‘You are what you eat.’
Written by Lieselotte Peeters
Can bat gut microbiomes provide proof for this generalized truth?
Host-microbe interactions play a pivotal role in the ecological and evolutionary history of life on Earth. We could even go as far as calling them shaping factors, as many animals have adapted to their (current) diets through a combination of physiological adaptations and nutritional pathways encoded by the gut microbiome. Therefore it is not surprising that the residing gut bacteria in many vertebrate groups reflect their host’s evolutionary history and dietary strategies; this phenomenon is called phylosymbiosis. However, while many recent studies report patterns of phylosymbiosis, few of them examine the functional contributions of these microbes to their host’s dietary habits. This makes it impossible to properly assess the true impact of microbial symbionts on host fitness and evolution.
A group of scientists led by Melissa R. Ingala hypothesized that microbiome functions should vary among mammals with different diets. To test this hypothesis they examined the predicted nutritional pathways (i.e. from food to energy source used by the host) of 545 gut microbiome samples from over 500 bats (13 families, 42 genera, 60 species). Now bats are an ideal model system for this kind of study because they adhere to very specific diets depending on the bat species. In addition they also inhabit different parts of the world, which allows us to examine the mechanisms that have led geographically separated bat species to adapt to similar diets.
The nutritional pathways examined in this study resulted from the microbial and functional profiling of bat guano samples — guano is just a scientific word for dried bat poop. In short, the scientist extracted microbial DNA from these bat guano samples, which they then analyzed using bioinformatic tools to 1) examine the bacterial community composition (16S rRNA gene profiling) and 2) the functions these bacteria fulfill to accommodate their host’s nutritional needs (PICRUSt2). The team uncovered 448 nutritional pathways (448 MetaCyc pathways), which they tested for enrichment across five bat diet types: frugivore (fruit-eating), insectivore (insect-eating), omnivore (all-eating), carnivore (fish and/or meat-eating) and sanguivore (blood-eating).
They found that the predicted microbiota functions were significantly differentiated by host taxonomy ànd — you guessed it — host diet. The question is of course how much diet contributes to this observed difference. So Ingala et al. compared the predicted microbiome functions of the different dietary groups to see if they were significantly different or not. Following their hypothesis, you’d expect that the most specialized, or restricted, diet would be most distinguished. However, it were the carnivorous bats’ and insectivorous bats’ microbiome functions that turned out to be most distinguishable from all other groups. The hyper-specialized vampire bats’ microbiome functions were distinctive, but they could not be told apart from the omnivorous bats’. The latter not surprisingly displayed some overlap with other dietary groups, but turned out to be distinct from strict insectivores and carnivores (Fig. 2).
When the research group compared the microbiome functions in terms of primary animal-feeding (animalivorous) versus primary plant-feeding (i.e. herbivorous), they found 37 differentially enriched nutritional pathways. Of note, the pathways enriched in herbivorous bats were associated with the production of essential amino acids. These amino acids cannot be synthesized de novo by the host, so they must either be present in the diet or produced through microbial metabolism and absorbed through the gut. This poses a nutritional challenge for obligate frugivores as fruits are deficient in proteins compared to for example insects.
However, the metabolic contributions of symbiotic microbes can help supplement these essential amino acids. This phenomenon is already shown in a mouse-model fed on a protein-deficient diet. Other functions enriched in this dietary group were related to carbohydrate degradation (e.g. glycogen and starch) and biosynthesis of B-vitamin folate. This is expected as most fruits are primarily made up of water and simple carbohydrates. Animalivorous bats displayed a more generalized arsenal of microbial functions. Within this dietary group, the vampire bat stands out with a gut microbiota that is characterized by the presence of Peptostreptococcaceae. This bacterial family has the rare ability to ferment amino acids, a metabolic process that comes in very handy given the fact that blood contains a lot of proteins. Just to give you an idea, blood is 78% liquid, but its solid cellular phase contains 93% proteins. This suggests that gut microbes can fulfill or supplement critical nutritional pathways, such as essential amino acid synthesis, fatty acid biosynthesis, generation of cofactors and vitamins to provide their host with proper nutrition (Fig. 3).
So Ingala et al. managed to show a clear link between bacterial metabolism and host diet, which translates into differently enriched nutritional pathways. But how strong is this link? Can we determine host diet based on the microbiome function composition? Attempting to answer this question, Ingala et al. conducted a specific analysis, called the Random Forest analysis, to test if they could classify bats into dietary groups as well as host family and genus based on their gut microbiomes. The model managed to predict host diet based on the gut microbiomes (accuracy rates between 80 and 85%). However, it mostly succeeded at identifying primarily animalivorous bats and performed substantially worse for the plant-feeding and omnivorous animals. In addition, the model couldn’t predict the host family or genus based on microbiome functions alone. Thus, it seems that while microbiome functions may be characteristic of host diet, they are not robust enough to discriminate among related hosts.
Taken together Ingala et al. supplied results that indicate that bats may rely on their gut symbionts to fulfill essential metabolic roles that align with host dietary ecology. The strength of this host-microbe interaction probably depends on the degree of host dietary specialization (e.g. strictly frugivorous versus occasionally insectivorous). So yes, there seems to be a scientific ground for the all too familiar ‘you are what you eat’-phrase. However, a few key questions remain: 1) How specific must this host diet be before we can distinguish it from others based on microbiome functions? 2) What is the precise impact of host-microbe interactions on host diversity? and 3) Are these microbiome functions subjected to selective pressure? I am sure that future studies will provide compelling insights into this fascinating topic.
Link to the original post: Ingala, M.R., Simmons, N.B., Dunbar, M. et al. You are more than what you eat: potentially adaptive enrichment of microbiome functions across bat dietary niches. anim microbiome 3, 82 (2021). https://doi.org/10.1186/s42523-021-00139-8
Featured image: Featured image created by author using BioRender.com
Originally published at https://micro-bites.org on March 14, 2022.
