Abstract
Streptococcus suis (S. suis) is an important zoonotic agent, which seriously impacts the pig industry and human health in various countries. Biofilm formation is likely contributing to the virulence and drug resistance in S. suis. A better knowledge of biofilm formation as well as to biofilm-dependent drug resistance mechanisms in S. suis can be of great significance for the prevention and treatment of S. suis infections. This literature review updates the latest scientific data related to biofilm formation in S. suis and its impact on drug tolerance and resistance.
Key points
• Biofilm formation is the important reasons for drug resistance of SS infections.
• The review includes the regulatory mechanism of SS biofilm formation.
• The review includes the drug resistance mechanisms of SS biofilm.
Similar content being viewed by others
References
Aiassa V, Barnes AI, Smania AM, Albesa I (2012) Sublethal ciprofloxacin treatment leads to resistance via antioxidant systems in Proteus mirabilis. FEMS Microbiol Lett 327(1):25–32. https://doi.org/10.1111/j.1574-6968.2011.02453.x
Allen HK, Donato J, Wang HH, Cloud-Hansen KA, Davies J, Handelsman J (2010) Call of the wild: antibiotic resistance genes in natural environments. Nat Rev Microbiol 8(4):251–259. https://doi.org/10.1038/nrmicro2312
Ambroset C, Coluzzi C, Guedon G, Devignes MD, Loux V, Lacroix T, Payot S, Leblond-Bourget N (2015) New insights into the classification and integration specificity of Streptococcus integrative conjugative elements through extensive genome exploration. Front Microbiol 6:1483. https://doi.org/10.3389/fmicb.2015.01483
Anderl JN, Zahller J, Roe F, Stewart PS (2003) Role of nutrient limitation and stationary-phase existence in Klebsiella pneumoniae biofilm resistance to ampicillin and ciprofloxacin. Antimicrob Agents Chemother 47(4):1251–1256. https://doi.org/10.1128/aac.47.4.1251-1256.2003
Athey TB, Teatero S, Takamatsu D, Wasserscheid J, Dewar K, Gottschalk M, Fittipaldi N (2016) Population structure and antimicrobial resistance profiles of Streptococcus suis serotype 2 sequence type 25 strains. PLoS One 11(3):e0150908. https://doi.org/10.1371/journal.pone.0150908
Bazire A, Shioya K, Soum-Soutera E, Bouffartigues E, Ryder C, Guentas-Dombrowsky L, Hemery G, Linossier I, Chevalier S, Wozniak DJ, Lesouhaitier O, Dufour A (2010) The sigma factor AlgU plays a key role in formation of robust biofilms by nonmucoid Pseudomonas aeruginosa. J Bacteriol 192(12):3001–3010. https://doi.org/10.1128/JB.01633-09
Beaber JW, Hochhut B, Waldor MK (2004) SOS response promotes horizontal dissemination of antibiotic resistance genes. Nature 427(6969):72–74. https://doi.org/10.1038/nature02241
Bhattacharya G, Dey D, Das S, Banerjee A (2017) Exposure to sub-inhibitory concentrations of gentamicin, ciprofloxacin and cefotaxime induces multidrug resistance and reactive oxygen species generation in meticillin-sensitive Staphylococcus aureus. J Med Microbiol 66(6):762–769. https://doi.org/10.1099/jmm.0.000492
Bojarska A, Molska E, Janas K, Skoczynska A, Stefaniuk E, Hryniewicz W, Sadowy E (2016) Streptococcus suis in invasive human infections in Poland: clonality and determinants of virulence and antimicrobial resistance. Eur J Clin Microbiol Infect Dis 35(6):917–25. https://doi.org/10.1007/s10096-016-2616-x
Bonifait L, Grignon L, Grenier D (2008) Fibrinogen induces biofilm formation by Streptococcus suis and enhances its antibiotic resistance. Appl Environ Microbiol 74(15):4969–4972. https://doi.org/10.1128/AEM.00558-08
