Developing an empirical model for spillover and emergence: Orsay virus host range in Caenorhabditis

A lack of tractable experimental systems in which to test hypotheses about the ecological and evolutionary drivers of disease spillover and emergence has limited our understanding of these processes. Here we introduce a promising system: Caenorhabditis hosts and Orsay virus, a positive-sense single-stranded RNA virus that naturally infects C. elegans. We assayed the susceptibility of species across the Caenorhabditis tree and found 21 of 84 wild strains belonging to 14 of 44 species to be susceptible to Orsay virus. Confirming patterns documented in other systems, we detected effects of host phylogeny on susceptibility. We then tested whether susceptible strains were capable of transmitting Orsay virus by transplanting exposed hosts and determining whether they transmitted infection to conspecifics during serial passage. We found no evidence of transmission in 10 strains (virus undetectable after passaging), evidence of low-level transmission in 5 strains (virus lost between passage 1 and 5), and evidence of sustained transmission in 6 strains (including all 3 experimental C. elegans strains). Transmission was associated with host phylogeny and with viral amplification in exposed populations. Variation in Orsay virus susceptibility and transmission among Caenorhabditis species suggests that the system could be powerful for studying spillover and emergence.

Mammalian gut metabolomes mirror microbiome composition and host phylogeny

In the past decade, studies on the mammalian gut microbiome have revealed that different animal species have distinct gut microbial compositions. The functional ramifications of this variation in microbial composition remain unclear: do these taxonomic differences indicate microbial adaptations to host-specific functionality, or are these diverse microbial communities essentially functionally redundant, as has been indicated by previous metagenomics studies? Here, we examine the metabolic content of mammalian gut microbiomes as a direct window into ecosystem function, using an untargeted metabolomics platform to analyze 101 fecal samples from a range of 25 exotic mammalian species in collaboration with a zoological center. We find that mammalian metabolomes are chemically diverse and strongly linked to microbiome composition, and that metabolome composition is further correlated to the phylogeny of the mammalian host. Specific metabolites enriched in different animal species included modified and degraded host and dietary compounds such as bile acids and triterpenoids, as well as fermentation products such as lactate and short-chain fatty acids. Our results suggest that differences in microbial taxonomic composition are indeed translated to host-specific metabolism, indicating that taxonomically distant microbiomes are more functionally diverse than redundant.

The functional evolution of termite gut microbiota

SUMMARYTermites primarily feed on lignocellulose or soil in association with specific gut microbes. The functioning of the termite gut microbiota is partly understood in a handful of wood-feeding pest species, but remains largely unknown in other taxa. We intend to feel this gap and provide a global understanding of the functional evolution of termite gut microbiota. We sequenced the gut metagenomes of 145 samples representative of the termite diversity. We show that the prokaryotic fraction of the gut microbiota of all termites possesses similar genes for carbohydrate and nitrogen metabolisms, in proportions varying with termite phylogenetic position and diet. The presence of a conserved set of gut prokaryotic genes implies that key nutritional functions were present in the ancestor of modern termites. Furthermore, the abundance of these genes largely correlated with the host phylogeny. Finally, we found that the adaptation to a diet of soil by some termite lineages was accompanied by a change in the stoichiometry of genes involved in important nutritional functions rather than by the acquisition of new genes and pathways. Our results reveal that the composition and function of termite gut prokaryotic communities have been remarkably conserved since termites first appeared ∼150 million years ago. Therefore, the “world smallest bioreactor” has been operating as a multipartite symbiosis composed of termites, archaea, bacteria, and cellulolytic flagellates since its inception.

