ABSTRACT Intra-species genomic variation provides the raw material for natural selection and can reflect the recent diversification history of microbial populations. Environmental stress may be regarded as the ultimate accelerator of the evolutionary process, especially for microorganisms, which can alter their DNA if presented with nutrient limitation, toxins, or pathogen attack. Chronic intestinal inflammation, as in inflammatory bowel disease (IBD), represents prolonged environmental stress for gut commensal bacteria, bringing many enteric species down to undetectable levels. However, it remains unclear how microbes that colonize IBD patients actually respond to IBD-associated stressors and whether stress-driven bacterial dynamics may be identified at the population level from the bacterial gut metagenome. To investigate IBD-associated strain-level population dynamics, we performed metagenomic analyses focusing on measuring within-individual bacterial diversity for a panel of gut commensals present across IBD patients and Controls. First, we found species-specific differences in genome-level bacterial diversity. Then, we found that certain genes and functions may harbor different levels and kinds of genetic divergence within the same species across IBD patients and Controls. Functions that were enriched in IBD with both neutral divergence and functional divergence were associated with motility and iron-scavenging, among others. These results may point toward functions that are under selection in the context of IBD stress and could inform future mechanistic work, exploring previously unknown routes of bacterial diversification and adaptation to stress in the gut microbiome. IMPORTANCE Inflammatory bowel disease (IBD) is characterized by profound alterations in the gut microbiome composition, and most research so far has focused on changes in species-level abundance to understand gut microbiome contributions to disease dynamics. However, investigating strain-level variation has the potential to uncover previously unknown factors underlying bacterial persistence during gut inflammation, hence revealing key aspects driving gut dysbiosis. Here, we showed that IBD is associated with species-specific changes in gut microbial population-level genetic diversity and identified individual genes and functions that seem to harbor differential genetic diversity within IBD-associated strains. More broadly, our results highlight how intra-species population- and gene-level diversity could be used as sensors of environmental stress in the gut microbiome, and further studies could follow up on the functions highlighted in this work to establish causal links between gut inflammatory conditions and processes of bacterial adaptation to stress.
ABSTRACT Chlamydia psittaci is a zoonotic pathogen that can cause severe human respiratory infections. To assess its genetic diversity and zoonotic risk, we screened 1,525 samples from humans, poultry, and wild birds in East China (EC) during 2020–2023 and recovered 41 genomes using a targeted capture assay, together with 103 publicly available genomes. Phylogenomic analysis identified a distinct whole-genome lineage, designated the EC lineage, that was significantly enriched among human-derived isolates relative to other lineages. The EC lineage showed an elevated substitution rate, extensive recombination, and multiple Chlamydia abortus -like genomic regions, indicating a distinctive evolutionary history. Genetically linked poultry–human clusters were consistent with recent cross-host transmission, whereas the potential for human-to-human transmission remains unresolved. Strengthened genomic surveillance is warranted to monitor this lineage. IMPORTANCE Chlamydia psittaci is a bird-associated pathogen that can cause severe respiratory disease in humans, yet its local evolution and transmission between animals and humans remain poorly understood. Here, we identify a distinct lineage circulating mainly in East China that is disproportionately represented among human infections and is genetically linked to poultry isolates. This lineage also shows unusually extensive genomic change, including recombination and regions similar to those found in the related species Chlamydia abortus . These findings highlight poultry as an important interface for monitoring emerging C. psittaci lineages and demonstrate the value of genomic surveillance for detecting pathogen variants with increased relevance to human health. The study provides a framework for integrating animal and human surveillance within a One Health strategy.
ABSTRACT Industrialization has reshaped human gut microbiomes, but its effects on other human-associated mammals remain poorly understood. Domestic dogs provide an informative comparative system because they have shared human environments and food systems for millennia yet retain distinct host biology. However, most canine microbiome studies have focused on industrialized companion, colony, or controlled-feeding dogs, limiting our understanding of the ecological range of the domestic dog gut microbiome. We analyzed fecal 16S rRNA gene profiles from 261 dogs sampled across Nepal, Thailand, the United Arab Emirates, and the United States, spanning forager, agrarian, pastoralist, urban, and industrialized lifestyles; 257 dogs remained after excluding those with reported recent antibiotic exposure. Lifestyle was the strongest measured correlate of canine gut bacterial composition, and this association persisted in restricted analyses of mature, non-shelter dogs sampled from temperate regions. Industrialized dogs differed from non-industrialized dogs through directional genus-level shifts, prevalence-defined VANISH-like and BloSSUM-like bacterial guilds, coabundance structure, and shifts in predicted functional potential. Non-industrialized dogs were not microbiologically uniform: pastoralist dogs showed non-industrialized gut bacterial community profiles but diverged from a simple forager-to-industrialized continuum. Cross-species comparisons with humans sampled across matched lifestyle categories showed parallel lifestyle-associated restructuring in both hosts, but host species remained the dominant axis of variation, and genus-level responses were largely host specific. These findings expand the ecological baseline for canine gut bacterial communities and identify industrialization-associated lifestyle change as a major axis of gut bacterial community restructuring in a long-term human-associated mammal. More broadly, they show that shared lifestyle transitions can impose parallel ecological pressures across host species without overriding host-specific community assembly. IMPORTANCE Domestic dogs are one of the closest animal companions of humans, yet we know surprisingly little about how their gut microbiomes vary outside industrialized pet populations. This study shows that industrialization-associated lifestyle change is not only relevant to human microbiomes but also a broader ecological force that reshapes gut microbial communities in animals living alongside us. By comparing dogs across diverse human lifestyles, we show that shared environments can impose parallel pressures on the gut bacterial communities of humans and dogs, while each host maintains a distinct microbial identity. These findings suggest that gut microbial communities are shaped by the interaction between host biology and changing ecological conditions. Expanding microbiome research beyond industrialized settings is therefore essential for understanding what microbial diversity has been retained, altered, or lost during recent lifestyle transitions.