Bozdogan B, Berrezouga L, Kuo MS, Yurek DA, Farley KA, Stockman BJ, Leclercq R (1999) A new resistance gene, linB, conferring resistance to lincosamides by nucleotidylation in Enterococcus faecium HM1025. Antimicrob Agents Chemother 43(4):925–9
Chander Y, Oliveira SR, Goyal SM (2011) Identification of the tet(B) resistance gene in Streptococcus suis. Vet J 189(3):359–360. https://doi.org/10.1016/j.tvjl.2010.07.004
Chiang WC, Nilsson M, Jensen PO, Hoiby N, Nielsen TE, Givskov M, Tolker-Nielsen T (2013) Extracellular DNA shields against aminoglycosides in Pseudomonas aeruginosa biofilms. Antimicrob Agents Chemother 57(5):2352–2361. https://doi.org/10.1128/AAC.00001-13
Choi KS, Veeraragouda Y, Cho KM, Lee SO, Jo GR, Cho K, Lee K (2007) Effect of gacS and gacA mutations on colony architecture, surface motility, biofilm formation and chemical toxicity in Pseudomonas sp. KL28. J Microbiol 45(6):492–498
Chu YW, Cheung TK, Chu MY, Tsang VY, Fung JT, Kam KM, Lo JY (2009) Resistance to tetracycline, erythromycin and clindamycin in Streptococcus suis serotype 2 in Hong Kong. Int J Antimicrob Agents 34(2):181–182. https://doi.org/10.1016/j.ijantimicag.2009.01.007
Crabbe A, Jensen PO, Bjarnsholt T, Coenye T (2019) Antimicrobial tolerance and metabolic adaptations in microbial biofilms. Trends Microbiol 27(10):850–863. https://doi.org/10.1016/j.tim.2019.05.003
Davies DG, Parsek MR, Pearson JP, Iglewski BH, Costerton JW, Greenberg EP (1998) The involvement of cell-to-cell signals in the development of a bacterial biofilm. Science 280(5361):295–298. https://doi.org/10.1126/science.280.5361.295
Dorr T, Vulic M, Lewis K (2010) Ciprofloxacin causes persister formation by inducing the TisB toxin in Escherichia coli. PLoS Biol 8(2):e1000317. https://doi.org/10.1371/journal.pbio.1000317
Dufour D, Leung V, Lévesque CM (2012) Bacterial biofilm: structure, function, and antimicrobial resistance. Endod Top 22(1):2–16
Dutkiewicz J, Zajac V, Sroka J, Wasinski B, Cisak E, Sawczyn A, Kloc A, Wojcik-Fatla A (2018) Streptococcus suis: a re-emerging pathogen associated with occupational exposure to pigs or pork products. Part II - pathogenesis. Ann Agric Environ Med 25(1):186–203. https://doi.org/10.26444/aaem/85651
Fuqua WC, Winans SC, Greenberg EP (1994) Quorum sensing in bacteria: the LuxR-LuxI family of cell density-responsive transcriptional regulators. J Bacteriol 176(2):269–275. https://doi.org/10.1128/jb.176.2.269-275.1994
Grenier D, Grignon L, Gottschalk M (2009) Characterisation of biofilm formation by a Streptococcus suis meningitis isolate. Vet J 179(2):292–295. https://doi.org/10.1016/j.tvjl.2007.09.005
Gui Z, Wang H, Ding T, Zhu W, Zhuang X, Chu W (2014) Azithromycin reduces the production of alpha-hemolysin and biofilm formation in Staphylococcus aureus. Indian J Microbiol 54(1):114–117. https://doi.org/10.1007/s12088-013-0438-4
Habash M, Reid G (1999) Microbial biofilms: their development and significance for medical device-related infections. J Clin Pharmacol 39(9):887–898. https://doi.org/10.1177/00912709922008506
Hall CW, Mah TF (2017) Molecular mechanisms of biofilm-based antibiotic resistance and tolerance in pathogenic bacteria. FEMS Microbiol Rev 41(3):276–301. https://doi.org/10.1093/femsre/fux010
