Search bioRxiv⌕ Search

Biology subjects

Brealey, J. C.

Publications and source records attributed to Brealey, J. C..

10 recordsLinked to original sources

Museum specimens reveal evolutionary drivers and functions of oral microbiome in mammals

The microbiomes of wild animals, despite being integral to host survival, remain largely unexplored, particularly beyond the gut. Here, using > 450 museum-preserved dental calculus samples from 34 ecologically and phylogenetically diverse mammalian species, most of them previously unstudied, we determine the main drivers of oral microbiome evolution. We show that, similar to the gut, the oral microbiome is shaped by host ecology, particularly diet, and to a lesser extent host phylogenetic relationships. It may contribute to host adaptation, by synthesising essential micronutrients and degrading potentially harmful compounds. We also find that some oral microorganisms consistently associated with mammals throughout over evolutionary time scales and provide evidence for a likely oral origin of some rumen taxa. Together our findings demonstrate the importance of this mostly overlooked microbial community for mammalian biology.

evolutionary biology↗

Pleistocene reindeer dental calculus as a source for ancient oral and digestive flora

Dental calculus offers an extraordinary window into the past, preserving a rich archive of genetic material that can unlock new insights into ancient ecosystems. By capturing traces of oral microbiomes, dietary components, and even gut microbes regurgitated by ruminants, dental calculus provides an extraordinary window into the past to reconstruct ecological interactions and past environmental conditions. Here, we harness the power of ancient metagenomics to explore the oral microbiome, digestive microbiomes and diet of Pleistocene reindeer (Rangifer tarandus) from archaeological sites in France, a region that once served as a glacial refugium before reindeer disappeared from the area. We used shotgun metagenomic sequencing to assemble microbial genomes (MAGs) and classify microbial and dietary reads from dental calculus of 19 ancient reindeer (ca. 12,000 - 23,000 years BP) and 27 modern and historical (1861 - 1958 CE) Scandinavian reindeer. Notably, six bacterial taxa associated with the rumen microbiome were consistently detected across both ancient and modern samples, offering a rare glimpse into the continuity of digestive adaptations over thousands of years. Our recovery of oral microbial and putative dietary plant DNA suggest adaptive capability. Our results suggest a spatio-temporal turnover in oral microbiome and putative dietary plant DNA, which might be explained by ecological differences between Pleistocene France and contemporary Scandinavia. As soft tissue preservation is rare in ancient remains, dental calculus emerges as an exciting and powerful tool for reconstructing the environmental and ecological histories of both past and extinct populations.

evolutionary biology↗

Multiple, single trait GWAS and supervised machine learning reveal the genetic architecture of Fraxinus excelsior tolerance to ash dieback in Europe

Common ash (Fraxinus excelsior) is under intensive attack from the invasive alien pathogenic fungus Hymenoscyphus fraxineus, causing ash dieback at epidemic levels throughout Europe. Previous studies have found significant genetic variation among clones in ash dieback susceptibility and that host phenology, such as autumn yellowing, is correlated with susceptibility of ash trees to H. fraxineus; however, the genomic basis of ash dieback tolerance in F. excelsior remains poorly understood. Here, we integrate quantitative genetics and genome-wide association analyses with machine learning to reveal the genetic architecture of ash dieback tolerance and its relationship to phenological traits in F. excelsior populations in six European countries (Austria, Denmark, Germany, Ireland, Lithuania, Sweden). We use whole-genome sequencing of 486 F. excelsior genotypes to confirm the genotypic correlation between crown damage caused by ash dieback and intensity of autumn leaf yellowing within multiple sampling sites. Although, our results suggest that the examined traits are polygenic, a relatively small number of single nucleotide polymorphisms (SNPs) explained a large proportion of the variation in both disease tolerance and autumn leaf yellowing. We could explain up to 63% (based on 9155 unlinked SNPs) of variation in individual response to ash dieback crown damage and up to 72% (based on 3740 unlinked SNPs) of variation in autumn yellowing. We identified eight SNPs encoding non-synonymous substitutions, of which those with the highest predictive power were located within genes related to plant defence (pattern triggered immunity, pathogen detection) and phenology (regulation of flowering and seed maturation, auxin transport). Overall, our results provide insights of a multifaceted defence response, according to which a combination of direct defence mechanisms and phenological avoidance of pathogen spread constitute tolerance to ash dieback.

