is a result of increased stochasticity in the assembly of complex microbial communities. We also note that despite hosting rich microbiomes, mammals commonly exhibit phylosymbiosis. We hypothesize that this pattern is a result of a unique combination of mammalian traits, including viviparous birth, lactation and the co-evolution of haemochorial placentas and the eutherian immune system, which compound to ensure deterministic microbial community assembly. Examining both the individual and the combined importance of these traits in driving phylosymbiosis provides a new framework for research in this area moving forward.
Industrialized diets that incorporate processed foods and are often high in simple sugars and fats and low in fiber have myriad health impacts, many of which may operate via impacts on the gut ...microbiota. Examining how these diets affect the gut microbiota can be challenging given that lab animal models experience altered environmental contexts, and human studies include a suite of co-varying cultural and environmental factors that are likely to shape the gut microbiota alongside diet. To complement these approaches, we compare the microbiomes of wild populations of olive baboons (Papio anubis) with differential access to human trash high in processed foods, simple sugars, and fats in Rwanda's Akagera National Park. Baboons are a good model system since their microbiomes are compositionally similar to those of humans. Additionally, this population inhabits a common environment with different social groups consuming qualitatively different amounts of human trash, limiting variation in non-dietary factors. Using 16S rRNA gene amplicon sequencing we find that baboons with unlimited access to human trash have reduced microbial alpha diversity and reduced relative abundances of fiber-degrading taxa such as Ruminococcaceae, Prevotellaceae, and Lachnospiraceae. In contrast, baboons with limited access to human trash have a microbiome more similar to that of baboons with no access to human trash. Our results suggest that while a human-influenced diet high in processed foods, simple sugars, and fats is sufficient to alter the microbiome in wild baboons, there is a minimum threshold of dietary alteration that must occur before the microbiome is substantially altered. We recommend that data from wild primate populations such as these be used to complement ongoing research on diet-microbiome-health interactions in humans and lab animal models.
Recent studies increasingly note the effect of captivity or the built environment on the microbiome of humans and other animals. As symbiotic microbes are essential to many aspects of biology (e.g., ...digestive and immune functions), it is important to understand how lifestyle differences can impact the microbiome, and, consequently, the health of hosts. Animals living in captivity experience a range of changes that may influence the gut bacteria, such as diet changes, treatments, and reduced contact with other individuals, species and variable environmental substrates that act as sources of bacterial diversity. Thus far, initial results from previous studies point to a pattern of decreased bacterial diversity in captive animals. However, these studies are relatively limited in the scope of species that have been examined. Here we present a dataset that includes paired wild and captive samples from mammalian taxa across six Orders to investigate generalizable patterns of the effects captivity on mammalian gut bacteria. In comparing the wild to the captive condition, our results indicate that alpha diversity of the gut bacteria remains consistent in some mammalian hosts (bovids, giraffes, anteaters, and aardvarks), declines in the captive condition in some hosts (canids, primates, and equids), and increases in the captive condition in one host taxon (rhinoceros). Differences in gut bacterial beta diversity between the captive and wild state were observed for most of the taxa surveyed, except the even-toed ungulates (bovids and giraffes). Additionally, beta diversity variation was also strongly influenced by host taxonomic group, diet type, and gut fermentation physiology. Bacterial taxa that demonstrated larger shifts in relative abundance between the captive and wild states included members of the Firmicutes and Bacteroidetes. Overall, the patterns that we observe will inform a range of disciplines from veterinary practice to captive breeding efforts for biological conservation. Furthermore, bacterial taxa that persist in the captive state provide unique insight into symbiotic relationships with the host.
The human microbiome in evolution Davenport, Emily R; Sanders, Jon G; Song, Se Jin ...
BMC biology,
12/2017, Letnik:
15, Številka:
1
Journal Article
Recenzirano
Odprti dostop
The trillions of microbes living in the gut-the gut microbiota-play an important role in human biology and disease. While much has been done to explore its diversity, a full understanding of our ...microbiomes demands an evolutionary perspective. In this review, we compare microbiomes from human populations, placing them in the context of microbes from humanity's near and distant animal relatives. We discuss potential mechanisms to generate host-specific microbiome configurations and the consequences of disrupting those configurations. Finally, we propose that this broader phylogenetic perspective is useful for understanding the mechanisms underlying human-microbiome interactions.
The gastrointestinal (GI) microbiome contributes significantly to host nutrition and health. However, relationships involving GI microbes, their hosts and host macrohabitats remain to be established. ...Here, we define clear patterns of variation in the GI microbiomes of six groups of Mexican black howler monkeys (Alouatta pigra) occupying a gradation of habitats including a continuous evergreen rainforest, an evergreen rainforest fragment, a continuous semi-deciduous forest and captivity. High throughput microbial 16S ribosomal RNA gene sequencing indicated that diversity, richness and composition of howler GI microbiomes varied with host habitat in relation to diet. Howlers occupying suboptimal habitats consumed less diverse diets and correspondingly had less diverse gut microbiomes. Quantitative real-time PCR also revealed a reduction in the number of genes related to butyrate production and hydrogen metabolism in the microbiomes of howlers occupying suboptimal habitats, which may impact host health.