Han X, Liu L, Fan G, Zhang Y, Xu D, Zuo J, Wang S, Wang X, Tian M, Ding C, Yu S (2015) Riemerella anatipestifer lacks luxS, but can uptake exogenous autoinducer-2 to regulate biofilm formation. Res Microbiol 166(6):486–493. https://doi.org/10.1016/j.resmic.2015.06.004
Hoa NT, Chieu TT, Nghia HD, Mai NT, Anh PH, Wolbers M, Baker S, Campbell JI, Chau NV, Hien TT, Farrar J, Schultsz C (2011) The antimicrobial resistance patterns and associated determinants in Streptococcus suis isolated from humans in southern Vietnam, 1997-2008. BMC Infect Dis 11:6. https://doi.org/10.1186/1471-2334-11-6
Helaine S, Kugelberg E (2014) Bacterial persisters: formation, eradication, and experimental systems. Trends Microbiol 22(7):417–424. https://doi.org/10.1016/j.tim.2014.03.008
Hoiby N, Bjarnsholt T, Givskov M, Molin S, Ciofu O (2010) Antibiotic resistance of bacterial biofilms. Int J Antimicrob Agents 35(4):322–332. https://doi.org/10.1016/j.ijantimicag.2009.12.011
Hu Y, Hu Q, Wei R, Li R, Zhao D, Ge M, Yao Q, Yu X (2018) The XRE family transcriptional regulator SrtR in Streptococcus suis is involved in oxidant tolerance and virulence. Front Cell Infect Microbiol 8:452. https://doi.org/10.3389/fcimb.2018.00452
Huang J, Liang Y, Guo D, Shang K, Ge L, Kashif J, Wang L (2016a) 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 7:55. https://doi.org/10.3389/fmicb.2016.00055
Huang J, Ma J, Shang K, Hu X, Liang Y, Li D, Wu Z, Dai L, Chen L, Wang L (2016b) 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 6:118. https://doi.org/10.3389/fcimb.2016.00118
Huang K, Song Y, Zhang Q, Zhang A, Jin M (2016c) Characterisation of a novel integrative and conjugative element ICESsD9 carrying erm(B) and tet(O) resistance determinants in Streptococcus suis, and the distribution of ICESsD9-like elements in clinical isolates. J Glob Antimicrob Resist 7:13–18. https://doi.org/10.1016/j.jgar.2016.05.008
Huang Y, Zhang L, Tiu L, Wang HH (2015) Characterization of antibiotic resistance in commensal bacteria from an aquaculture ecosystem. Front Microbiol 6:914. https://doi.org/10.3389/fmicb.2015.00914
Hughes D (2014) Selection and evolution of resistance to antimicrobial drugs. IUBMB Life 66(8):521–529. https://doi.org/10.1002/iub.1278
Imlay JA (2008) Cellular defenses against superoxide and hydrogen peroxide. Annu Rev Biochem 77:755–776. https://doi.org/10.1146/annurev.biochem.77.061606.161055
Jorgensen KM, Wassermann T, Jensen PO, Hengzuang W, Molin S, Hoiby N, Ciofu O (2013) Sublethal ciprofloxacin treatment leads to rapid development of high-level ciprofloxacin resistance during long-term experimental evolution of Pseudomonas aeruginosa. Antimicrob Agents Chemother 57(9):4215–4221. https://doi.org/10.1128/AAC.00493-13
Kalia VC (2013) Quorum sensing inhibitors: an overview. Biotechnol Adv 31(2):224–245. https://doi.org/10.1016/j.biotechadv.2012.10.004
Keren I, Kaldalu N, Spoering A, Wang Y, Lewis K (2004) Persister cells and tolerance to antimicrobials. FEMS Microbiol Lett 230(1):13–18. https://doi.org/10.1016/S0378-1097(03)00856-5
Kint CI, Verstraeten N, Fauvart M, Michiels JJ (2012) New-found fundamentals of bacterial persistence. Trends Microbiol 20(12):577–585
Kumar S, Lekshmi M, Parvathi A, Ojha M, Wenzel N, Varela MF (2020) Functional and structural roles of the major facilitator superfamily bacterial multidrug efflux pumps. Microorganisms 8(2). https://doi.org/10.3390/microorganisms8020266
Kusakizako T, Miyauchi H, Ishitani R, Nureki O (2019) Structural biology of the multidrug and toxic compound extrusion superfamily transporters. Biochim Biophys Acta Biomembr:183154. https://doi.org/10.1016/j.bbamem.2019.183154
