Search bioRxiv⌕ Search

bioRxiv · 10.1101/2023.12.14.571744

Metabolic and genomic characterization of two novel butyrate producing Lachnospiraceae isolated from swine feces

Abstract

Commensal bacteria from the swine gut microbiome that can be isolated have numerous potential applications in the animal production industry, including mitigation of disease, improving performance, and promoting colonization resistance to human foodborne pathogens. Butyrate-producing bacteria are targets for next-generation probiotics and microbiome-engineering strategies because butyrate is a metabolite of central importance in large intestinal homeostasis and may augment colonization resistance to enteric pathogens. However, relatively few butyrate-producers from swine have been cultured and extensively characterized. Here, we describe the substrate utilization, metabolic profiles, and genomic features of two novel species that produce high concentration of butyrate in vitro, Roseburia sp. 831b and Petralouisia sp. 499, isolated from swine feces. The complete genomes illustrated versatility in carbon metabolism and unique carbohydrate-active enzymes not observed in other species of Roseburia and Petralouisia that encode a combination of glycosidic hydrolases and carbohydrate-binding modules involved in starch and pectin utilization. Roseburia sp. 831b fermented a broader range and more complex mono- and polysaccharides than Petralouisia sp. 499. Fecal and cecal metagenomes from eight-week-old pigs challenged with Salmonella revealed that Roseburia sp. 831b increased to detectable abundances in the swine hindgut in most animals at [~]63-70 days of age. Additionally, the abundance of Roseburia sp. 831b in fecal metagenomes correlated with fecal butyrate concentrations in the pigs fed a diet supplemented with a prebiotic resistant potato starch. Together, these findings highlight the probiotic potential and ecological niche in the swine gastrointestinal tract for two novel butyrate-producers. ImportanceAntibiotics have been important for swine production and management of enteric pathogens; however, the Veterinary Feed Directive limits the use of medically important in-feed antibiotics for production purposes. As a result, there is a need for alternatives to antibiotics. Butyrate-producing bacteria can improve colonization resistance to human pathogens within the swine gastrointestinal tract by reinforcing the intestinal barrier, increasing mucus production, and reducing local oxygen and pH levels. Here, we demonstrate the versatile substrate utilization and metabolic potential of two novel species isolated from swine that produce high butyrate concentrations in vitro. These findings will help develop strategies that increase the abundance of these species and other butyrate producers in the swine gut. Further, isolating and characterizing swine butyrate producers is necessary for controlled studies that provide a mechanistic understanding of how this functional group of bacteria promotes swine gut health and colonization resistance to bacteria of public health concern.

Explore related subjects

Keep this discovery

Explore connections, maps & timelines

BibTeXRIS

Watkins, H. R., Trachsel, J. M., Bearson, S. M. D., Loving, C. L., Anderson, C. L.. 2023-12-15. Metabolic and genomic characterization of two novel butyrate producing Lachnospiraceae isolated from swine feces. https://doi.org/10.1101/2023.12.14.571744

Cite the original work for its findings. Save a collection to share your selection of sources.

KEEP EXPLORING

Related preprints

A population-scale landscape of the subgingival microbiome reveals divergent routes to periodontal dysbiosis

Periodontitis is an archetypical mucosal inflammatory disease in which microbiome dysbiosis at the tooth-epithelial interface interacts with host genetic and behavioral risk factors to drive immune-mediated tissue destruction. Although subgingival microbiome compositional shifts are thought to parallel disease severity, microbiome variation at the population-level and its relationship to periodontal clinical phenotypes and disease-modifying factors remain poorly defined. Here, we use unsupervised manifold learning to map the compositional landscape of the subgingival microbiome in 1,355 adults spanning periodontal health to severe periodontitis. We identified eight latent microbiome states organized along a branching continuum from eubiosis to dysbiosis. An intermediate microbial configuration marked ecological destabilization and bifurcation into two distinct periodontitis-associated dysbiotic trajectories, distinguished by links to gingival inflammation and smoking. Although the microbiome trajectories broadly tracked periodontal destruction, a minority of individuals showed discordant microbiome-clinical phenotypes, with some individuals with periodontitis retaining otherwise eubiotic microbiomes enriched for low-abundance pathobionts, while some cases of health or mild disease had highly dysbiotic communities, suggesting distinct host susceptibility. Together, these findings define a population-scale ecological landscape of the subgingival microbiome, reveal divergent trajectories to periodontal dysbiosis, and highlight heterogeneity in the relationship between microbial community structure and clinical disease expression.

microbiology↗

The iron-binding siderophore enterobactin is required for the response of multi-drug resistant Klebsiella pneumoniae to zinc limitation

To persist during infection Klebsiella pneumoniae must overcome nutrient iron and zinc limitation imposed by the host immune system through a process called nutritional immunity. Secreted small molecule siderophores are a major virulence determinant of Klebsiella pneumoniae pathogenesis and are presumed to overcome nutritional immunity by binding iron for bacterial acquisition. In this work, we set out to identify how a multi-drug resistant K. pneumoniae grows in zinc limited environments. Using unbiased transcriptomics, proteomics, and an arrayed transposon screen, we identified that synthesis and uptake of the siderophore enterobactin is required to allow for growth in low zinc conditions. Iron-specific chelators did not replicate this phenotype and addition of supplemental iron through heme in growth media could not complement severe growth defects of enterobactin mutant K. pneumoniae experiencing zinc limitation. Finally, zinc starvation induced enterobactin production independent of the canonical zinc uptake regulator (Zur) transcription factor suggesting an unidentified regulatory mechanism by which Gram-negative pathogens may respond to zinc stress. Together, these studies expand the role of enterobactin beyond iron regulation and highlight a previously unreported link between iron and zinc homeostasis in Klebsiella pneumoniae.

microbiology↗

A microbiota-derived protease links phage susceptibility to host epithelial responses

Bacteriophages are major ecological drivers of gut microbial ecology, yet whether bacterial mechanisms that determine phage susceptibility have consequences for the mammalian host remains poorly understood. Here, we identify dipeptidyl peptidase 11 (Dpp11a), the predominant active serine protease of the prevalent gut commensal Phocaeicola vulgatus, as an unexpected bacterial defence factor. Dpp11a protects against environmental proteases and confers resistance to bacteriophage infection. Metatranscriptomic analyses further reveal increased expression of both dpp11a and P. vulgatus-associated phage transcripts in ulcerative colitis stool samples, indicating that both components of this interaction are transcriptionally active in disease-associated human microbiomes. Using the microfluidic gut-on-a-chip co-culture model HuMiX, we show that the absence of Dpp11 is accompanied by altered epithelial tight-junction remodelling during phage-bacterial infection. Together, our findings reveal that the consequences of bacterial phage defence can extend beyond phage-bacterium interactions to the mammalian epithelium.

microbiology↗