plant biology↗

A paleogenomic investigation of overharvest implications in an endemic wild reindeer subspecies

Overharvest can severely reduce the abundance and distribution of a species and thereby impact its genetic diversity and threaten its future viability. Overharvest remains an ongoing issue for Arctic mammals, which due to climate change now also confront one of the fastest changing environments on Earth. The high-Arctic Svalbard reindeer (Rangifer tarandus platyrhynchus), endemic to Svalbard, experienced a harvest-induced demographic bottleneck that occurred during the 17-20th century. Here we investigate changes in genetic diversity, population structure and gene-specific differentiation during and after this overharvesting event. Using whole-genome shotgun sequencing, we generated the first ancient nuclear (n = 11) and mitochondrial (n = 18) genomes from Svalbard reindeer (up to 4000 BP) and integrated these data with a large collection of modern genome sequences (n = 90), to infer temporal changes. We show that hunting resulted in major genetic changes and restructuring in reindeer populations. Near-extirpation and 400 years of genetic drift have altered the allele frequencies of important genes contributing to diverse biological functions. Median heterozygosity was reduced by 23%, while the mitochondrial genetic diversity was reduced only to a limited extent, likely due to low pre-harvest diversity and a complex post-harvest recolonization process. Such genomic erosion and genetic isolation of populations due to past anthropogenic disturbance will likely play a major role in metapopulation dynamics (i.e., extirpation, recolonization) under further climate change. Our results from a high-arctic case study therefore emphasize the need to understand the long- term interplay of past, current, and future stressors in wildlife conservation.

genomics↗

Host-gut microbiota interactions shape parasite infections in farmed Atlantic salmon

Animals and their associated microbiota share long evolutionary histories. Both host genotype and associated microbiota influence phenotypes such as growth and disease resilience. We applied a hologenomic approach to explore the relationship between host and microbiota in shaping lifetime growth and parasitic cestode infection in farmed Atlantic salmon. Genomes, transcriptomes, metabolomes and metagenomes were generated from the guts of 460 harvest-aged salmon, 82% of which were naturally infected with an intestinal cestode. One salmonid-specific Mycoplasma dominated the gut microbiota of uninfected salmon. However, the microbiota was perturbed in smaller, parasitised fish, with increased abundance of Vibrionaceae and other Mycoplasma species previously linked to the cestode microbiota. The cestode-associated Mycoplasma carry more virulence-associated genes than the salmonid Mycoplasma. Colonisation by one cestode-associated Mycoplasma was associated with a region of the salmon genome encoding several long noncoding RNA genes previously associated with host control of intestinal microbiota. Integrating the multiple omic datasets revealed coordinated changes in the salmon gut transcriptome and metabolome that correlated with shifts in the microbiota of smaller, parasitised fish. Our results suggest that cestode infections introduce new microbes and trigger host responses, altering the gut microbiota with increases in potentially pathogenic microbes. Establishment of these microbes is partially shaped by the genetic background of the host. Our study highlights the value of a hologenomic approach for gaining an in-depth understanding of trilateral interactions among host, microbiota and parasite.

systems biology↗

Dental calculus metagenomics suggest that ecology, not host phylogeny, shapes the oral microbiome in closely related species

Host-associated microbiomes are essential for a multitude of biological processes. Placed at the contact zone between external and internal environments, the little-studied oral microbiome has important roles in host physiology and health. Here we investigate the contribution of host evolutionary relationships and ecology in shaping the oral microbiome in three closely related gorilla subspecies (mountain, Grauers, and western lowland gorillas) using shotgun metagenomics of 46 museum-preserved dental calculus samples. We find that the oral microbiomes of mountain gorillas are functionally and taxonomically distinct from the other two subspecies, despite close evolutionary relationships and geographic proximity with Grauers gorillas. Grauers gorillas show intermediate bacterial taxonomic and functional, and dietary profiles. Altitudinal differences in gorilla subspecies ranges appear to explain these patterns, proposing a close connection between dental calculus microbiome and the environment, which is further supported by the presence of gorilla subspecies-specific phyllosphere/rhizosphere taxa. Mountain gorillas show high abundance of nitrate-reducing oral taxa, which may contribute to high altitude adaptation by modulating blood pressure. Our results suggest that ecology, rather than evolutionary relationships and geographic proximity, primarily shape the oral microbiome in these closely related species.

