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Characterization of novel bovine gastrointestinal tract Treponema isolates and comparison with bovine digital dermatitis treponemes.

ABSTRACT: This study aimed to isolate and characterize treponemes present in the bovine gastrointestinal (GI) tract and compare them with bovine digital dermatitis (BDD) treponemes. Seven spirochete isolates were obtained from the bovine GI tract, which, on the basis of 16S rRNA gene comparisons, clustered within the genus Treponema as four novel phylotypes. One phylotype was isolated from several different GI tract regions, including the omasum, colon, rumen, and rectum. These four phylotypes could be divided into two phylotype pairs that clustered closest with each other and then with different, previously reported rumen treponemes. The treponemes displayed great genotypic and phenotypic diversity between phylotypes and differed considerably from named treponeme species and those recently reported by metagenomic studies of the bovine GI tract. Phylogenetic inference, based on comparisons of 16S rRNA sequences from only bovine treponemes, suggested a marked divergence between two important groups. The dendrogram formed two major clusters, with one cluster containing GI tract treponemes and the other containing BDD treponemes. This division among the bovine treponemes is likely the result of adaptation to different niches. To further differentiate the bovine GI and BDD strains, we designed a degenerate PCR for a gene encoding a putative virulence factor, tlyC, which gave a positive reaction only for treponemes from the BDD cluster.

SUBMITTER: Evans NJ

PROVIDER: S-EPMC3019712 | biostudies-literature | 2011 Jan

REPOSITORIES: biostudies-literature

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Characterization of novel bovine gastrointestinal tract Treponema isolates and comparison with bovine digital dermatitis treponemes.

Evans Nicholas J NJ Brown Jennifer M JM Murray Richard D RD Getty Brian B Birtles Richard J RJ Hart C Anthony CA Carter Stuart D SD

Applied and environmental microbiology 20101105 1

This study aimed to isolate and characterize treponemes present in the bovine gastrointestinal (GI) tract and compare them with bovine digital dermatitis (BDD) treponemes. Seven spirochete isolates were obtained from the bovine GI tract, which, on the basis of 16S rRNA gene comparisons, clustered within the genus Treponema as four novel phylotypes. One phylotype was isolated from several different GI tract regions, including the omasum, colon, rumen, and rectum. These four phylotypes could be di ...[more]

PMID: 21057019

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Project description:Bovine digital dermatitis (BDD) is a common infectious disease of digital skin in cattle and an important cause of lameness worldwide, with limited treatment options. It is of increasing global concern for both animal welfare and food security, imposing a large economic burden on cattle farming industries each year. A polytreponemal etiology has been consistently identified, with three key phylogroups implicated globally: Treponema medium, Treponema phagedenis, and Treponema pedis. Pathogenic mechanisms which might enable targeted treatment/therapeutic development are poorly defined. This study used RNA sequencing to determine global differential mRNA expression in primary bovine foot skin fibroblasts following challenge with three representative BDD treponemes and a commensal treponeme, Treponema ruminis. A pro-inflammatory response was elicited by the BDD treponemes, mediated through IL-8/IL-17 signaling. Unexpectedly, the three BDD treponemes elicited distinct mechanisms of pathogenesis. T. phagedenis and T. pedis increased abundance of mRNA transcripts associated with apoptosis, while T. medium and T. pedis increased transcripts involved in actin rearrangement and loss of cell adhesion, likely promoting tissue invasion. The upregulation of antimicrobial peptide precursor, DEFB123, by T. phagedenis spirochaetes may present a microbial ecological advantage to all treponemes within BDD infected tissue, explaining their dominance within lesions. A commensal, T. ruminis, significantly dysregulated over three times the number of host mRNA transcripts compared to BDD treponemes, implying BDD treponemes, akin to the syphilis pathogen (Treponema pallidum), have evolved as "stealth pathogens" which avoid triggering substantial host immune/inflammatory responses to enable persistence and tissue invasion. Immunohistochemistry demonstrated increased IL-6, IL-8, RND1, and CFB protein expression in BDD lesions, confirming in vitro fibroblast observations and highlighting the system's value in modeling BDD pathogenesis. Several unique shared gene targets were identified, particularly RGS16, GRO1, MAFF, and ZC3H12A. The three key BDD Treponema phylogroups elicited both distinct and shared pathogenic mechanisms in bovine foot skin; upregulating inflammation whilst simultaneously suppressing adaptive immunity. The novel gene targets identified here should enable future vaccine/therapeutic approaches.

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:Purpose, aims and objectives: Bovine digital dermatitis (BDD) is a painful and ulcerative, inflammatory, infectious disease of digital skin in dairy and beef cattle and is one of the most economically important causes of severe cattle lameness worldwide. A polytreponemal aetiology has been consistently implicated in BDD pathogenesis with three key phylogroups implicated globally: Treponema medium, Treponema phagedenis and Treponema pedis. This study aimed to investigate the hypothesis that the three Treponema phylogroups implement distict mechanisms of pathogenesis within cells of the bovine foot skin tissue during infection. Using a next generation RNA sequencing (RNA-Seq) approach, the dysregulation of global mRNA expression was investigated in primary bovine foot skin fibroblasts following challenge with representative strains of the three predominant BDD Treponema phylogroups (T19, T320A and T3552B respectively). Transcriptome profiles were compared to that of a commensal treponeme, Treponema ruminis strain Ru1, in attempts to identify pathogenic signatures. Results and conclusions: Here, for the first time, we implicate fibroblasts as a likely source of interleukin-8 dysregulation in BDD lesions. Despite treponemes reportedly having atypical LPS, a strong pro-inflammatory response was elicited by the BDD treponemes in a similar manner to the Gram-negative LPS control, which appeared to be mediated through interleukin-17 signalling. Along with interleukin-17, several interesting gene targets were identified which may help to inform and drive future vaccine development and therapeutic approaches; particularly those of RGS16, GRO1, MAFF and ZC3H12A, which were only stimulated by BDD treponemes. Interestingly, the three BDD treponemes were found to elicit very distinct mechanisms of pathogenesis in fibroblasts. T. phagedenis and T. pedis spirochaetes were found to upregulate several genes associated with apoptosis. Both T. medium and T. pedis spirochaetes, but notably not T. phagedenis, stimulated genes associated with actin rearrangement and a loss of cell adhesion, which may promote their persistence and deeper invasion within host tissues. The upregulation of antimicrobial peptide precursor, DEFB123, by T. phagedenis spirochaetes may present a microbial ecological advantage to all treponemes within BDD infected tissue, explaining their dominance within lesions. Interestingly, T. medium phylogroup was the least stimulatory and appeared to induce immunosuppression via the dysregulation of genes such as TSC22D3. Together with findings that the commensal, T. ruminis, significantly dysregulated over three times the number of host genes compared to each BDD treponeme; this suggests that, alike the syphilis pathogen (Treponema pallidum), BDD treponemes have evolved to become “stealth pathogens” and avoid triggering a substantial host immune/inflammatory response to promote persistence and facilitate invasion of host tissues. Overall, this study has highlighted the complexities of BDD pathogenesis; three key Treponema phylogroups appear to elicit very distinct mechanisms of pathogenesis in bovine foot skin cells. Several interesting gene targets have been identified from this study which may help to inform and drive future vaccine development and therapeutic approaches.

Dataset Information

Characterization of novel bovine gastrointestinal tract Treponema isolates and comparison with bovine digital dermatitis treponemes.

Publications

Characterization of novel bovine gastrointestinal tract Treponema isolates and comparison with bovine digital dermatitis treponemes.

Similar Datasets

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