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1. Microbiome metabolic capacity is buffered against phylotype losses by functional redundancy

   https://doi.org/10.1128/aem.02368-24  

   Cross, Kayla; Beckman, Noelle; Jahnes, Benjamin; Sabree, Zakee L (February 2025, Applied and Environmental Microbiology)

   Rudi, Knut (Ed.)

   ABSTRACT Many animals contain a species-rich and diverse gut microbiota that likely contributes to several host-supportive services that include diet processing and nutrient provisioning. Loss of microbiome taxa and their associated metabolic functions as result of perturbations may result in loss of microbiome-level services and reduction of metabolic capacity. If metabolic functions are shared by multiple taxa (i.e., functional redundancy), including deeply divergent lineages, then the impact of taxon/function losses may be dampened. We examined to what degree alterations in phylotype diversity impact microbiome-level metabolic capacity. Feeding two nutritionally imbalanced diets to omnivorousPeriplaneta americanaover 8 weeks reduced the diversity of their phylotype-rich gut microbiomes by ~25% based on 16S rRNA gene amplicon sequencing, yet PICRUSt2-inferred metabolic pathway richness was largely unaffected due to their being polyphyletic. We concluded that the nonlinearity between taxon and metabolic functional losses is due to microbiome members sharing many well-characterized metabolic functions, with lineages remaining after perturbation potentially being capable of preventing microbiome “service outages” due to functional redundancy. IMPORTANCEDiet can affect gut microbiome taxonomic composition and diversity, but its impacts on community-level functional capabilities are less clear. Host health and fitness are increasingly being linked to microbiome composition and further modeling of the relationship between microbiome taxonomic and metabolic functional capability is needed to inform these linkages. Invertebrate animal models like the omnivorous American cockroach are ideal for this inquiry because they are amenable to various diets and provide high replicates per treatment at low costs and thus enabling rigorous statistical analyses and hypothesis testing. Microbiome taxonomic composition is diet-labile and diversity was reduced after feeding on unbalanced diets (i.e., post-treatment), but the predicted functional capacities of the post-treatment microbiomes were less affected likely due to the resilience of several abundant taxa surviving the perturbation as well as many metabolic functions being shared by several taxa. These results suggest that both taxonomic and functional profiles should be considered when attempting to infer how perturbations are altering gut microbiome services and possible host outcomes. 

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

   https://doi.org/10.1073/pnas.2108787118  

   Weinstein, Sara B.; Martínez-Mota, Rodolfo; Stapleton, Tess E.; Klure, Dylan M.; Greenhalgh, Robert; Orr, Teri J.; Dale, Colin; Kohl, Kevin D.; Dearing, M. Denise (November 2021, Proceedings of the National Academy of Sciences)

   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 genusNeotoma, 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. 

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3. Disentangling the link between zebrafish diet, gut microbiome succession, and Mycobacterium chelonae infection

   https://doi.org/10.1186/s42523-023-00254-8  

   Sieler, Michael J; Al-Samarrie, Colleen E; Kasschau, Kristin D; Varga, Zoltan M; Kent, Michael L; Sharpton, Thomas J (December 2023, Animal Microbiome)

   Abstract BackgroundDespite the long-established importance of zebrafish (Danio rerio) as a model organism and their increasing use in microbiome-targeted studies, relatively little is known about how husbandry practices involving diet impact the zebrafish gut microbiome. Given the microbiome’s important role in mediating host physiology and the potential for diet to drive variation in microbiome composition, we sought to clarify how three different dietary formulations that are commonly used in zebrafish facilities impact the gut microbiome. We compared the composition of gut microbiomes in approximately 60 AB line adult (129- and 214-day-old) zebrafish fed each diet throughout their lifespan. ResultsOur analysis finds that diet has a substantial impact on the composition of the gut microbiome in adult fish, and that diet also impacts the developmental variation in the gut microbiome. We further evaluated how 214-day-old fish microbiome compositions respond to exposure of a common laboratory pathogen,Mycobacterium chelonae, and whether these responses differ as a function of diet. Our analysis finds that diet determines the manner in which the zebrafish gut microbiome responds toM. chelonaeexposure, especially for moderate and low abundance taxa. Moreover, histopathological analysis finds that male fish fed different diets are differentially infected byM. chelonae. ConclusionsOverall, our results indicate that diet drives the successional development of the gut microbiome as well as its sensitivity to exogenous exposure. Consequently, investigators should carefully consider the role of diet in their microbiome zebrafish investigations, especially when integrating results across studies that vary by diet. 

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4. Heterosis of leaf and rhizosphere microbiomes in field‐grown maize

   https://doi.org/10.1111/nph.16730  

   Wagner, Maggie R.; Roberts, Joseph H.; Balint‐Kurti, Peter; Holland, James B. (July 2020, New Phytologist)

   Summary Macroorganisms’ genotypes shape their phenotypes, which in turn shape the habitat available to potential microbial symbionts. This influence of host genotype on microbiome composition has been demonstrated in many systems; however, most previous studies have either compared unrelated genotypes or delved into molecular mechanisms. As a result, it is currently unclear whether the heritability of host‐associated microbiomes follows similar patterns to the heritability of other complex traits.We take a new approach to this question by comparing the microbiomes of diverse maize inbred lines and their F₁hybrid offspring, which we quantified in both rhizosphere and leaves of field‐grown plants using 16S‐v4 and ITS1 amplicon sequencing.We show that inbred lines and hybrids differ consistently in the composition of bacterial and fungal rhizosphere communities, as well as leaf‐associated fungal communities. A wide range of microbiome features display heterosis within individual crosses, consistent with patterns for nonmicrobial maize phenotypes. For leaf microbiomes, these results were supported by the observation that broad‐sense heritability in hybrids was substantially higher than narrow‐sense heritability.Our results support our hypothesis that at least some heterotic host traits affect microbiome composition in maize. 

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5. Covariation of diet and gut microbiome in African megafauna

   https://doi.org/10.1073/pnas.1905666116  

   Kartzinel, Tyler R.; Hsing, Julianna C.; Musili, Paul M.; Brown, Bianca R.; Pringle, Robert M. (November 2019, Proceedings of the National Academy of Sciences)

   A major challenge in biology is to understand how phylogeny, diet, and environment shape the mammalian gut microbiome. Yet most studies of nonhuman microbiomes have relied on relatively coarse dietary categorizations and have focused either on individual wild populations or on captive animals that are sheltered from environmental pressures, which may obscure the effects of dietary and environmental variation on microbiome composition in diverse natural communities. We analyzed plant and bacterial DNA in fecal samples from an assemblage of 33 sympatric large-herbivore species (27 native, 6 domesticated) in a semiarid East African savanna, which enabled high-resolution assessment of seasonal variation in both diet and microbiome composition. Phylogenetic relatedness strongly predicted microbiome composition ( r = 0.91) and was weakly but significantly correlated with diet composition ( r = 0.20). Dietary diversity did not significantly predict microbiome diversity across species or within any species except kudu; however, diet composition was significantly correlated with microbiome composition both across and within most species. We found a spectrum of seasonal sensitivity at the diet−microbiome nexus: Seasonal changes in diet composition explained 25% of seasonal variation in microbiome composition across species. Species’ positions on (and deviations from) this spectrum were not obviously driven by phylogeny, body size, digestive strategy, or diet composition; however, domesticated species tended to exhibit greater diet−microbiome turnover than wildlife. Our results reveal marked differences in the influence of environment on the degree of diet−microbiome covariation in free-ranging African megafauna, and this variation is not well explained by canonical predictors of nutritional ecology. 

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