evolutionary biology↗

Uncovering the hologenomic basis of an extraordinary plant invasion

While invasive species are a key driver of the global biodiversity crisis, the drivers of invasiveness remain debated. To investigate the genomic basis of invasiveness in plants, we use the invasive weed Ambrosia artemisiifolia, introduced to Europe in the late 19th century, resequencing 655 ragweed genomes, including 308 herbarium specimens collected up to 190 years ago. In introduced European populations, we report selection signatures in defense genes and lower prevalence of particular plant pathogens in the invasive range. Together with temporal changes in population structure associated with introgression from closely related Ambrosia species, escape from microbial enemies likely favoured the plants remarkable success as an invasive species. One-Sentence SummaryThe invasive success of European ragweed was facilitated by release from enemy microbes and inter-species hybridization.

genomics↗

Wild animal oral microbiomes reflect the history of human antibiotics use

Following the advent of industrial-scale antibiotics production in the 1940s, antimicrobial resistance (AMR) has been on the rise and now poses a major global health threat. Because AMR can be exchanged between humans, livestock and wildlife, evaluating the potential of wild animals to act as AMR reservoirs is essential. We used shotgun metagenomics sequencing of dental calculus, the calcified form of the oral microbial biofilm, to determine the abundance and repertoire of AMR genes in the oral microbiome of Swedish brown bears from museum specimens collected over the last 200 years. Our temporal metagenomics approach allowed us to establish a baseline of natural AMR in the pre-antibiotics era and to quantify a significant increase in total AMR load and diversity of AMR genes that is correlated with human antibiotics use. We also demonstrated that Swedish public health policies were effective in limiting AMR spillover into wildlife.

microbiology↗

Conservation Genomic Analyses of African and Asiatic Cheetahs (Acinonyx jubatus) Across Their Current and Historic Species Range.

Cheetahs (Acinonyx jubatus) are majestic carnivores and the fastest land animals; yet, they are quickly heading towards an uncertain future. Threatened by habitat loss, human-interactions and illegal trafficking, there are only approximately 7,100 individuals remaining in the wild. Cheetahs used to roam large parts of Africa, and Western and Southern Asia. Today they are confined to about 9% of their original distribution. To investigate their genetic diversity and conservation status, we generated genome-wide data from historical and modern samples of all four currently recognized subspecies, along with mitochondrial DNA (mtDNA) and major histo-compatibility complex (MHC) data. We found clear genetic differentiation between the sub-species, thus refuting earlier assumptions that cheetahs show only little population differentiation. Our genome-wide nuclear data indicate that cheetahs from East Africa may be more closely related to A. j. soemmeringii than they are to A. j. jubatus. This supports the need for further research on the classification of cheetah subspecies, as East African cheetahs are currently included in the Southern Africa subspecies, A. j. jubatus. We detected stronger inbreeding in individuals of the Critically Endangered A. j. venaticus (Iran) and A. j. hecki (Northwest Africa), and show that overall genome-wide heterozygosity in cheetah is lower than that reported for other threatened and endangered felids, such as tigers and lions. Furthermore, we show that MHC class II diversity in cheetahs is generally higher than previously reported, but still lower than in other felids. Our results provide new and important information for efficient genetic monitoring, subspecies assignments and evidence-based conservation policy decisions.

evolutionary biology↗

Dental calculus as a tool to study the evolution of the oral microbiome in mammals

Animals and their associated microbiomes share a long evolutionary history, influenced by a complex interplay between extrinsic environmental and intrinsic host factors. However, we know little about microbiome responses to long-lasting environmental and host-centred processes, which require studying microbiome changes through time. Here, we apply a temporal metagenomics approach to dental calculus, the calcified oral microbial biofilm. We establish dental calculus as a valuable tool for the study of host microbiome evolution by characterising the taxonomic and functional composition of the oral microbiome in a variety of wild mammals. We detect oral pathogens in individuals with evidence of oral disease, assemble near-complete bacterial genomes from historical specimens, characterise antibiotic resistance genes even before the advent of industrial antibiotic production, reconstruct components of the host diet and recover host genetic profiles. Our work demonstrates how dental calculus can be used in the future to study the evolution of oral microbiomes and pathogens, and the impact of anthropogenic changes on wildlife and the environment.

evolutionary biology↗