Genetic Diversity and Antimicrobial Susceptibility of Campylobacter jejuni Isolates Associated with Sheep Abortion in the United States and Great Britain

Wu, Zhongliang; Sippy, Rachel; Şahin, Orhan; Plummer, Paul J.; Vidal, Ana Maria Centola; Newell, Diane G.; Zhang, Qijing

doi:10.1128/jcm.00355-14

Cited by 44 publications

(54 citation statements)

References 42 publications

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“…fetus as the predominant cause of ovine abortion outbreaks in the United States. Considering the high genetic diversity of Campylobacter species and the strains responsible for sheep abortion in the United States prior to the predominance of the SA clone (5)(6)(7)(8), this finding was unexpected and indicates that clone SA has evolved to possess novel virulence traits that may have been favored or selected by current agricultural practices in sheep production. In contrast, Campylobacter isolates from sheep abortions in Great Britain and New Zealand remain genetically diverse and comprise both species (predominantly C. fetus subsp.…”

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confidence: 61%

“…In contrast, Campylobacter isolates from sheep abortions in Great Britain and New Zealand remain genetically diverse and comprise both species (predominantly C. fetus subsp. fetus) (5,9). The hypervirulence of clone SA in the induction of abortion was confirmed in a pregnant guinea pig model, in which it showed a distinct abortifacient ability compared with other C. jejuni strains (10).…”

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confidence: 74%

“…doylei 269.97, C. jejuni G1, and C. jejuni strain X) that were associated with systemic infection, bacteremia, and severe bloody diarrhea (19,20), suggesting the existence of a link between a particular capsular structure and the disease phenotype. This possibility was further substantiated by the observation that C. jejuni isolates belonging to clone SA had a homogenous CPS structure, as suggested by DNA microarray analysis of sheep abortion strains (5).…”

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confidence: 75%

“…Ovine abortion poses a major economic burden on sheep producers worldwide, and C. jejuni clone SA has been consistently the predominant cause of this important disease in the United States for over a decade (4,5). Whole-cell-based killed vaccines (along with antibiotics) have been used for the control of Campylobacter-associated abortions in sheep; however, their efficacy appears to be poor and varies widely in the United States (47,48).…”

Section: Discussionmentioning

confidence: 99%

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Key Role of Capsular Polysaccharide in the Induction of Systemic Infection and Abortion by Hypervirulent Campylobacter jejuni

et al. 2017

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Campylobacter jejuni is a zoonotic pathogen, and a hypervirulent clone, named clone SA, has recently emerged as the predominant cause of ovine abortion in the United States. To induce abortion, orally ingested Campylobacter must translocate across the intestinal epithelium, spread systemically in the circulation, and reach the fetoplacental tissue. Bacterial factors involved in these steps are not well understood. C. jejuni is known to produce capsular polysaccharide (CPS), but the specific role that CPS plays in systemic infection and particularly abortion in animals remains to be determined. In this study, we evaluated the role of CPS in bacteremia using a mouse model and in abortion using a pregnant guinea pig model following oral challenge. Compared with C. jejuni NCTC 11168 and 81-176, a clone SA isolate (IA3902) resulted in significantly higher bacterial counts and a significantly longer duration of bacteremia in mice. The loss of capsule production via gene-specific mutagenesis in IA3902 led to the complete abolishment of bacteremia in mice and abortion in pregnant guinea pigs, while complementation of capsule expression almost fully restored these phenotypes. The capsule mutant strain was also impaired for survival in guinea pig sera and sheep blood. Sequence-based analyses revealed that clone SA possesses a unique CPS locus with a mosaic structure, which has been stably maintained in all clone SA isolates derived from various hosts and times. These findings establish CPS as a key virulence factor for the induction of systemic infection and abortion in pregnant animals and provide a viable candidate for the development of vaccines against hypervirulent C. jejuni. KEYWORDS Campylobacter, capsule, systemic infection, abortion, sheep, bacteremiaA s a zoonotic pathogen, Campylobacter is a leading cause of bacterial foodborne gastroenteritis in humans (1). In addition, Campylobacter species have been recognized as one of the most common causes of ovine abortion in the United States and worldwide, with an overall abortion rate of 5 to 50% in affected flocks (2). As a consequence, Campylobacter poses a significant economic burden on sheep producers and greatly impacts sheep health and welfare. A national study, NAHMS Sheep 2001, conducted by the USDA/APHIS/Veterinary Services in collaboration with the American Sheep Industry Association revealed that Campylobacter species ranked first among all infectious causes of abortion within the last 3 years of the study, with 53.7% of the reported cases being confirmed by a veterinarian or diagnostic laboratory (3).Historically, Campylobacter fetus subsp. fetus accounted for the majority of the Campylobacter spp. associated with ovine abortion; however, we recently discovered a remarkable shift in the etiology of the disease (4, 5). Specifically, a highly virulent