You are more than what you eat: potentially adaptive enrichment of microbiome functions across bat dietary niches

Background Animals evolved in a microbial world, and their gut microbial symbionts have played a role in their ecological diversification. While many recent studies report patterns of phylosymbiosis between hosts and their gut bacteria, fewer studies examine the potentially adaptive functional contributions of these microbes to the dietary habits of their hosts. In this study, we examined predicted metabolic pathways in the gut bacteria of more than 500 individual bats belonging to 60 species and compare the enrichment of these functions across hosts with distinct dietary ecologies. Results We found that predicted microbiome functions were differentially enriched across hosts with different diets. Using a machine-learning approach, we also found that inferred microbiome functions could be used to predict specialized host diets with reasonable accuracy. We detected a relationship between both host phylogeny and diet with respect to microbiome functional repertoires. Because many predicted functions could potentially fill nutritional gaps for bats with specialized diets, we considered pathways discriminating dietary niches as traits of the host and fit them to comparative phylogenetic models of evolution. Our results suggest that some, but not all, predicted microbiome functions may evolve toward adaptive optima and thus be visible to the forces of natural selection operating on hosts over evolutionary time. Conclusions Our results suggest that bats with specialized diets may partially rely on their gut microbes to fulfill or augment critical nutritional pathways, including essential amino acid synthesis, fatty acid biosynthesis, and the generation of cofactors and vitamins essential for proper nutrition. Our work adds to a growing body of literature suggesting that animal microbiomes are structured by a combination of ecological and evolutionary processes and sets the stage for future metagenomic and metabolic characterization of the bat microbiome to explore links between bacterial metabolism and host nutrition.

Microbiome stability and structure is governed by host phylogeny over diet and geography in woodrats (Neotoma spp.)

The microbiome is critical for host survival and fitness, but gaps remain in our understanding of how this symbiotic community is structured. Despite evidence that related hosts often harbor similar bacterial communities, it is unclear whether this pattern is due to genetic similarities between hosts or to common ecological selection pressures. Here, using herbivorous rodents in the genus Neotoma, we quantify how geography, diet, and host genetics, alongside neutral processes, influence microbiome structure and stability under natural and captive conditions. Using bacterial and plant metabarcoding, we first characterized dietary and microbiome compositions for animals from 25 populations, representing seven species from 19 sites across the southwestern United States. We then brought wild animals into captivity, reducing the influence of environmental variation. In nature, geography, diet, and phylogeny collectively explained ∼50% of observed microbiome variation. Diet and microbiome diversity were correlated, with different toxin-enriched diets selecting for distinct microbial symbionts. Although diet and geography influenced natural microbiome structure, the effects of host phylogeny were stronger for both wild and captive animals. In captivity, gut microbiomes were altered; however, responses were species specific, indicating again that host genetic background is the most significant predictor of microbiome composition and stability. In captivity, diet effects declined and the effects of host genetic similarity increased. By bridging a critical divide between studies in wild and captive animals, this work underscores the extent to which genetics shape microbiome structure and stability in closely related hosts.

Daily feeding rhythm linked to microbiome composition in two zooplankton species

Host-associated microbial communities are impacted by external and within-host factors, i.e., diet and feeding behavior. For organisms known to have a circadian rhythm in feeding behavior, microbiome composition is likely impacted by the different rates of microbe introduction and removal across a daily cycle, in addition to any diet-induced changes in microbial interactions. Here, we measured feeding behavior and used 16S rRNA sequencing to compare the microbial community across a diel cycle in two distantly related species of Daphnia, that differ in their life history traits, to assess how daily feeding patterns impact microbiome composition. We find that Daphnia species reared under similar laboratory conditions have significantly different microbial communities. Additionally, we reveal that Daphnia have daily differences in their microbial composition that correspond with feeding behavior, such that there is greater microbiome diversity at night during the host's active feeding phase. These results highlight that zooplankton microbiomes are relatively distinct and are likely influenced by host phylogeny.

Vertebrate host phylogeny influences gut archaeal diversity

Commonly used 16S rRNA gene primers do not detect the full range of archaeal diversity present in the vertebrate gut. As a result, several questions regarding the archaeal component of the gut microbiota remain, including which Archaea are host-associated, the specificities of such associations and the major factors influencing archaeal diversity. Using 16S rRNA gene amplicon sequencing with primers that specifically target Archaea, we obtained sufficient sequence data from 185 gastrointestinal samples collected from 110 vertebrate species that span five taxonomic classes (Mammalia, Aves, Reptilia, Amphibia and Actinopterygii), of which the majority were wild. We provide evidence for previously undescribed Archaea–host associations, including Bathyarchaeia and Methanothermobacter, the latter of which was prevalent among Aves and relatively abundant in species with higher body temperatures, although this association could not be decoupled from host phylogeny. Host phylogeny explained archaeal diversity more strongly than diet, while specific taxa were associated with both factors, and cophylogeny was significant and strongest for mammalian herbivores. Methanobacteria was the only class predicted to be present in the last common ancestors of mammals and all host species. Further analysis indicated that Archaea–Bacteria interactions have a limited effect on archaeal diversity. These findings expand our current understanding of Archaea–vertebrate associations.

