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Peptide ELISA and FRET-Qpcr Identified a Significantly Higher Prevalence of Chlamydia Suis in Domestic Pigs Than in Feral Swine from the State of Alabama, USA

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Peptide ELISA and FRET-Qpcr Identified a Significantly Higher Prevalence of Chlamydia Suis in Domestic Pigs Than in Feral Swine from the State of Alabama, USA University of Nebraska - Lincoln DigitalCommons@University of Nebraska - Lincoln USDA National Wildlife Research Center - Staff U.S. Department of Agriculture: Animal and Publications Plant Health Inspection Service 2021 Peptide ELISA and FRET-qPCR Identified a Significantly Higher Prevalence of Chlamydia suis in Domestic Pigs Than in Feral Swine from the State of Alabama, USA Md Monirul Hoque Folasade Adekanmbi Subarna Barua Kh. Shamsur Rahman Virginia Aida See next page for additional authors Follow this and additional works at: https://digitalcommons.unl.edu/icwdm_usdanwrc Part of the Natural Resources and Conservation Commons, Natural Resources Management and Policy Commons, Other Environmental Sciences Commons, Other Veterinary Medicine Commons, Population Biology Commons, Terrestrial and Aquatic Ecology Commons, Veterinary Infectious Diseases Commons, Veterinary Microbiology and Immunobiology Commons, Veterinary Preventive Medicine, Epidemiology, and Public Health Commons, and the Zoology Commons This Article is brought to you for free and open access by the U.S. Department of Agriculture: Animal and Plant Health Inspection Service at DigitalCommons@University of Nebraska - Lincoln. It has been accepted for inclusion in USDA National Wildlife Research Center - Staff Publications by an authorized administrator of DigitalCommons@University of Nebraska - Lincoln. Authors Md Monirul Hoque, Folasade Adekanmbi, Subarna Barua, Kh. Shamsur Rahman, Virginia Aida, Brian Anderson, Anil Poudel, Anwar Kalalah, Sara Bolds, Steven Madere, Steven Kitchens, Stuart Price, Vienna Brown, B. Graeme Lockaby, Constantinos S. Kyriakis, Bernhard Kaltenboeck, and Chengming Wang pathogens Article Peptide ELISA and FRET-qPCR Identified a Significantly Higher Prevalence of Chlamydia suis in Domestic Pigs Than in Feral Swine from the State of Alabama, USA Md Monirul Hoque 1 , Folasade Adekanmbi 1, Subarna Barua 1, Kh. Shamsur Rahman 1, Virginia Aida 1, Brian Anderson 2, Anil Poudel 1, Anwar Kalalah 1, Sara Bolds 3 , Steven Madere 3, Steven Kitchens 1, Stuart Price 1, Vienna Brown 4, B. Graeme Lockaby 3, Constantinos S. Kyriakis 1, Bernhard Kaltenboeck 1 and Chengming Wang 1,* 1 College of Veterinary Medicine, Auburn University, Auburn, AL 36849, USA; [email protected] (M.M.H.); [email protected] (F.A.); [email protected] (S.B.); [email protected] (K.S.R.); [email protected] (V.A.); [email protected] (A.P.); [email protected] (A.K.); [email protected] (S.K.); [email protected] (S.P.); [email protected] (C.S.K.); [email protected] (B.K.) 2 Swine Research and Education Center, Auburn University, Auburn, AL 36830, USA; [email protected] 3 School of Forestry and Wildlife Sciences, Auburn University, Auburn, AL 36849, USA; [email protected] (S.B.); [email protected] (S.M.); [email protected] (B.G.L.) 4 National Feral Swine Damage Management Program, Wildlife Services, Animal and Plant Health Inspection Service, United States Department of Agriculture, Fort Collins, CO 80521, USA; [email protected] * Correspondence: [email protected] Abstract: Chlamydia suis is an important, highly prevalent, and diverse obligate intracellular pathogen infecting pigs. In order to investigate the prevalence and diversity of C. suis in the U.S., 276 whole blood samples from feral swine were collected as well as 109 fecal swabs and 60 whole blood samples Citation: Hoque, M.M.; Adekanmbi, F.; from domestic pigs. C. suis-specific peptide ELISA identified anti-C. suis antibodies in 13.0% of Barua, S.; Rahman, K.S.; Aida, V.; the blood of feral swine (26/276) and 80.0% of the domestic pigs (48/60). FRET-qPCR and DNA Anderson, B.; Poudel, A.; Kalalah, A.; sequencing found C. suis DNA in 99.1% of the fecal swabs (108/109) and 21.7% of the whole blood Bolds, S.; Madere, S.; et al. Peptide (13/60) of the domestic pigs, but not in any of the assayed blood samples (0/267) in feral swine. ELISA and FRET-qPCR Identified a Phylogenetic comparison of partial C. suis ompA gene sequences and C. suis-specific multilocus Significantly Higher Prevalence of sequencing typing (MLST) revealed significant genetic diversity of the C. suis identified in this study. Chlamydia suis in Domestic Pigs Than Highly genetically diverse C. suis strains are prevalent in domestic pigs in the USA. As crowding in Feral Swine from the State of strongly enhances the frequency and intensity of highly prevalent Chlamydia infections in animals, Alabama, USA. Pathogens 2021, 10, 11. less population density in feral swine than in domestic pigs may explain the significantly lower https://dx.doi.org/10.3390/ C. suis prevalence in feral swine. A future study is warranted to obtain C. suis DNA from feral swine pathogens10010011 to perform genetic diversity of C. suis between commercial and feral pigs. Received: 10 December 2020 Accepted: 22 December 