Lewis K (2012) Persister cells: molecular mechanisms related to antibiotic tolerance. Handb Exp Pharmacol 211:121–133. https://doi.org/10.1007/978-3-642-28951-4_8
Li XZ, Nikaido H (2004) Efflux-mediated drug resistance in bacteria. Drugs 64(2):159–204. https://doi.org/10.2165/00003495-200464020-00004
Li XZ, Nikaido H (2009) Efflux-mediated drug resistance in bacteria: an update. Drugs 69(12):1555–1623. https://doi.org/10.2165/11317030-000000000-00000
Libante V, Nombre Y, Coluzzi C, Staub J, Guedon G, Gottschalk M, Teatero S, Fittipaldi N, Leblond-Bourget N, Payot S (2019) Chromosomal conjugative and mobilizable elements in Streptococcus suis: major actors in the spreading of antimicrobial resistance and Bacteriocin synthesis genes. Pathogens 9(1). https://doi.org/10.3390/pathogens9010022
Liu B, Yi L, Li J, Wang Y, Mao C, Wang Y (2020) Autoinducer-2 influences tetracycline resistance in Streptococcus suis by regulating the tet(M) gene via transposon Tn916. Res Vet Sci 128:269–274. https://doi.org/10.1016/j.rvsc.2019.12.007
Liu YY, Chen CC (2017) Computational analysis of the molecular mechanism of RamR mutations contributing to antimicrobial resistance in Salmonella enterica. Sci Rep 7(1):13418. https://doi.org/10.1038/s41598-017-14008-5
Ma F, Yi L, Yu N, Wang G, Ma Z, Lin H, Fan H (2017) Streptococcus suis serotype 2 biofilms inhibit the formation of neutrophil extracellular traps. Front Cell Infect Microbiol 7:86. https://doi.org/10.3389/fcimb.2017.00086
Madsen JS, Burmolle M, Hansen LH, Sorensen SJ (2012) The interconnection between biofilm formation and horizontal gene transfer. FEMS Immunol Med Microbiol 65(2):183–195. https://doi.org/10.1111/j.1574-695X.2012.00960.x
Mah TF, O’Toole GA (2001) Mechanisms of biofilm resistance to antimicrobial agents. Trends Microbiol 9(1):34–39. https://doi.org/10.1016/s0966-842x(00)01913-2
Matsuyama BY, Krasteva PV, Baraquet C, Harwood CS, Sondermann H, Navarro MV (2016) Mechanistic insights into c-di-GMP-dependent control of the biofilm regulator FleQ from Pseudomonas aeruginosa. Proc Natl Acad Sci U S A 113(2):E209–E218. https://doi.org/10.1073/pnas.1523148113
Mei JJ, Wang Y, Li YI, Zhang JK, Cheng XC, Zhang CJ, Zu-Hua YU, Ting-Cai WU (2016) Effect of OCT protein on the biofilm formation and the bacterial adherence of Streptococcus suis. Chin Vet Sci 46(02):192–197
Meng X, Shi Y, Ji W, Meng X, Zhang J, Wang H, Lu C, Sun J, Yan Y (2011) Application of a bacteriophage lysin to disrupt biofilms formed by the animal pathogen Streptococcus suis. Appl Environ Microbiol 77(23):8272–8279. https://doi.org/10.1128/AEM.05151-11
Molin S, Tolker-Nielsen T (2003) Gene transfer occurs with enhanced efficiency in biofilms and induces enhanced stabilisation of the biofilm structure. Curr Opin Biotechnol 14(3):255–261. https://doi.org/10.1016/s0958-1669(03)00036-3
Mulcahy H, Charron-Mazenod L, Lewenza S (2008) Extracellular DNA chelates cations and induces antibiotic resistance in Pseudomonas aeruginosa biofilms. PLoS Pathog 4(11):e1000213. https://doi.org/10.1371/journal.ppat.1000213
Nilsson M, Rybtke M, Givskov M, Hoiby N, Twetman S, Tolker-Nielsen T (2016) The dlt genes play a role in antimicrobial tolerance of Streptococcus mutans biofilms. Int J Antimicrob Agents 48(3):298–304. https://doi.org/10.1016/j.ijantimicag.2016.06.019
