Conceptual scientific and medical advances have led to a recent realization that there may be no single, one-size-fits-all diet and that differential human responses to dietary inputs may rather be driven by unique and quantifiable host and microbiome features. Integration of these person-specific host and microbiome readouts into actionable modules may complement traditional food measurement approaches in devising diets that are of benefit to the individual. Although many host-derived factors are hardwired and difficult to modulate, the microbiome may be more readily reshaped by environmental factors such as dietary exposures and is increasingly recognized to potentially impact human physiology by participating in digestion, the absorption of nutrients, shaping of the mucosal immune response and the synthesis or modulation of a plethora of potentially bioactive compounds. Thus, diet-induced microbiota alterations may be harnessed in order to induce changes in host physiology, including disease development and progression. However, major limitations in ‘big-data’ processing and analysis still limit our interpretive and translational capabilities concerning these person-specific host, microbiome and diet interactions. In this Review, we describe the latest advances in understanding diet–microbiota interactions, the individuality of gut microbiota composition and how this knowledge could be harnessed for personalized nutrition strategies to improve human health. In this Review, Kolodziejczyk, Zheng and Elinav describe the latest advances in understanding diet–microbiota interactions, the individuality of gut microbiota composition and how this knowledge could be harnessed for personalized nutrition strategies to improve human health.

Diet–microbiota interactions and personalized nutrition

One major limitation of microbial community marker gene sequencing is that it does not provide direct information on the functional composition of sampled communities. Here, we present PICRUSt2, which expands the capabilities of the original PICRUSt method to predict approximate functional potential of a community based on marker gene sequencing profiles. This updated method and implementation includes several improvements over the previous algorithm: an expanded database of gene families and reference genomes, a new approach now compatible with any OTU-picking or denoising algorithm, novel phenotype predictions, and novel fungal reference databases that enable predictions from 18S rRNA gene and internal transcribed spacer amplicon data. Upon evaluation, PICRUSt2 was more accurate than PICRUSt1 and other current approaches and also more flexible to allow the addition of custom reference databases. Last, we demonstrate the utility of PICRUSt2 by identifying potential disease-associated microbial functional signatures based on 16S rRNA gene sequencing of ileal biopsies collected from a cohort of human subjects with inflammatory bowel disease. PICRUSt2 is freely available at: https://github.com/picrust/picrust2.

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PICRUSt2: An improved and extensible approach for metagenome inference

One major limitation of microbial community marker gene sequencing is that it does not provide direct information on the functional composition of sampled communities. Here, we present PICRUSt2 (https://github.com/picrust/picrust2), which expands the capabilities of the original PICRUSt method1 to predict the functional potential of a community based on marker gene sequencing profiles. This updated method and implementation includes several improvements over the previous algorithm: an expanded database of gene families and reference genomes, a new approach now compatible with any OTU-picking or denoising algorithm, and novel phenotype predictions. Upon evaluation, PICRUSt2 was more accurate than PICRUSt1 and other current approaches overall. PICRUSt2 is also now more flexible and allows the addition of custom reference databases. We highlight these improvements and also important caveats regarding the use of predicted metagenomes, which are related to the inherent challenges of analyzing metagenome data in general.

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PICRUSt2: An improved and customizable approach for metagenome inference

Diet and host phylogeny drive the taxonomic and functional contents of the gut microbiome in mammals, yet it is unknown whether these patterns hold across all vertebrate lineages. Here, we assessed gut microbiomes from ∼900 vertebrate species, including 315 mammals and 491 birds, assessing contributions of diet, phylogeny, and physiology to structuring gut microbiomes. In most nonflying mammals, strong correlations exist between microbial community similarity, host diet, and host phylogenetic distance up to the host order level. In birds, by contrast, gut microbiomes are only very weakly correlated to diet or host phylogeny. Furthermore, while most microbes resident in mammalian guts are present in only a restricted taxonomic range of hosts, most microbes recovered from birds show little evidence of host specificity. Notably, among the mammals, bats host especially bird-like gut microbiomes, with little evidence for correlation to host diet or phylogeny. This suggests that host-gut microbiome phylosymbiosis depends on factors convergently absent in birds and bats, potentially associated with physiological adaptations to flight. Our findings expose major variations in the behavior of these important symbioses in endothermic vertebrates and may signal fundamental evolutionary shifts in the cost/benefit framework of the gut microbiome.IMPORTANCE In this comprehensive survey of microbiomes of >900 species, including 315 mammals and 491 birds, we find a striking convergence of the microbiomes of birds and animals that fly. In nonflying mammals, diet and short-term evolutionary relatedness drive the microbiome, and many microbial species are specific to a particular kind of mammal, but flying mammals and birds break this pattern with many microbes shared across different species, with little correlation either with diet or with relatedness of the hosts. This finding suggests that adaptation to flight breaks long-held relationships between hosts and their microbes.