ABSTRACT Microbial life strategies are shaped by a fundamental ecological trade-off: specialization enables peak performance in a narrow niche, while generalization allows persistence across diverse environments, but may constrain maximal growth rates. In soils, this trade-off is particularly relevant in the rhizosphere and detritusphere—and at their interface, where co-occurring living roots and decaying residues are hypothesized to generate emergent biogeochemical conditions. Using H₂¹⁸O quantitative stable isotope probing (qSIP), we measured bacterial and fungal growth rates in the rhizosphere, the detritusphere, and in the combined presence of rhizosphere + root detritus. We classified taxa operationally as specialists (defined as microbes actively growing only within a single habitat) or generalists (defined as microbes actively growing in two or more habitats), reflecting realized growth breadth under the conditions tested. Bacterial specialists exhibited faster growth than generalists within the habitats where they grew, a pattern consistent with a trade-off between niche breadth and growth rate. Net relatedness and nearest taxon indices showed that total bacterial communities were phylogenetically clustered, while specialist and generalist communities were phylogenetically random, consistent with functional traits—rather than lineage—predicting realized growth-breadth strategy. In annual grassland soils, fast-growing specialists may dominate ecosystem processes when resources abound, and slow-growing generalists may sustain element transformations when conditions shift; understanding this interplay may inform predictions of soil-carbon trajectories. IMPORTANCE Soil microbes play a crucial role in cycling carbon and nutrients, but their strategies for surviving and growing in different environments remain poorly understood. This study asks whether soil microbes that grow rapidly in one habitat trade off that speed against the breadth of habitats they can occupy. Using quantitative stable isotope probing of H 2 18 O —an approach that measures active growth rather than mere presence—we tracked bacterial and fungal growth rates across three root-influenced habitats: the rhizosphere, the detritusphere, and the combined rhizosphere + detritusphere. We found that microbes detected growing in only one habitat (“specialists”) tended to grow faster within their habitat than microbes detected growing across multiple habitats (“generalists”), a pattern consistent with a trade-off between niche breadth and growth rate. This pattern was clearer for bacteria than for fungi. Although these classifications describe realized growth breadth under the conditions tested rather than universal organismal traits, understanding where and when specialists or generalists dominate may help inform predictions about the fate of soil carbon under changing plant inputs.
ABSTRACT Semen quality is critical for reproductive performance in dairy cattle; however, its microbial, metabolic, and genetic bases remain poorly understood. We integrated rumen microbiota, metabolome, and genome-wide variation from 55 Holstein bulls stratified into relative semen quality high (RSQH) and relative semen quality low (RSQL) groups based on semen quality records to investigate host-microbiome-metabolome interactions associated with fertility. The rumen microbiota was dominated by Bacteroidota, Firmicutes, and Proteobacteria, while Fibrobacter (phylum Fibrobacterota) was enriched in RSQH bulls and positively associated with sperm motility and density. The metabolome distinguished the two groups with 64 discriminatory metabolites, including elevated N-acetyl-L-phenylalanine and prostaglandin H2 in RSQH and sebacic acid in RSQL. Machine learning models were used to prioritize microbial and metabolic features, identifying candidate markers that may contribute to differences in semen quality. Fibrobacter, thromboxane B2, and N1-[4-(cyanomethyl)phenyl]-4-chlorobenzamide emerged as candidate indicators of semen quality, supported by machine learning, high heritability, and genome-wide association study signals. Overall, 511 single-nucleotide polymorphisms (SNPs) were jointly associated with Fibrobacter and these metabolites, including six significantly linked to sperm motility based on GWAS analysis. These SNPs were grouped into two contrasting types, with C1-type variants showing decreasing trends and C2-type variants showing increasing trends in semen quality-related traits. Structural equation modeling revealed that C2-type variants were positively associated with semen traits through microbial and metabolite enrichment, whereas C1-type variants were negatively associated with them. These findings highlight coordinated host genetic, microbial, and metabolic contributions to semen quality in Holstein bulls and provide candidate biomarkers for fertility-related research and breeding. IMPORTANCE Improving bull fertility is important for reproductive efficiency in dairy production, but the biological factors underlying semen quality remain incompletely understood. This study shows that variation in semen quality in Holstein bulls is associated with coordinated differences in rumen microbiota, metabolites, and host genetic variation. In particular, Fibrobacter, thromboxane B2, and N1-[4-(cyanomethyl)phenyl]-4-chlorobenzamide emerged as promising indicators of semen quality. These findings provide a basis for future fertility biomarker research and may support the development of genetics- and microbiota-informed strategies for bull selection and reproductive management. Improving bull fertility is important for reproductive efficiency in dairy production, but the biological factors underlying semen quality remain incompletely understood. This study shows that variation in semen quality in Holstein bulls is associated with coordinated differences in rumen microbiota, metabolites, and host genetic variation. In particular, Fibrobacter, thromboxane B2, and N1-[4-(cyanomethyl)phenyl]-4-chlorobenzamide emerged as promising indicators of semen quality. These findings provide a basis for future fertility biomarker research and may support the development of genetics- and microbiota-informed strategies for bull selection and reproductive management.