Nishino K, Yamaguchi A (2001) Analysis of a complete library of putative drug transporter genes in Escherichia coli. J Bacteriol 183(20):5803–5812. https://doi.org/10.1128/JB.183.20.5803-5812.2001
Novick RP (2003) Autoinduction and signal transduction in the regulation of staphylococcal virulence. Mol Microbiol 48(6):1429–1449. https://doi.org/10.1046/j.1365-2958.2003.03526.x
Nystrom T (2002) Aging in bacteria. Curr Opin Microbiol 5(6):596–601. https://doi.org/10.1016/s1369-5274(02)00367-3
Olsen I (2015) Biofilm-specific antibiotic tolerance and resistance. Eur J Clin Microbiol Infect Dis 34(5):877–886. https://doi.org/10.1007/s10096-015-2323-z
Osterblad M, Norrdahl K, Korpimaki E, Huovinen P (2001) Antibiotic resistance. How wild are wild mammals? Nature 409(6816):37–38. https://doi.org/10.1038/35051173
Pabst B, Pitts B, Lauchnor E, Stewart PS (2016) Gel-entrapped Staphylococcus aureus bacteria as models of biofilm infection exhibit growth in dense aggregates, oxygen limitation, antibiotic tolerance, and heterogeneous gene expression. Antimicrob Agents Chemother 60(10):6294–6301. https://doi.org/10.1128/AAC.01336-16
Palmieri C, Varaldo PE, Facinelli B (2011) Streptococcus suis, an emerging drug-resistant animal and human pathogen. Front Microbiol 2:235. https://doi.org/10.3389/fmicb.2011.00235
Pan Z, Liu J, Zhang Y, Chen S, Ma J, Dong W, Wu Z, Yao H (2019) A novel integrative conjugative element mediates transfer of multi-drug resistance between Streptococcus suis strains of different serotypes. Vet Microbiol 229:110–116. https://doi.org/10.1016/j.vetmic.2018.11.028
Polkade AV, Mantri SS, Patwekar UJ, Jangid K (2016) Quorum sensing: an under-explored phenomenon in the phylum Actinobacteria. Front Microbiol 7:131. https://doi.org/10.3389/fmicb.2016.00131
Potrykus K, Cashel M (2008) (p)ppGpp: still magical? Annu Rev Microbiol 62:35–51. https://doi.org/10.1146/annurev.micro.62.081307.162903
Rachid S, Ohlsen K, Witte W, Hacker J, Ziebuhr W (2000) Effect of subinhibitory antibiotic concentrations on polysaccharide intercellular adhesin expression in biofilm-forming Staphylococcus epidermidis. Antimicrob Agents Chemother 44(12):3357–3363. https://doi.org/10.1128/aac.44.12.3357-3363.2000
Sauer K, Camper AK, Ehrlich GD, Costerton JW, Davies DG (2002) Pseudomonas aeruginosa displays multiple phenotypes during development as a biofilm. J Bacteriol 184(4):1140–1154. https://doi.org/10.1128/jb.184.4.1140-1154.2002
Scott M, Gunderson CW, Mateescu EM, Zhang Z, Hwa T (2010) Interdependence of cell growth and gene expression: origins and consequences. Science 330(6007):1099–1102. https://doi.org/10.1126/science.1192588
Segura M, Fittipaldi N, Calzas C, Gottschalk M (2017) Critical Streptococcus suis virulence factors: are they all really critical? Trends Microbiol 25(7):585–599. https://doi.org/10.1016/j.tim.2017.02.005
Sitkiewicz I, Green NM, Guo N, Mereghetti L, Musser JM (2011) Lateral gene transfer of streptococcal ICE element RD2 (region of difference 2) encoding secreted proteins. BMC Microbiol 11:65. https://doi.org/10.1186/1471-2180-11-65
Soto SM (2013) Role of efflux pumps in the antibiotic resistance of bacteria embedded in a biofilm. Virulence 4(3):223–229. https://doi.org/10.4161/viru.23724
Southey-Pillig CJ, Davies DG, Sauer K (2005) Characterization of temporal protein production in Pseudomonas aeruginosa biofilms. J Bacteriol 187(23):8114–8126. https://doi.org/10.1128/JB.187.23.8114-8126.2005