2020 Keywords: Chlamydia suis; peptide ELISA; PCR; feral swine; USA Published: 25 December 2020 Publisher’s Note: MDPI stays neu- tral with regard to jurisdictional claims 1. Introduction in published maps and institutional Obligate intracellular bacteria of genus Chlamydia contains 13 recognized species affiliations. (C. abortus, C. avium, C. caviae, C. felis, C. gallinacea, C. muridarum, C. pecorum, C. pneumoniae, C. poikilotermis, C. psittaci, C. serpentis, C. suis, and C. trachomatis)[1,2]. Of all thirteen chlamydial species, only five (C. suis, C. abortus, C. pecorum, C. psittaci and C. trachomatis) Copyright: © 2020 by the authors. Li- are known to infect pigs [3,4]. The pig is the only known natural host of C. suis, and censee MDPI, Basel, Switzerland. This C. suis infections in pigs have been reported to be associated with a variety of clinical signs article is an open access article distributed including conjunctivitis, rhinitis, pneumonia, enteritis, and reproductive disorders [4–7]. under the terms and conditions of the However, most recent reports also demonstrated asymptomatic C. suis infections in pigs in Creative Commons Attribution (CC BY) Austria, Belgium, China, Germany, Japan, Italy, and Switzerland [7–11]. license (https://creativecommons.org/ Feral swine are considered to be the single most invasive animal species in the United licenses/by/4.0/). States and have expanded from 17 to 38 states in the last 30 years [12]. In the state of Pathogens 2021, 10, 11. https://dx.doi.org/10.3390/pathogens10010011 https://www.mdpi.com/journal/pathogens Pathogens 2021, 10, x FOR PEER REVIEW 2 of 10 infections in pigs have been reported to be associated with a variety of clinical signs in- cluding conjunctivitis, rhinitis, pneumonia, enteritis, and reproductive disorders [4–7]. However, most recent reports also demonstrated asymptomatic C. suis infections in pigs in Austria, Belgium, China, Germany, Japan, Italy, and Switzerland [7–11]. Pathogens 2021, 10, 11 2 of 10 Feral swine are considered to be the single most invasive animal species in the United States and have expanded from 17 to 38 states in the last 30 years [12]. In the state of Ala- bama,Alabama, the thehome home range range of feral of feral swine swine has has also also spread spread to to all all 67 67 counties counties [13]. [13]. It It has has been been reportedreported that that there there is is a a high high probability probability of of interaction interaction between between domestic domestic pigs pigs having having out- out- doordoor access access and and feral feral swine swine in in certain certain geograph geographicic regions. regions. Close Close contact contact between between domestic domestic pigspigs and and feral feral swine swine is is considered a risk factor for transmission of pathogens, including C.C. suis suis [14].[14]. Wahdan Wahdan et et al. al. reported reported a a low low prevalence prevalence of of ChlamydiaChlamydia DNADNA in in the the investigated investigated feralferal swine swine populations populations (1.4%, (1.4%, 4/292) in in Switzerland. Switzerland. In In addition, addition, microimmunofluores- microimmunofluores- cencecence test test was was performed performed to to test test for for antibodies antibodies to to ChlamydiaChlamydia spp.spp. in in sera sera from from hunter-killed hunter-killed feralferal swine swine harvested harvested during during the the 2006–2009 2006–2009 hu huntingnting seasons seasons in in three three Italian Italian regions, regions, and 63.6%63.6% (110/173) (110/173) tested tested sera sera were were shown shown to to have have antibody antibody titers titers to to chlamydiae chlamydiae >1:32 >1:32 [15]. [15]. WhileWhile C.C. suis suis waswas isolated isolated from from domestic domestic pigs pigs in the the USA USA [5,16], [5,16], little little is is known known about about thethe prevalence prevalence and and diversity diversity of of C.C. suis suis inin pigs pigs in in the the USA. USA. Therefore, Therefore, the the present present study study waswas undertaken undertaken to to investigate investigate the the molecular molecular and and serological serological prevalence prevalence of of C.C. suis suis inin feral feral andand domestic domestic pigs pigs in in Alabama. Alabama. In In addition, addition, phylogenetic phylogenetic analysis analysis using using both both ompAompA andand a C.C. suis suis-specific-specific MLST MLST typing typing scheme scheme was performed to analyze the C. suis diversity. 2.2. Results Results C.C. suis suis-specific-specific peptide peptide ELISA ELISA determined determined a a sign significantlyificantly higher higher prevalence prevalence of of anti- anti- C.C. suis suis antibodiesantibodies in in domestic domestic pigs pigs than than in inthe the feral feral swine. swine. The Theanti- anti-C. suisC. antibody suis antibody was detectedwas detected in 13.0% in 13.0% (240/276) (240/276) of whole of blood whole samples blood samples in the feral in theswine, feral being swine, significantly being sig- −4 lowernificantly than lower80.0% thanpositivity 80.0% (12/60) positivity in domestic (12/60) pigs in domestic (Figure 1A) pigs (p (Figure< 10−4).
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