The antimicrobial systems of Streptococcus suis promote niche competition in pig tonsils

References

• Goyette-Desjardins G, Auger JP, Xu J, et al. Streptococcus suis, an important pig pathogen and emerging zoonotic agent-an update on the worldwide distribution based on serotyping and sequence typing. Emerg Microbes Infect. 2014;3(6):e45. DOI:10.1038/emi.2014.45
   PubMed Web of Science ®Google Scholar
• Ferrando ML, de Greeff A, van Rooijen WJ, et al. Host-pathogen interaction at the intestinal Mucosa correlates with zoonotic potential of Streptococcus suis. J Infect Dis. 2015;212(1):95–105.
   PubMed Web of Science ®Google Scholar
• Segura M, Fittipaldi N, Calzas C, et al. Critical Streptococcus suis virulence factors: are they all really critical? Trends Microbiol. 2017;25(7):585–599. DOI:10.1016/j.tim.2017.02.005
   PubMed Web of Science ®Google Scholar
• Huang J, Liang Y, Guo D, et al. Comparative genomic analysis of the ICESa2603 family ICEs and spread of erm(b)- and tet(o)-carrying transferable 89K-subtype ICEs in Swine and Bovine Isolates in China. Front Microbiol. 2016;7:55.
   PubMed Web of Science ®Google Scholar
• Pan Z, Ma J, Dong W, et al. Novel variant serotype of Streptococcus suis isolated from piglets with meningitis. Appl Environ Microbiol. 2015;81(3):976–985.
   PubMed Web of Science ®Google Scholar
• Huang J, Liu X, Chen H, et al. Identification of six novel capsular polysaccharide loci (NCL) from Streptococcus suis multidrug resistant non-typeable strains and the pathogenic characteristic of strains carrying new NCLs. Transbound Emerg Dis. 2019;66(2):995–1003. DOI:10.1111/tbed.13123
   PubMed Web of Science ®Google Scholar
• Zheng H, Ji S, Liu Z, et al. Eight novel capsular polysaccharide synthesis gene loci identified in nontypeable Streptococcus suis isolates. Appl Environ Microbiol. 2015;81(12):4111–4119.
   PubMed Web of Science ®Google Scholar
• Zheng H, Qiu X, Roy D, et al. Genotyping and investigating capsular polysaccharide synthesis gene loci of non-serotypeable Streptococcus suis isolated from diseased pigs in Canada. Vet Res. 2017;48(1):10.
   PubMedGoogle Scholar
• Bojarska A, Janas K, Pejsak Z, et al. Diversity of serotypes and new cps loci variants among Streptococcus suis isolates from pigs in Poland and Belarus. Vet Microbiol. 2020;240:108534.
   PubMed Web of Science ®Google Scholar
• Lowe BA, Marsh TL, Isaacs-Cosgrove N, et al. Microbial communities in the tonsils of healthy pigs. Vet Microbiol. 2011;147(3–4):346–357.
   PubMed Web of Science ®Google Scholar
• Vötsch D, Willenborg M, Weldearegay YB, et al. Streptococcus suis - the “Two Faces” of a pathobiont in the porcine respiratory tract. Front Microbiol. 2018;9:480.
   PubMed Web of Science ®Google Scholar
• Arndt ER, Farzan A, Slavic D, et al. An epidemiological study of Streptococcus suis serotypes of pigs in Ontario determined by a multiplex polymerase chain reaction. Can Vet J. 2018;59(9):997–1000
   PubMed Web of Science ®Google Scholar
• Liang P, Wang M, Gottschalk M, et al. Genomic and pathogenic investigations of Streptococcus suis serotype 7 population derived from a human patient and pigs. Emerg Microbes Infect. 2021;10(1):1960–1974. DOI:10.1080/22221751.2021.1988725
   PubMed Web of Science ®Google Scholar
• Wang X, Sun J, Bian C, et al. The population structure, antimicrobial resistance, and pathogenicity of Streptococcus suis cps31. Vet Microbiol. 2021;259:109149. DOI:10.1016/j.vetmic.2021.109149
   PubMed Web of Science ®Google Scholar
• Swildens B, Nielen M, Wisselink HJ, et al. Elimination of strains of Streptococcus suis serotype 2 from the tonsils of carrier sows by combined medication and vaccination. Vet Rec. 2007;160(18):619–621.