Stewart PS, Roe F, Rayner J, Elkins JG, Lewandowski Z, Ochsner UA, Hassett DJ (2000) Effect of catalase on hydrogen peroxide penetration into Pseudomonas aeruginosa biofilms. Appl Environ Microbiol 66(2):836–838. https://doi.org/10.1128/aem.66.2.836-838.2000
Taylor PK, Yeung AT, Hancock RE (2014) Antibiotic resistance in Pseudomonas aeruginosa biofilms: towards the development of novel anti-biofilm therapies. J Biotechnol 191:121–130. https://doi.org/10.1016/j.jbiotec.2014.09.003
Thurnheer T, Gmur R, Shapiro S, Guggenheim B (2003) Mass transport of macromolecules within an in vitro model of supragingival plaque. Appl Environ Microbiol 69(3):1702–1709. https://doi.org/10.1128/aem.69.3.1702-1709.2003
Tsuchiya H, Doki S, Takemoto M, Ikuta T, Higuchi T, Fukui K, Usuda Y, Tabuchi E, Nagatoishi S, Tsumoto K, Nishizawa T, Ito K, Dohmae N, Ishitani R, Nureki O (2016) Structural basis for amino acid export by DMT superfamily transporter YddG. Nature 534(7607):417–420. https://doi.org/10.1038/nature17991
Van Acker H, Van Dijck P, Coenye T (2014) Molecular mechanisms of antimicrobial tolerance and resistance in bacterial and fungal biofilms. Trends Microbiol 22(6):326–333. https://doi.org/10.1016/j.tim.2014.02.001
Venkatesan N, Perumal G, Doble M (2015) Bacterial resistance in biofilm-associated bacteria. Future Microbiol 10(11):1743–1750. https://doi.org/10.2217/fmb.15.69
Votsch D, Willenborg M, Weldearegay YB, Valentin-Weigand P (2018) Streptococcus suis - the “two faces” of a pathobiont in the porcine respiratory tract. Front Microbiol 9:480. https://doi.org/10.3389/fmicb.2018.00480
Waack U, Nicholson TL (2018) Subinhibitory concentrations of amoxicillin, lincomycin, and oxytetracycline commonly used to treat swine increase Streptococcus suis biofilm formation. Front Microbiol 9:2707. https://doi.org/10.3389/fmicb.2018.02707
Walters MC 3rd, Roe F, Bugnicourt A, Franklin MJ, Stewart PS (2003) Contributions of antibiotic penetration, oxygen limitation, and low metabolic activity to tolerance of Pseudomonas aeruginosa biofilms to ciprofloxacin and tobramycin. Antimicrob Agents Chemother 47(1):317–323. https://doi.org/10.1128/aac.47.1.317-323.2003
Wang F, Li D, Zheng Z, Kin Wah To K, Chen Z, Zhong M, Su X, Chen L, Fu L (2020a) Reversal of ABCB1-related multidrug resistance by ERK5-IN-1. J Exp Clin Cancer Res 39(1):50. https://doi.org/10.1186/s13046-020-1537-9
Wang N, Guo X, Yan Z, Wang W, Chen B, Ge F, Ye B (2016) A Comprehensive Analysis on Spread and Distribution Characteristic of Antibiotic Resistance Genes in Livestock Farms of Southeastern China. PLoS One 11(7):e0156889. https://doi.org/10.1371/journal.pone.0156889
Wang Y, Liu B, Li J, Gong S, Dong X, Mao C, Yi L (2019a) LuxS/AI-2 system is involved in fluoroquinolones susceptibility in Streptococcus suis through overexpression of efflux pump SatAB. Vet Microbiol 233:154–158. https://doi.org/10.1016/j.vetmic.2019.05.006
Wang Y, Wang Y, Liu B, Wang S, Li J, Gong S, Sun L, Yi L (2019b) pdh modulate virulence through reducing stress tolerance and biofilm formation of Streptococcus suis serotype 2. Virulence 10(1):588–599. https://doi.org/10.1080/21505594.2019.1631661
Wang Y, Wang Y, Sun L, Grenier D, Yi L (2018a) The LuxS/AI-2 system of Streptococcus suis. Appl Microbiol Biotechnol 102(17):7231–7238. https://doi.org/10.1007/s00253-018-9170-7
Wang Y, Wang Y, Sun L, Grenier D, Yi L (2018b) Streptococcus suis biofilm: regulation, drug-resistance mechanisms, and disinfection strategies. Appl Microbiol Biotechnol 102(21):9121–9129. https://doi.org/10.1007/s00253-018-9356-z
