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Identification of Conditionally Essential Genes for Streptococcus Suis Infection in Pigs

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Identification of Conditionally Essential Genes for Streptococcus Suis Infection in Pigs Virulence ISSN: (Print) (Online) Journal homepage: https://www.tandfonline.com/loi/kvir20 Identification of conditionally essential genes for Streptococcus suis infection in pigs Jesús Arenas , Aldert Zomer , Jose Harders-Westerveen , Hester J. Bootsma , Marien I. De Jonge , Norbert Stockhofe-Zurwieden , Hilde E. Smith & Astrid De Greeff To cite this article: Jesús Arenas , Aldert Zomer , Jose Harders-Westerveen , Hester J. Bootsma , Marien I. De Jonge , Norbert Stockhofe-Zurwieden , Hilde E. Smith & Astrid De Greeff (2020) Identification of conditionally essential genes for Streptococcussuis infection in pigs, Virulence, 11:1, 446-464, DOI: 10.1080/21505594.2020.1764173 To link to this article: https://doi.org/10.1080/21505594.2020.1764173 © 2020 The Author(s). Published by Informa View supplementary material UK Limited, trading as Taylor & Francis Group. Published online: 18 May 2020. Submit your article to this journal Article views: 201 View related articles View Crossmark data Full Terms & Conditions of access and use can be found at https://www.tandfonline.com/action/journalInformation?journalCode=kvir20 VIRULENCE 2020, VOL. 11, NO. 1, 446–464 https://doi.org/10.1080/21505594.2020.1764173 RESEARCH PAPER Identification of conditionally essential genes for Streptococcus suis infection in pigs Jesús Arenas a,b, Aldert Zomer c,d, Jose Harders-Westerveena, Hester J. Bootsmad, Marien I. De Jonged, Norbert Stockhofe-Zurwiedena, Hilde E. Smitha, and Astrid De Greeff a aDepartment of Infection Biology, Wageningen Bioveterinary Research (WBVR), Lelystad, The Netherlands; bUnit of Microbiology and Immunology, Faculty of Veterinary, University of Zaragoza, Zaragoza, Spain; cDepartment of Infectious Diseases and Immunology, Faculty of Veterinary Medicine, Utrecht University, Utrecht, The Netherlands; dSection Pediatric Infectious Diseases, Laboratory of Medical Immunology, Radboud, Institute for Molecular Life Sciences, Radboudumc, Nijmegen, The Netherlands ABSTRACT ARTICLE HISTORY Streptococcus suis is a Gram-positive bacterium and zoonotic pathogen that causes meningitis and Received 27 November 2019 sepsis in pigs and humans. The aim of this study was to identify genes required for S. suis infection. We Revised 14 March 2020 created Tn-Seq libraries in a virulent S. suis strain10,whichwasusedtoinoculate pigs in an intrathecal Accepted 10 April 2020 experimental infection. Comparative analysis of the relative abundance of mutants recovered from KEYWORDS different sites of infection (blood, cerebrospinal fluid, and meninges of the brain) identified 361 Streptococcus suis; conditionally essential genes, i.e. required for infection, which is about 18% of the genome. The pathogenesis; zoonotic conditionally essential genes were primarily involved in metabolic and transport processes, regulation, pathogen; infection; ribosomal structure and biogenesis, transcription, and cell wall membrane and envelope biogenesis, transposon mutagenesis; Tn- stress defenses, and immune evasion. Directed mutants were created in a set of 10 genes of different Seq genetic ontologies and their role was determined in ex vivo models. Mutants showed different levels of sensitivity to survival in whole blood, serum, cerebrospinal fluid, thermic shock, and stress conditions, as compared to the wild type. Additionally, the role of three selected mutants was validated in co-infection experiments in which pigs were infected with both wild type and isogenic mutant strains. The genetic determinants of infection identified in this work contribute to novel insights in S. suis pathogenesis and could serve as targets for novel vaccines or antimicrobial drugs. Introduction present in the bacterin and are not equally efficacious for all Streptococcus suis is the major etiological agent of strep- serotypes [4]. Alternatives are live attenuated or subunit- tococcal disease in pigs, a systemic infection that is the based vaccines. Several live-attenuated vaccine strategies major cause of morbidity and mortality in young pigs were described; including those based on auxotrophic leading to significant economic losses to the swine indus- mutants for aromatic amino acids [5], or mutants lacking try worldwide. The bacterium resides asymptomatically virulence-associated factors [6,7]. In general, these vaccine in the oropharynx, gut, and genitals of pigs as part of the preparations show a better efficacy than bacterins; however, microbiota. Particularly during the nursery period in there are sometimes concerns regarding safety when the piglets