   PubMed Web of Science ®Google Scholar
• Ngo TH, Tran TB, Tran TT, et al. Slaughterhouse pigs are a major reservoir of Streptococcus suis serotype 2 capable of causing human infection in southern Vietnam. PLoS One. 2011;6(3):e17943.
   PubMed Web of Science ®Google Scholar
• Dong X, Chao Y, Zhou Y, et al. The global emergence of a novel Streptococcus suis clade associated with human infections. EMBO Mol Med. 2021;13(7) ;e13810. doi:10.15252/emmm.202013810.
   PubMed Web of Science ®Google Scholar
• Bottai D, Groschel MI, Brosch R. Type VII secretion systems in gram-positive bacteria. Curr Top Microbiol Immunol. 2017;404:235–265.
   PubMed Web of Science ®Google Scholar
• Houben D, Demangel C, van Ingen J, et al. ESX-1-Mediated translocation to the cytosol controls virulence of mycobacteria. Cell Microbiol. 2012;14(8):1287–1298. DOI:10.1111/j.1462-5822.2012.01799.x
   PubMed Web of Science ®Google Scholar
• Burts ML, Williams WA, DeBord K, et al. EsxA and EsxB are secreted by an ESAT-6-like system that is required for the pathogenesis of Staphylococcus aureus infections. P Natl Acad Sci USA. 2005;102(4):1169–1174.
   PubMed Web of Science ®Google Scholar
• Taylor JC, Gao XS, Xu J, et al. A type VII secretion system of Streptococcus gallolyticus subsp. gallolyticus contributes to gut colonization and the development of colon tumors. PLoS Pathog. 2021;17(1):e1009182. DOI:10.1371/journal.ppat.1009182
   PubMed Web of Science ®Google Scholar
• Liu Y, Shu X, Chen L, et al. The beneficial rhizobacterium Bacillus velezensis acquires iron from roots via a type VII secretion system for colonization. bioRxiv. 2021 https://doi.org/10.1101/2021.08.01.454677.
   Google Scholar
• Li MF, Zhang BC, Li J, et al. Sil: a Streptococcus iniae bacteriocin with dual role as an antimicrobial and an immunomodulator that inhibits innate immune response and promotes S. iniae infection. PLoS One. 2014;9(4): e96222. doi:10.1371/journal.pone.0096222.
   PubMed Web of Science ®Google Scholar
• Heilbronner S, Krismer B, Brotz-Oesterhelt H, et al. The microbiome-shaping roles of bacteriocins. Nat Rev Microbiol. 2021;19(11):726–739. DOI:10.1038/s41579-021-00569-w
   PubMed Web of Science ®Google Scholar
• Li R, Li Y, Kristiansen K, et al. SOAP: short oligonucleotide alignment program. Bioinformatics. 2008;24(5):713–714.
   PubMed Web of Science ®Google Scholar
• Bertelli C, Laird MR, Williams KP, et al. IslandViewer 4: expanded prediction of genomic islands for larger-scale datasets. Nucleic Acids Res. 2017;45(W1):W30–W35.
   PubMed Web of Science ®Google Scholar
• Yoon SH, Ha SM, Lim J, et al. A large-scale evaluation of algorithms to calculate average nucleotide identity. Antonie Van Leeuwenhoek. 2017;110(10):1281–1286. DOI:10.1007/s10482-017-0844-4
   PubMed Web of Science ®Google Scholar
• Kumar S, Stecher G, Li M, et al. MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol. 2018;35(6):1547–1549.
   PubMed Web of Science ®Google Scholar
• Darling AE, Mau B, Perna NT. ProgressiveMauve: multiple genome alignment with gene gain, loss and rearrangement. PLoS One. 2010;5(6):e11147.