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confidence: 61%

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confidence: 74%

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confidence: 75%

Section: Discussionmentioning

confidence: 99%

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Key Role of Capsular Polysaccharide in the Induction of Systemic Infection and Abortion by Hypervirulent Campylobacter jejuni

et al. 2017

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“…The most obvious genetic difference between the two strains is that IA3902 contains a pVir plasmid of 37,174 bp, while NCTC11168 does not. Even though a later study found that not all clone SA isolates harbor the pVir plasmid (Wu et al ., ), the potential role of pVir in virulence (Bacon et al ., ; Bacon et al ., ) prompted us to determine if it contributed to abortion induction by this hypervirulent C. jejuni strain. To determine the role of pVir in virulence, multiple methods were used to cure it from IA3902, but all failed.…”

Section: Introductionmentioning

confidence: 99%

Identification and functional analysis of two toxin–antitoxin systems in Campylobacter jejuni

Shen

Patil

Şahin

et al. 2016

Molecular Microbiology

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Toxin-antitoxin (TA) systems are widely distributed in bacteria and play an important role in maintaining plasmid stability. The leading foodborne pathogen, Campylobacter jejuni, can carry multiple plasmids associated with antibiotic resistance or virulence. Previously a virulence plasmid named pVir was identified in C. jejuni 81-176 and IA3902, but determining the role of pVir in pathogenesis has been hampered because the plasmid cannot be cured. In this study, we report the identification of two TA systems that are located on the pVir plasmid in 81-176 and IA3902, respectively. The virA (proteic antitoxin)/virT (proteic toxin) pair in IA3902 belongs to a Type II TA system, while the cjrA (RNA antitoxin)/cjpT (proteic toxin) pair in 81-176 belongs to a Type I TA system. Notably, cjrA (antitoxin) represents the first noncoding small RNA demonstrated to play a functional role in Campylobacter physiology to date. By inactivating the TA systems, pVir was readily cured from Campylobacter, indicating their functionality in Campylobacter. Using pVir-cured IA3902, we demonstrated that pVir is not required for abortion induction in the guinea pig model. These findings establish the key role of the TA systems in maintaining plasmid stability and provide a means to evaluate the function of pVir in Campylobacter pathobiology.

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Campylobacter species abortion in sheep

Smith,

Brzozowska,

Dempsey

2023

Veterinary Record

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Genetic Diversity and Antimicrobial Susceptibility of Campylobacter jejuni Isolates Associated with Sheep Abortion in the United States and Great Britain

Cited by 44 publications

References 42 publications

Key Role of Capsular Polysaccharide in the Induction of Systemic Infection and Abortion by Hypervirulent Campylobacter jejuni

Key Role of Capsular Polysaccharide in the Induction of Systemic Infection and Abortion by Hypervirulent Campylobacter jejuni

Identification and functional analysis of two toxin–antitoxin systems in Campylobacter jejuni

Campylobacter species abortion in sheep

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