Wang Y, Yi L, Sun LY, Liu YC, Wen WY, Li XK, Mei JJ, Ding K, Wu TC, Grenier D (2020b) Identification and characterization of a Streptococcus suis immunogenic ornithine carbamoytransferase involved in bacterial adherence. J Microbiol Immunol Infect 53(2):234–239. https://doi.org/10.1016/j.jmii.2018.05.004
Wang Y, Yi L, Zhang Z, Fan H, Cheng X, Lu C (2013) Overexpression of luxS cannot increase autoinducer-2 production, only affect the growth and biofilm formation in Streptococcus suis. Sci World J 2013:924276–924276. https://doi.org/10.1155/2013/924276
Wang Y, Yi L, Zhang Z, Fan H, Cheng X, Lu C (2014) Biofilm formation, host-cell adherence, and virulence genes regulation of Streptococcus suis in response to autoinducer-2 signaling. Curr Microbiol 68(5):575–580. https://doi.org/10.1007/s00284-013-0509-0
Waters B, Davies J (1997) Amino acid variation in the GyrA subunit of bacteria potentially associated with natural resistance to fluoroquinolone antibiotics. Antimicrob Agents Chemother 41(12):2766–2769
Werner E, Roe F, Bugnicourt A, Franklin MJ, Heydorn A, Molin S, Pitts B, Stewart PS (2004) Stratified growth in Pseudomonas aeruginosa biofilms. Appl Environ Microbiol 70(10):6188–6196. https://doi.org/10.1128/AEM.70.10.6188-6196.2004
Wendlandt S, Lozano C, Kadlec K, Gomez-Sanz E, Zarazaga M, Torres C, Schwarz S (2013) The enterococcal ABC transporter gene lsa(E) confers combined resistance to lincosamides, pleuromutilins and streptogramin A antibiotics in methicillin-susceptible and methicillin-resistant Staphylococcus aureus. J Antimicrob Chemother 68(2):473–5. https://doi.org/10.1093/jac/dks398
Whitchurch CB, Tolker-Nielsen T, Ragas PC, Mattick JS (2002) Extracellular DNA required for bacterial biofilm formation. Science 295(5559):1487. https://doi.org/10.1126/science.295.5559.1487
Williams P, Camara M, Hardman A, Swift S, Milton D, Hope VJ, Winzer K, Middleton B, Pritchard DI, Bycroft BW (2000) Quorum sensing and the population-dependent control of virulence. Philos Trans R Soc Lond Ser B Biol Sci 355(1397):667–680. https://doi.org/10.1098/rstb.2000.0607
Xu J, Zhang N, Cao M, Ren S, Zeng T, Qin M, Zhao X, Yuan F, Chen H, Bei W (2018) Identification of three type II toxin-antitoxin systems in Streptococcus suis serotype 2. Toxins (Basel) 10(11):467. https://doi.org/10.3390/toxins10110467
Yi L, Li J, Liu B, Wang Y (2019) Advances in research on signal molecules regulating biofilms. World J Microbiol Biotechnol 35(8):130. https://doi.org/10.1007/s11274-019-2706-x
Funding
This work was financially supported by the National Natural Science Foundation of China (31772761, 31902309, U1704117).
Author information
Authors and Affiliations
Contributions
YW and LY designed the concept of the review article. LY, MYJ, and LY contributed to writing the manuscript. YW and DG critically read and corrected the manuscript. All authors read and approved the final manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Ethical statement
This article does not contain any studies with human participants or animals performed by any of the authors.
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Yi, L., Jin, M., Li, J. et al. Antibiotic resistance related to biofilm formation in Streptococcus suis. Appl Microbiol Biotechnol 104, 8649–8660 (2020). https://doi.org/10.1007/s00253-020-10873-9
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00253-020-10873-9