   PubMed Web of Science ®Google Scholar
• Krzywinski M, Schein J, Birol I, et al. Circos: an information aesthetic for comparative genomics. Genome Res. 2009;19(9):1639–1645. DOI:10.1101/gr.092759.109
   PubMed Web of Science ®Google Scholar
• Wu Z, Wu C, Shao J, et al. The Streptococcus suis transcriptional landscape reveals adaptation mechanisms in pig blood and cerebrospinal fluid. Rna. 2014;20(6):882–898. DOI:10.1261/rna.041822.113
   PubMed Web of Science ®Google Scholar
• Reed LJ, Muench H. A simple method of estimating fifty percent endpoints. Am J Hyg. 1938;27:493–497.
   Google Scholar
• Wu ZF, Wang WX, Tang M, et al. Comparative genomic analysis shows that Streptococcus suis meningitis isolate SC070731 contains a unique 105 K genomic island. Gene. 2014;535(2):156–164.
   PubMed Web of Science ®Google Scholar
• Zhu Y, Dong W, Ma J, et al. Utilization of the ComRS system for the rapid markerless deletion of chromosomal genes in Streptococcus suis. Future Microbiol. 2019;14(3):207–222. DOI:10.2217/fmb-2018-0279
   PubMed Web of Science ®Google Scholar
• Lai LY, Dai J, Tang HY, et al. Streptococcus suis serotype 9 strain GZ0565 contains a type VII secretion system putative substrate EsxA that contributes to bacterial virulence and a vanZ-like gene that confers resistance to teicoplanin and dalbavancin in Streptococcus agalactiae. Vet Microbiol. 2017;205:26–33.
   PubMed Web of Science ®Google Scholar
• Zeghouf M, Li J, Butland G, et al. Sequential Peptide Affinity (SPA) system for the identification of mammalian and bacterial protein complexes. J Proteome Res. 2004;3(3):463–468. DOI:10.1021/pr034084x
   PubMed Web of Science ®Google Scholar
• Xu J, Dai W, Liang Q, et al. The microbiomes of adenoid and middle ear in children with otitis media with effusion and hypertrophy from a tertiary hospital in China. Int J Pediatr Otorhinolaryngol. 2020;134:110058.
   PubMed Web of Science ®Google Scholar
• Tindall BJ, Rossello-Mora R, Busse HJ, et al. Notes on the characterization of prokaryote strains for taxonomic purposes. Int J Syst Evol Microbiol. 2010;60(Pt 1):249–266. DOI:10.1099/ijs.0.016949-0
   PubMedGoogle Scholar
• Edgar RC. UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods. 2013 Oct;10(10):996–998.
   PubMed Web of Science ®Google Scholar
• Huang J, Ma J, Shang K, et al. Evolution and diversity of the antimicrobial resistance associated mobilome in Streptococcus suis: a probable mobile genetic elements reservoir for other streptococci. Front Cell Infect Microbiol. 2016;6:118.
   PubMed Web of Science ®Google Scholar
• Schwarz S, Silley P, Simjee S, et al. Editorial: assessing the antimicrobial susceptibility of bacteria obtained from animals. J Antimicrob Chemother. 2010;65(4):601–604. DOI:10.1093/jac/dkq037
   PubMed Web of Science ®Google Scholar
• Ma JL, Liu J, Zhang Y, et al. Bacitracin resistance and enhanced virulence of Streptococcus suis via a novel efflux pump. BMC Vet Res. 2019;15(1):377. doi:10.1186/s12917-019-2115-2.
