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Identification and Quantification of Bovine Digital Dermatitis-Associated Microbiota across Lesion Stages in Feedlot Beef Cattle.

ABSTRACT: Bovine digital dermatitis (DD) is a skin disorder that is a significant cause of infectious lameness in cattle around the world. However, very little is known about the etiopathogenesis of the disease and the microbiota associated with DD in beef cattle. In this study, we provide a comprehensive characterization of DD and healthy skin microbiota of feedlot beef cattle. We also developed and validated a novel multiplex quantitative PCR (qPCR) assay to quantify the distribution of DD-associated bacterial species across DD lesion stages. We determined the DD-associated microbiota with deep amplicon sequencing of the V3-V4 hypervariable region of the 16S rRNA gene, followed by the application of novel and existing qPCR assays to quantify species distributions of Treponema, Porphyromonas, Fusobacterium, and Bacteroides across lesion stages. Deep amplicon sequencing revealed that Treponema, Mycoplasma, Porphyromonas, and Fusobacterium were associated with DD lesions. Culturing of DD biopsy specimens identified Porphyromonas levii, Bacteroides pyogenes, and two Fusobacterium spp. within DD lesions. Using species-specific qPCR on DD lesion DNA, we identified P. levii in 100% of active lesion stages. Early-stage lesions were particularly associated with Treponema medium, T. phagedenis, and P. levii. This study suggests a core DD microbial group consisting of species of Treponema, Fusobacterium, Porphyromonas, and Bacteroides, which may be closely tied with the etiopathogenesis of DD. Further characterizations of these species and Mycoplasma spp. are necessary to understand the microbial factors involved in DD pathogenesis, which will help elucidate DD etiology and facilitate more targeted and effective mitigation and treatment strategies. IMPORTANCE Previous work, primarily in dairy cattle, has identified various taxa associated with digital dermatitis (DD) lesions. However, there is a significant gap in our knowledge of DD microbiology in beef cattle. In addition, characterization of bacteria at the species level in DD lesions is limited. In this study, we provide a framework for the accurate and reproducible quantification of major DD-associated bacterial species from DNA samples. Our findings support DD as a polymicrobial infection, and we identified a variety of bacterial species spanning multiple genera that are consistently associated with DD lesions. The DD-associated microbiota identified in this study may be capable of inducing the formation and progression of DD lesions and thus should be primary targets in future DD pathogenesis studies.

SUBMITTER: Caddey B

PROVIDER: S-EPMC8409723 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:BACKGROUND: Bovine papillomatous digital dermatitis (DD) is the leading cause of lameness in dairy cattle and represents a serious welfare and economic burden. Found primarily in high production dairy cattle worldwide, DD is characterized by the development of an often painful red, raw ulcerative or papillomatous lesion frequently located near the interdigital cleft and above the bulbs of the heel. While the exact etiology is unknown, several spirochete species have been isolated from lesion material. Four isolates of Treponema phagedenis-like spirochetes were isolated from dairy cows in Iowa. Given the distinct differences in host, environmental niche, and disease association, a closer analysis of phenotypic characteristics, growth characteristics, and genomic sequences of T. phagedenis, a human genitalia commensal, and the Iowa DD isolates was undertaken. RESULTS: Phenotypically, these isolates range from 8.0 to 9.7 ?m in length with 6-8 flagella on each end. These isolates, like T. phagedenis, are strictly anaerobic, require serum and volatile fatty acids for growth, and are capable of fermenting fructose, mannitol, pectin, mannose, ribose, maltose, and glucose. Major glucose fermentation products produced are formate, acetate, and butyrate. Further study was conducted with a single isolate, 4A, showing an optimal growth pH of 7.0 (range of 6-8.5) and an optimal growth temperature of 40 °C (range of 29 °C-43 °C). Comparison of partial genomic contigs of isolate 4A and contigs of T. phagedenis F0421 revealed > 95% amino acid sequence identity with amino acid sequence of 4A. In silico DNA-DNA whole genome hybridization and BLAT analysis indicated a DDH estimate of >80% between isolate 4A and T. phagedenis F0421, and estimates of 52.5% or less when compared to the fully sequenced genomes of other treponeme species. CONCLUSION: Using both physiological, biochemical and genomic analysis, there is a lack of evidence for difference between T. phagedenis and isolate 4A. The description of Treponema phagedenis should be expanded from human genital skin commensal to include being an inhabitant within DD lesions in cattle.

Project description:The nasopharyngeal (NP) microbiota is important in defining respiratory health in feedlot cattle, with certain NP commensals potentially protecting against bovine respiratory disease (BRD) pathogens. In the present study, we evaluated longitudinal changes in the NP microbiota with a focus on lactic acid-producing bacteria (LAB) and their linkage with BRD-associated bacteria in steers (n = 13) that were first transported to an auction market, and then to a feedlot. Deep nasopharyngeal swabs were collected at the farm before transportation to the auction market (day 0), at feedlot placement (day 2), and 5 (day 7) and 12 (day 14) days after feedlot placement. Swabs were processed for the assessment of the NP microbiota using 16S rRNA gene sequencing, and for the detection of Mannheimia haemolytica, Pasteurella multocida, and Histophilus somni by culturing. Possible associations among the top 15 most relatively abundant bacterial genera were predicted using a stepwise-selected generalized linear mixed model. Correlations between LAB and BRD-associated Pasteurellaceae families were also assessed. In addition, antimicrobial activity of selected LAB isolates against M. haemolytica was evaluated in vitro. A noticeable shift was observed in the NP microbial community structure, and in the relative abundance of LAB families as a result of auction market exposure, transport and feedlot placement. Varying degrees of positive or negative associations between the 15 most relatively abundant genera were observed. Many of the LAB families were inversely correlated with the BRD-associated Pasteurellaceae family as the cattle were transported to the auction market and then to the feedlot. Nearly all steers were culture-negative for M. haemolytica and H. somni, and P. multocida became less prevalent after feedlot placement. Isolates from the Lactobacillaceae, Streptococcaceae, and Enterococcaceae families inhibited the growth of M. haemolytica. The results of this study indicated that the NP microbiota became more diverse with an increase in microbial richness following transport to an auction market and feedlot. This study provides evidence of potential cooperation and exclusion taking place in the respiratory microbial community of cattle which may be useful for developing microbial-based strategies to mitigate BRD.

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Identification and Quantification of Bovine Digital Dermatitis-Associated Microbiota across Lesion Stages in Feedlot Beef Cattle.

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