Taxonomic Features and Comparison of the Gut Microbiome from Two Edible Fungus-Farming Termites (Macrotermes falciger, M. natalensis) Harvested in the Vhembe District of Limpopo, South Africa

Background Termites are an important food resource for many human populations around the world, and are a good supply of nutrients. The fungus-farming ‘higher’ termite members of Macrotermitinae are also consumed by modern great apes and are implicated as critical dietary resources for early hominins. While the chemical nutritional composition of edible termites is well known, their microbiomes are unexplored in the context of human health. Here we sequenced the V4 region of the 16S rRNA gene of gut microbiota extracted from the whole intestinal tract of two Macrotermes sp. soldiers collected from the Limpopo region of South Africa. Results Major and minor soldier subcastes of M. falciger exhibit consistent differences in taxonomic representation, and are variable in microbial presence and abundance patterns when compared to another edible but less preferred species, M. natalensis. Subcaste differences include alternate patterns in sulfate-reducing bacteria and methanogenic Euryarchaeota abundance, and differences in abundance between Alistipes and Ruminococcaceae. M. falciger minor soldiers and M. natalensissoldiers have similar microbial profiles, likely from close proximity to the termite worker castes, particularly during foraging and fungus garden cultivation. Compared with previously published termite and cockroach gut microbiome data, the taxonomic representation was generally split between termites that directly digest lignocellulose and humic substrates and those that consume a more distilled form of nutrition as with the omnivorous cockroaches and fungus-farming termites. Lastly, to determine if edible termites may point to a shared reservoir for rare bacterial taxa found in the gut microbiome of humans, we focused on the genus Treponema. The majority of Treponemasequences from edible termite gut microbiota most closely relate to species recovered from other termites or from environmental samples, except for one novel OTU strain, which clustered separately with Treponema found in hunter-gatherer human groups. Conclusions Macrotermes consumed by humans display special gut microbial arrangements that are atypical for a lignocellulose digesting invertebrate, but are instead suited to the simplified nutrition in the fungus-farmer diet. Our work brings to light the particular termite microbiome features that should be explored further as avenues in human health, agricultural sustainability, and evolutionary research

Biogeographic Study of Human Gut-Associated CrAssphage Suggests Impacts From Industrialization and Recent Expansion

CrAssphage (cross-assembly phage) is a bacteriophage that was first discovered in human gut metagenomic data. CrAssphage belongs to a diverse family of crAss-like bacteriophages thought to infect gut commensal bacteria belonging to Bacteroides species. However, not much is known about the biogeography of crAssphage and whether certain strains are associated with specific human populations. In this study, we screened publicly available human gut metagenomic data from 3,341 samples for the presence of crAssphage sensu stricto (NC_024711.1). We found that crAssphage prevalence is low in traditional, hunter-gatherer populations, such as the Hadza from Tanzania and Matses from Peru, as compared to industrialized, urban populations. Statistical comparisons showed no association of crAssphage prevalence with variables such as age, sex, body mass index, and health status of individuals. Phylogenetic analyses show that crAssphage strains reconstructed from the same individual over multiple time-points, cluster together. CrAssphage strains from individuals from the same study population do not always cluster together. Some evidence of clustering is seen at the level of broadly defined geographic regions, however, the relative positions of these clusters within the crAssphage phylogeny are not well-supported. We hypothesize that this lack of strong biogeographic structuring is suggestive of an expansion event within crAssphage. Using a Bayesian dating approach, we estimate that this expansion has occurred fairly recently. Overall, we determine that crAssphage presence is associated with an industrialized lifestyle and the absence of strong biogeographic structuring within global crAssphage strains is likely due to a recent population expansion within this bacteriophage.This study was supported by a grant from the National Institutes of Health (https://www.nih.gov/), NIH R01 GM089886, awarded to C.M.L., C.W., and K.S. Open Access fees paid for in whole or in part by the University of Oklahoma Libraries.Ye

Plasticity in the Human Gut Microbiome Defies Evolutionary Constraints

The gut microbiome of primates, including humans, is reported to closely follow host evolutionary history, with gut microbiome composition being specific to the genetic background of its primate host. However, the comparative models used to date have mainly included a limited set of closely related primates. To further understand the forces that shape the primate gut microbiome, with reference to human populations, we expanded the comparative analysis of variation among gut microbiome compositions and their primate hosts, including 9 different primate species and 4 human groups characterized by a diverse set of subsistence patterns (n = 448 samples). The results show that the taxonomic composition of the human gut microbiome, at the genus level, exhibits increased compositional plasticity. Specifically, we show unexpected similarities between African Old World monkeys that rely on eclectic foraging and human populations engaging in nonindustrial subsistence patterns; these similarities transcend host phylogenetic constraints. Thus, instead of following evolutionary trends that would make their microbiomes more similar to that of conspecifics or more phylogenetically similar apes, gut microbiome composition in humans from nonindustrial populations resembles that of generalist cercopithecine monkeys. We also document that wild cercopithecine monkeys with eclectic diets and humans following nonindustrial subsistence patterns harbor high gut microbiome diversity that is not only higher than that seen in humans engaging in industrialized lifestyles but also higher compared to wild primates that typically consume fiber-rich diets

Impact of Brief Roasting on Starch Gelatinization in Whole Foods and Implications for Plant Food nNutritional Ecology in Human Evolution