Host genetics influence the gut microbiome Cortes-Ortiz, Liliana; Amato, Katherine R.
Science (American Association for the Advancement of Science),
07/2021, Letnik:
373, Številka:
6551
Journal Article
Recenzirano
Longitudinal data from nonhuman primates reveal widespread gut microbiome heritability
The influences of the microbiota on host physiology are so pervasive that the microbiota has been hypothesized ...to play a critical role in host evolution by shaping key host phenotypes (
1
). However, to contribute to host evolution, traits must be transmitted across generations. One way to assess whether some or all microbes are influenced by the genetic composition of the host, and therefore conserved across generations, is by measuring heritability. Host species–specific patterns in the composition of the microbiome—the genetic content of the microbiota—suggest there is some degree of heritability in the microbiota (
2
). However, studies evaluating variation in the microbiota and host genetics within a single host species have generally reported low heritability for a small proportion of microbial taxa (
3
). On page 181 of this issue, Grieneisen
et al.
(
4
) reject this common conclusion by demonstrating that most gut microbiota traits in wild baboons exhibit some degree of heritability.
Adaptive shifts in gut microbiome composition are one route by which animals adapt to seasonal changes in food availability and diet. However, outside of dietary shifts, other potential environmental ...drivers of gut microbial composition have rarely been investigated, particularly in organisms living in their natural environments.
Here, we generated the largest wild nonhuman primate gut microbiome dataset to date to identify the environmental drivers of gut microbial diversity and function in 758 samples collected from wild Ethiopian geladas (Theropithecus gelada). Because geladas live in a cold, high-altitude environment and have a low-quality grass-based diet, they face extreme thermoregulatory and energetic constraints. We tested how proxies of food availability (rainfall) and thermoregulatory stress (temperature) predicted gut microbiome composition of geladas. The gelada gut microbiome composition covaried with rainfall and temperature in a pattern that suggests distinct responses to dietary and thermoregulatory challenges. Microbial changes were driven by differences in the main components of the diet across seasons: in rainier periods, the gut was dominated by cellulolytic/fermentative bacteria that specialized in digesting grass, while during dry periods the gut was dominated by bacteria that break down starches found in underground plant parts. Temperature had a comparatively smaller, but detectable, effect on the gut microbiome. During cold and dry periods, bacterial genes involved in energy, amino acid, and lipid metabolism increased, suggesting a stimulation of fermentation activity in the gut when thermoregulatory and nutritional stress co-occurred, and potentially helping geladas to maintain energy balance during challenging periods.
Together, these results shed light on the extent to which gut microbiota plasticity provides dietary and metabolic flexibility to the host, and might be a key factor to thriving in changing environments. On a longer evolutionary timescale, such metabolic flexibility provided by the gut microbiome may have also allowed members of Theropithecus to adopt a specialized diet, and colonize new high-altitude grassland habitats in East Africa. Video abstract.
Human evolution has been punctuated by climate anomalies, structuring environments, deadly infections, and altering landscapes. How well humans adapted to these new circumstances had direct effects ...on fitness and survival. Here, how the gut microbiome could have contributed to human evolutionary success through contributions to host nutritional buffering and infectious disease resistance is reviewed. How changes in human genetics, diet, disease exposure, and social environments almost certainly altered microbial community composition is also explored. Emerging research points to the microbiome as a key player in host responses to environmental change. Therefore, the reciprocal interactions between humans and their microbes are likely to have shaped human patterns of local adaptation throughout our shared evolutionary history. Recent alterations in human lifestyle, however, are altering human microbiomes in unprecedented ways. The consequences of interrupted host–microbe relationships for human adaptive potential in the future are unknown.
Humans live in a microbial world including microbial communities living on the body mucosal surfaces. This microbiome provides essential metabolic activities, and has played a key role in adaptation to nutritional and climatic changes during human evolution. This microbiome protects humans against pathogens, but can affect or modulate the expressivity of susceptibility to inflammatory and metabolic diseases.
For most mammals, including nonhuman primates, diet composition varies temporally in response to differences in food availability. Because diet influences gut microbiota composition, it is likely ...that the gut microbiota of wild mammals varies in response to seasonal changes in feeding patterns. Such variation may affect host digestive efficiency and, ultimately, host nutrition. In this study, we investigate the temporal variation in diet and gut microbiota composition and function in two groups (N = 13 individuals) of wild Mexican black howler monkeys (Alouatta pigra) over a 10-month period in Palenque National Park, Mexico. Temporal changes in the relative abundances of individual bacterial taxa were strongly correlated with changes in host diet. For example, the relative abundance of Ruminococcaceae was highest during periods when energy intake was lowest, and the relative abundance of Butyricicoccus was highest when young leaves and unripe fruit accounted for 68 % of the diet. Additionally, the howlers exhibited increased microbial production of energy during periods of reduced energy intake from food sources. Because we observed few changes in howler activity and ranging patterns during the course of our study, we propose that shifts in the composition and activity of the gut microbiota provided additional energy and nutrients to compensate for changes in diet. Energy and nutrient production by the gut microbiota appears to provide an effective buffer against seasonal fluctuations in energy and nutrient intake for these primates and is likely to have a similar function in other mammal species.
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