of 4 to 10 weeks old, S. suis can cross dermal and mutant is not fully attenuated [8,9]. Interestingly, a low mucosal barriers and reach the bloodstream causing virulent strain XS05 and a double mutant in two surface- arthritis, sepsis, meningitis, and other pathologies [1,2]. exposed proteins (SspepO and SspspC) were recently used S. suis can also infect humans and is one of the most as live vaccines [10,11], and induced protection against common causes of meningitis in pork-consuming coun- challenge experiments with strains of different serotypes, tries in Asia [3]. The rapid onset of disease together with indicating that these are promising vaccine candidates. In the emergence of multidrug-resistant strains makes ade- contrast to live-attenuated vaccines, subunit-based vaccines quate treatment and control difficult. are safe; however, costs are the main drawback for their Vaccination is used extensively to prevent S. suis infec- further development. In addition, the high diversity of cell tions. Current immunization strategies focus on commer- surface structures in S. suis makesitdifficulttoidentify cial and autologous whole-cell bacterins. These vaccine protective antigens common to all, while the identification formulations only induce protection against the serotype of one or a combination of universal antigens is required to CONTACT Jesús Arenas [email protected] Supplemental data for this article can be accessed here. © 2020 The Author(s). Published by Informa UK Limited, trading as Taylor & Francis Group. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. VIRULENCE 447 develop a broad protective formulation. Although several fluoride or 3 mM H2O2, incubated in a Bioscreen promising subunit vaccine candidates have been described, C instrument (Thermo Scientific) at 34°C, 37°C, or 42°C there is not yet a commercial cross-protecting vaccine on and the optical density at 600 nm was monitored every the market. 20 min. For studying the growth of the bacteria in different Conditionally essential genes required for S. suis infection host fluids, overnight THB cultures were diluted to around representattractivetargetsforthedesignofsubunitorlive- 106 CFU/ml in Dulbecco’s phosphate-buffered saline, and attenuated vaccines and other innovative interventions. The bacteria were inoculated in fresh porcine blood, 100% main discovery approach for novel antigens has been labor commercial porcine serum (Sigma-Aldrich) or porcine intensive focusing on a few genes. A non-biased and sys- cerebrospinal fluid (CSF) and incubated at 37°C and 5% of – tematic selective method requires the creation of large CO2. Blood and CSF were collected from healthy 3 6- libraries of mutants combined with genome-wide screens week-old specified pathogen-free piglets from a high health using hybridization [12], footprinting [13], or next- farm, as piglets are most at risk for streptococcal suis generation sequencing (Tn-Seq) [14]. In Tn-Seq, the gene infection at 4–10 weeks. Bacterial survival was monitored function of each mutated gene is disrupted by random by CFU counting using solid agar plates. insertion of a transposon into the gene. The resulting Tn- Seq library is subjected to selective conditions where the Preparation of S. suis Tn-Seq libraries relative abundance of every mutant in the pooled population is compared between the pooled input library and the out- S. suis strain 10 mariner transposon mutant libraries were put population after exposure to the selective condition. prepared as described previously for S. pneumoniae [18], Variation in the abundance of the mutants between input except for the procedure of S. suis transformation [19]. and output, e.g. after different growth conditions, indicates Briefly, 0.52–1 µg/ml of purified genomic DNA of S. suis the relevance of genetic regions for the fitness of bacteria strain 10 was incubated with a similar amount of Himar under the selective condition. Tn-Seq has been successfully I mariner transposon in the presence of purified transpo- applied to identify sets of conditionally essential genes in sase at 30°C for 4 h. Mutagenized genomic DNA was more than 40 microorganisms, including diverse repaired with T4 DNA polymerase and E. coli DNA ligase. Streptococcus species [14–16], an important evidence base 10 µl of the ligation mixture (approximately 1 µg/ml) was that this approach could also be applied to S. suis. used for transformation of 100 µl of S. suis strain 10 using The goal of this work was to identify genes of S. suis that the previously described peptide-induced competence sys- are conditionally essential during infection of pigs using tem [19], plated on THB-agar plates with spectinomycin Tn-Seq. A large number of putative essential genes were (100 µg/ml) and incubated for
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