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Comparative Analyses of Vertebrate Gut Microbiomes Reveal Convergence between Birds and Bats

The host-associated core microbiome was originally coined to refer to common groups of microbes or genes that were likely to be particularly important for host biological function. However, the term has evolved to encompass variable definitions across studies, often identifying key microbes with respect to their spatial distribution, temporal stability or ecological influence, as well as their contribution to host function and fitness. A major barrier to reaching a consensus over how to define the core microbiome and its relevance to biological, ecological and evolutionary theory is a lack of precise terminology and associated definitions, as well the persistent association of the core microbiome with host function. Common, temporal and ecological core microbiomes can together generate insights into ecological processes that act independently of host function, while functional and host-adapted cores distinguish between facultative and near-obligate symbionts that differ in their effects on host fitness. This commentary summarizes five broad definitions of the core microbiome that have been applied across the literature, highlighting their strengths and limitations for advancing our understanding of host-microbe systems, noting where they are likely to overlap, and discussing their potential relevance to host function and fitness. No one definition of the core microbiome is likely to capture the range of key microbes across a host population. Applied together, they have the potential to reveal different layers of microbial organization from which we can begin to understand the ecological and evolutionary processes that govern host-microbe interactions.

https://besjournals.onlinelibrary.wiley.com/doi/epdf/10.1111/1365-2656.13229

Applying the core microbiome to understand host–microbe systems

Over the past decade several studies have reported that the gut microbiomes of mammals with similar dietary niches exhibit similar compositional and functional traits. However, these studies rely heavily on samples from captive individuals and often confound host phylogeny, gut morphology, and diet. To more explicitly test the influence of host dietary niche on the mammalian gut microbiome we use 16S rRNA gene amplicon sequencing and shotgun metagenomics to compare the gut microbiota of 18 species of wild non-human primates classified as either folivores or closely related non-folivores, evenly distributed throughout the primate order and representing a range of gut morphological specializations. While folivory results in some convergent microbial traits, collectively we show that the influence of host phylogeny on both gut microbial composition and function is much stronger than that of host dietary niche. This pattern does not result from differences in host geographic location or actual dietary intake at the time of sampling, but instead appears to result from differences in host physiology. These findings indicate that mammalian gut microbiome plasticity in response to dietary shifts over both the lifespan of an individual host and the evolutionary history of a given host species is constrained by host physiological evolution. Therefore, the gut microbiome cannot be considered separately from host physiology when describing host nutritional strategies and the emergence of host dietary niches.

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Evolutionary trends in host physiology outweigh dietary niche in structuring primate gut microbiomes.

Comparative data from non-human primates provide insight into the processes that shaped the evolution of the human gut microbiome and highlight microbiome traits that differentiate humans from other primates. Here, in an effort to improve our understanding of the human microbiome, we compare gut microbiome composition and functional potential in 14 populations of humans from ten nations and 18 species of wild, non-human primates. Contrary to expectations from host phylogenetics, we find that human gut microbiome composition and functional potential are more similar to those of cercopithecines, a subfamily of Old World monkey, particularly baboons, than to those of African apes. Additionally, our data reveal more inter-individual variation in gut microbiome functional potential within the human species than across other primate species, suggesting that the human gut microbiome may exhibit more plasticity in response to environmental variation compared to that of other primates. Given similarities of ancestral human habitats and dietary strategies to those of baboons, these findings suggest that convergent ecologies shaped the gut microbiomes of both humans and cercopithecines, perhaps through environmental exposure to microbes, diet, and/or associated physiological adaptations. Increased inter-individual variation in the human microbiome may be associated with human dietary diversity or the ability of humans to inhabit novel environments. Overall, these findings show that diet, ecology, and physiological adaptations are more important than host-microbe co-diversification in shaping the human microbiome, providing a key foundation for comparative analyses of the role of the microbiome in human biology and health.

https://academicworks.cuny.edu/cgi/viewcontent.cgi?article=1376&context=qc_pubs

Gillian A. O. Britton

Papers

Evolutionary trends in host physiology outweigh dietary niche in structuring primate gut microbiomes.

Convergence of human and Old World monkey gut microbiomes demonstrates the importance of human ecology over phylogeny.