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. 2024 Aug 13;92(8):e0011724.
doi: 10.1128/iai.00117-24. Epub 2024 Jun 28.

Adherence and metal-ion acquisition gene expression increases during infection with Treponema phagedenis strains from bovine digital dermatitis

Colton Scott  1 , Angelica P Dias  1 , Jeroen De Buck  1
Affiliations

Adherence and metal-ion acquisition gene expression increases during infection with Treponema phagedenis strains from bovine digital dermatitis

Colton Scott et al. Infect Immun. .

Abstract

Digital dermatitis (DD) is an ulcerative foot lesion on the heel bulbs of dairy cattle. DD is a polymicrobial disease with no precise etiology, although Treponema spirochetes are found disproportionally abundant in diseased tissue. Within Treponema, several different species are found in DD; however, the species Treponema phagedenis is uniformly found in copious quantities and deep within the skin layers of the active, ulcerative stages of disease. The pathogenic mechanisms these bacteria use to persist in the skin and the precise role they play in the pathology of DD are widely unknown. To explore the pathogenesis and virulence of Treponema phagedenis, newly isolated strains of this species were investigated in a subcutaneous murine abscess model. In the first trial, a dosage study was conducted to compare the pathogenicity of different strains across three different treponemes per inoculum (TPI) doses based on abscess volumes. In the second trial, the expression levels of 11 putative virulence genes were obtained to gain insight into their involvement in pathogenesis. During the RT-qPCR analysis, it was determined that genes encoding for two metal-ion import lipoproteins and two adherence genes were found highly upregulated during infection. Conversely, two genes involved in motility and chemotaxis were found to not be significantly upregulated or utilized during infection. These results were supported by gene expression data from natural M2 lesions of dairy cattle. This gene expression analysis could highlight the preference in strategy for T. phagedenis to persist and adhere in the host rather than engage in motility and disseminate.

Keywords: Treponema phagedenis; bovine; dairy; digital dermatitis; lameness; murine model.

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Conflict of interest statement

The authors declare no conflict of interest.

Figures

Fig 1
Fig 1
Subcutaneous abscess volumes following infection challenge with eight Treponema phagedenis strains and formalin-killed (F-K) control. Abscess sizes were averaged from n = 6 infection groups. For all three doses, strain 11 was used as the F-K control. (A) Lesion size (mm3) for lowest infectious dose of 1.25 × 109 TPI. (B) Lesion size for an intermediate dose of 5 × 109 TPI. (C) Lesion size for the highest dose of 2 × 1010 TPI. The top of each bar represents the mean average lesion size for each strain and the whiskers span the standard deviation of each sample set. Individual data points are highlighted as scatter dots. Statistical significance lines are presented as follows: *P < 0.05, **P < 0.01, ***P < 0.001, ****P < 0.0001.
Fig 2
Fig 2
Gene expression heat map of 11 putative virulence genes from six T. phagedenis strains following infection in a murine model. Expression fold changes were calculated via 2−ΔΔCt method, and abscess Ct data were compared against in vitro Ct data. Fold changes were then log2 transformed.
Fig 3
Fig 3
Quantities of T. phagedenis strains found in In vitro (cell pellets) and in in vivo (abscesses) samples. Cell quantities are expressed as log10 genome equivalents (GE) obtained from species-specific qPCR. Bars represent the mean average log10 GE for each sample set and error bars indicate standard deviation. Statistical significance was calculated from multiple unpaired t-tests between in vitro and in vivo groups. Statistical significance lines are presented as follows: *P < 0.05, **P < 0.01, ****P < 0.0001, ns as non-significant.
Fig 4
Fig 4
Phylogenetic tree of the eight isolated T. phagedenis strains. The tree was constructed in PhyloPhlAn and is presented in a circular format. The tree is rooted to the reference strain B43.1T. The scale bar of 0.10 shows the length of each vertical branch and corresponds to the phylogenetic distance of 0.1 nucleotide substitutions per site or 10% nucleotide sequence deviation.
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