   PubMed Web of Science ®Google Scholar
• Huang J, Sun J, Wu Y, et al. Identification and pathogenicity of an XDR Streptococcus suis isolate that harbours the phenicol-oxazolidinone resistance genes optrA and cfr, and the bacitracin resistance locus bcrABDR. Int J Antimicrob Agents. 2019;54(1):43–48. DOI:10.1016/j.ijantimicag.2019.04.003
   PubMed Web of Science ®Google Scholar
• Sibinelli-Sousa S, Hespanhol JT, Bayer-Santos E. Targeting the Achilles’ heel of bacteria: different mechanisms to break down the peptidoglycan cell wall during bacterial warfare. J Bacteriol. 2021;203(7). DOI:10.1128/JB.00478-20
   PubMed Web of Science ®Google Scholar
• Vaillancourt K, LeBel G, Frenette M, et al. Suicin 3908, a new lantibiotic produced by a strain of Streptococcus suis serotype 2 isolated from a healthy carrier pig. PLoS One. 2015;10(2):e0117245. DOI:10.1371/journal.pone.0117245
   PubMed Web of Science ®Google Scholar
• Martinez B, Rodriguez A, Suarez JE. Lactococcin 972, a bacteriocin that inhibits septum formation in lactococci. Microbiol-Uk. 2000 Apr;146(4):949–955.
   PubMedGoogle Scholar
• Lowe BA, Marsh TL, Isaacs-Cosgrove N, et al. Defining the “core microbiome” of the microbial communities in the tonsils of healthy pigs. BMC Microbiol. 2012;12(1):20.
   PubMedGoogle Scholar
• Qiu XT, Bai XM, Lan RT, et al. Novel capsular polysaccharide loci and new diagnostic tools for high-throughput capsular gene typing in Streptococcus suis. Appl Environ Microb. 2016;82(24):7102–7112
   PubMed Web of Science ®Google Scholar
• Cao ZP, Casabona MG, Kneuper H, et al. The type VII secretion system of Staphylococcus aureus secretes a nuclease toxin that targets competitor bacteria. Nat Microbiol. 2017;2(1). DOI:10.1038/nmicrobiol.2016.183
   Web of Science ®Google Scholar
• Ulhuq FR, Gomes MC, Duggan GM, et al. A membrane-depolarizing toxin substrate of the Staphylococcus aureus type VII secretion system mediates intraspecies competition. Proc Natl Acad Sci U S a. 2020;117(34):20836–20847.
   PubMed Web of Science ®Google Scholar
• Zhang D, Iyer LM, Aravind L. A novel immunity system for bacterial nucleic acid degrading toxins and its recruitment in various eukaryotic and DNA viral systems. Nucleic Acids Res. 2011 Jun;39(11):4532–4552.
   PubMed Web of Science ®Google Scholar
• Whitney JC, Peterson SB, Kim J, et al. A broadly distributed toxin family mediates contact-dependent antagonism between gram-positive bacteria. Elife. 2017;6. DOI:10.7554/eLife.26938
   Web of Science ®Google Scholar
• Warne B, Harkins CP, Harris SR, et al. The Ess/Type VII secretion system of Staphylococcus aureus shows unexpected genetic diversity. BMC Genomics. 2016;17. DOI:10.1186/s12864-016-2426-7
   PubMed Web of Science ®Google Scholar
• Wholey WY, Kochan TJ, Storck DN, et al. Coordinated bacteriocin expression and competence in streptococcus pneumoniae contributes to genetic adaptation through neighbor predation. PLoS Pathog. 2016;12(2):e1005413. DOI:10.1371/journal.ppat.1005413
   PubMed Web of Science ®Google Scholar
• Janek D, Zipperer A, Kulik A, et al. High frequency and diversity of antimicrobial activities produced by nasal Staphylococcus strains against bacterial competitors. PLoS Pathog. 2016;12(8):e1005812. DOI:10.1371/journal.ppat.1005812
   PubMed Web of Science ®Google Scholar
• Quereda JJ, Dussurget O, Nahori MA, et al. Bacteriocin from epidemic Listeria strains alters the host intestinal microbiota to favor infection. P Natl Acad Sci USA. 2016;113(20):5706–5711.
   PubMed Web of Science ®Google Scholar
• Rolhion N, Chassaing B, Nahori M-A, et al. A Listeria monocytogenes bacteriocin can target the commensal Prevotella copri and modulate intestinal infection. Cell Host Microbe. 2019;26(5):691–701. e5. DOI:10.1016/j.chom.2019.10.016
   PubMed Web of Science ®Google Scholar