Cooking is an important technology for its capacity to increase food digestibility, particularly for plant foods, potentially playing a significant role in human evolution to increase nutritional acquisition. However, the contextual impetus for cooking is less well understood. One mode of cooking used by modern humans is to roast food directly in an open flame fire for very brief durations. This technique may be a behavioral analogue to that of early human ancestors. Here, we provide experimental data on starch gelatinization patterns in domesticated underground storage organs and starchy fruit as a result of brief fire roasting. We employed a count-based method using light-microscopy and a semi-quantitative photometric strategy to observe the kinetic process of gelatinization. We find that brief roasting over an open fire results in low levels of starch gelatinization. These findings suggest that brief roasting may not benefit a consumer through changes to starch structure alone

Biogeographic Study of Human Gut Associated CrAssphage Suggests Impacts from Industrialization and Recent Expansion

CrAssphage (cross-assembly phage) is a bacteriophage that was first discovered in human gut metagenomic data. CrAssphage belongs to a diverse family of crAss-like bacteriophages thought to infect gut commensal bacteria belonging to Bacteroides species. However, not much is known about the biogeography of crAssphage and whether certain strains are associated with specific human populations. In this study, we screened publicly available human gut metagenomic data from 3,341 samples for the presence of crAssphage sensu stricto (NC_024711.1). We found that crAssphage prevalence is low in traditional, hunter-gatherer populations, such as the Hadza from Tanzania and Matses from Peru, as compared to industrialized, urban populations. Statistical comparisons showed no association of crAssphage prevalence with variables such as age, sex, body mass index, and health status of individuals. Phylogenetic analyses show that crAssphage strains reconstructed from the same individual over multiple time-points, cluster together. CrAssphage strains from individuals from the same study population do not always cluster together. Some evidence of clustering is seen at the level of broadly defined geographic regions, however, the relative positions of these clusters within the crAssphage phylogeny are not well-supported. We hypothesize that this lack of strong biogeographic structuring is suggestive of a recent expansion event within crAssphage. Using a Bayesian dating approach, we estimate this expansion has occurred within the past 200 years. Overall, we determine that crAssphage presence is associated with an industrialized lifestyle. The absence of strong biogeographic structuring within global crAssphage strains is likely due to a recent population expansion within this bacteriophage

Variations in the post-weaning human gut metagenome profile as result of Bifidobacterium acquisition in the Western microbiome

Studies of the gut microbiome variation among human populations revealed the existence of robust compositional and functional layouts matching the three subsistence strategies that describe a trajectory of changes across our recent evolutionary history: hunting and gathering, rural agriculture, and urban post-industrialized agriculture. In particular, beside the overall reduction of ecosystem diversity, the gut microbiome of Western industrial populations is typically characterized by the loss of Treponema and the acquisition of Bifidobacterium as an abundant inhabitant of the post-weaning gut microbial ecosystem. In order to advance the hypothesis about the possible adaptive nature of this exchange, here we explore specific functional attributes that correspond to the mutually exclusive presence of Treponema and Bifidobacterium using publically available gut metagenomic data from Hadza hunter-gatherers and urban industrial Italians. According to our findings, Bifidobacterium provides the enteric ecosystem with a diverse panel of saccharolytic functions, well suited to the array of gluco- and galacto-based saccharides that abound in the Western diet. On the other hand, the metagenomic functions assigned to Treponema are more predictive of a capacity to incorporate complex polysaccharides, such as those found in unrefined plant foods, which are consistently incorporated in the Hadza diet. Finally, unlike Treponema, the Bifidobacterium metagenome functions include genes that permit the establishment of microbe-host immunological cross-talk, suggesting recent co-evolutionary events between the human immune system and Bifidobacterium that are adaptive in the context of agricultural subsistence and sedentary societies

Characterization of the human DNA gut virome across populations with different subsistence strategies and geographical origin

It is a matter of fact that the human gut microbiome also includes a non-bacterial fraction represented by eukaryotic cells and viruses. To further explore the gut microbiome variation in human populations, here we characterized the human DNA viral community from publicly available gut metagenome data sets from human populations with different geographical origin and lifestyle. In particular, such data sets encompass microbiome information from two western urban societies (USA and Italy), as well as two traditional hunter-gatherer communities (the Hadza from Tanzania and Matses from Peru) and one pre-agricultural tribe (Tunapuco from Peru). Our results allowed for the first taxonomic reconstruction of the complex viral metacommunities within the human gut. The core virome structure included herpesviruses, papillomaviruses, polyomaviruses, adenoviruses and anelloviruses. Using Random Forests and a co-occurrence analysis approach, we identified the viruses that distinguished populations according to their geographical origin and/or lifestyle. This paves the way for new research aimed at investigating the biological role of the gut virome in human physiology, and the importance of our viral counterpart in the microbiome-host co-evolutionary process

Infant and Adult Gut Microbiome and Metabolome in Rural Bassa and Urban Settlers from Nigeria

We assessed the subsistence-related variation of the human gut microbiome at a fine resolution for two of the main dimensions of microbiome variation, age and geography. For this, we investigated the fecal microbiome and metabolome in rural Bassa and urbanized individuals from Nigeria, including infants, and compared data with worldwide populations practicing varying subsistence. Our data highlight specific microbiome traits that are progressively lost with urbanization, such as the dominance of pristine fiber degraders and the low inter-individual variation. For the Bassa, this last feature is the result of their subsistence-related practices favoring microbial dispersal, such as their extensive environmental contact and the usage of untreated waters from the Usuma River. The high degree of microbial dispersal observed in the Bassa meta-community nullifies the differences between infant and adult intestinal ecosystems, suggesting that the infant-type microbiome in Western populations could be the result of microbiome-associated neotenic traits favored by urbanization. Ayeni et al. characterize the fecal microbiome and metabolome of rural Bassa and urban individuals from Nigeria, including infants. Their findings stress the loss of ancient signatures along with urbanization and support distinct trajectories of development of the intestinal ecosystem in early life, depending on human subsistence