Comparative Study of the Gut Microbiota Among Four Different Marine Mammals in an Aquarium

Despite an increasing appreciation in the importance of host–microbe interactions in ecological and evolutionary processes, information on the gut microbial communities of some marine mammals is still lacking. Moreover, whether diet, environment, or host phylogeny has the greatest impact on microbial community structure is still unknown. To fill part of this knowledge gap, we exploited a natural experiment provided by an aquarium with belugas (Delphinapterus leucas) affiliated with family Monodontidae, Pacific white-sided dolphins (Lagenorhynchus obliquidens) and common bottlenose dolphin (Tursiops truncatus) affiliated with family Delphinidae, and Cape fur seals (Arctocephalus pusillus pusillus) affiliated with family Otariidae. Results show significant differences in microbial community composition of whales, dolphins, and fur seals and indicate that host phylogeny (family level) plays the most important role in shaping the microbial communities, rather than food and environment. In general, the gut microbial communities of dolphins had significantly lower diversity compared to that of whales and fur seals. Overall, the gut microbial communities were mainly composed of Firmicutes and Gammaproteobacteria, together with some from Bacteroidetes, Fusobacteria, and Epsilonbacteraeota. However, specific bacterial lineages were differentially distributed among the marine mammal groups. For instance, Lachnospiraceae, Ruminococcaceae, and Peptostreptococcaceae were the dominant bacterial lineages in the gut of belugas, while for Cape fur seals, Moraxellaceae and Bacteroidaceae were the main bacterial lineages. Moreover, gut microbial communities in both Pacific white-sided dolphins and common bottlenose dolphins were dominated by a number of pathogenic bacteria, including Clostridium perfringens, Vibrio fluvialis, and Morganella morganii, reflecting the poor health condition of these animals. Although there is a growing recognition of the role microorganisms play in the gut of marine mammals, current knowledge about these microbial communities is still severely lacking. Large-scale research studies should be undertaken to reveal the roles played by the gut microbiota of different marine mammal species.

Ecology impacts the decrease of Spirochaetes and Prevotella in the fecal gut microbiota of urban humans

Compared to the huge microbial diversity in most mammals, human gut microbiomes have lost diversity while becoming specialized for animal-based diets – especially compared to chimps, their genetically closest ancestors. The lowered microbial diversity within the gut of westernized populations has also been associated with different kinds of chronic inflammatory diseases in humans. To further deepen our knowledge on phylogenetic and ecologic impacts on human health and fitness, we established the herein presented biobank as well as its comprehensive microbiota analysis. In total, 368 stool samples from 38 different animal species, including Homo sapiens, belonging to four diverse mammalian orders were collected at seven different locations and analyzed by 16S rRNA gene amplicon sequencing. Comprehensive data analysis was performed to (i) determine the overall impact of host phylogeny vs. diet, location, and ecology and to (ii) examine the general pattern of fecal bacterial diversity across captive mammals and humans.By using a controlled study design with captive mammals we could verify that host phylogeny is the most dominant driver of mammalian gut microbiota composition. However, the effect of ecology appears to be able to overcome host phylogeny and should therefore be studied in more detail in future studies. Most importantly, our study could observe a remarkable decrease of Spirochaetes and Prevotella in westernized humans and platyrrhines, which is probably not only due to diet, but also to the social behavior and structure in these communities.Our study highlights the importance of phylogenetic relationship and ecology within the evolution of mammalian fecal microbiota composition. Particularly, the observed decrease of Spirochaetes and Prevotella in westernized communities might be associated to lifestyle dependent rapid evolutionary changes, potentially involved in the establishment of dysbiotic microbiomes, which promote the etiology of chronic diseases.