Informacja

Drogi użytkowniku, aplikacja do prawidłowego działania wymaga obsługi JavaScript. Proszę włącz obsługę JavaScript w Twojej przeglądarce.

Tytuł pozycji:

Interspecies competition in oral biofilms mediated by Streptococcus gordonii extracellular deoxyribonuclease SsnA.

Tytuł:
Interspecies competition in oral biofilms mediated by Streptococcus gordonii extracellular deoxyribonuclease SsnA.
Autorzy:
Rostami N; School of Dental Sciences, Faculty of Medical Sciences, Newcastle University, Newcastle, UK.
Shields RC; School of Dental Sciences, Faculty of Medical Sciences, Newcastle University, Newcastle, UK.; Department of Biological Sciences, Arkansas State University, Jonesboro, AR, USA.
Serrage HJ; Bristol Dental School, University of Bristol, Bristol, UK.
Lawler C; Bristol Dental School, University of Bristol, Bristol, UK.
Brittan JL; Bristol Dental School, University of Bristol, Bristol, UK.
Yassin S; School of Dental Sciences, Faculty of Medical Sciences, Newcastle University, Newcastle, UK.; Department of Restorative Sciences, University of Alabama at Birmingham, Birmingham, AL, USA.
Ahmed H; School of Dental Sciences, Faculty of Medical Sciences, Newcastle University, Newcastle, UK.
Treumann A; Protein and Proteome Analysis Facility, Faculty of Medical Sciences, Newcastle University, Newcastle, UK.; KBI Biopharma BV, Leuven, Belgium.
Thompson P; Protein and Proteome Analysis Facility, Faculty of Medical Sciences, Newcastle University, Newcastle, UK.
Waldron KJ; Biosciences Institute, Faculty of Medical Sciences, Newcastle University, Newcastle, UK.
Nobbs AH; Bristol Dental School, University of Bristol, Bristol, UK.
Jakubovics NS; School of Dental Sciences, Faculty of Medical Sciences, Newcastle University, Newcastle, UK. .
Źródło:
NPJ biofilms and microbiomes [NPJ Biofilms Microbiomes] 2022 Dec 12; Vol. 8 (1), pp. 96. Date of Electronic Publication: 2022 Dec 12.
Typ publikacji:
Journal Article; Research Support, Non-U.S. Gov't
Język:
English
Imprint Name(s):
Original Publication: [New York, NY ?] : Nature Publishing Group, [2015]-
MeSH Terms:
Streptococcus gordonii*/genetics
Dental Plaque*
Humans ; Streptococcus mutans ; Biofilms ; Saliva
References:
Bik, E. M. et al. Bacterial diversity in the oral cavity of 10 healthy individuals. ISME J. 4, 962–974 (2010). (PMID: 10.1038/ismej.2010.30)
Huang, R., Li, M. & Gregory, R. L. Bacterial interactions in dental biofilm. Virulence 2, 435–444 (2011). (PMID: 10.4161/viru.2.5.16140)
Jakubovics, N. S. Intermicrobial interactions as a driver for community composition and stratification of oral biofilms. J. Mol. Biol. 427, 3662–3675 (2015). (PMID: 10.1016/j.jmb.2015.09.022)
Hajishengallis, G. & Lamont, R. J. Beyond the red complex and into more complexity: the polymicrobial synergy and dysbiosis (PSD) model of periodontal disease etiology. Mol. Oral. Microbiol. 27, 409–419 (2012). (PMID: 10.1111/j.2041-1014.2012.00663.x)
Diaz, P. I. & Valm, A. M. Microbial interactions in oral communities mediate emergent biofilm properties. J. Dent. Res. 99, 18–25 (2020). (PMID: 10.1177/0022034519880157)
Zijnge, V. et al. Oral biofilm architecture on natural teeth. PLoS ONE 5, e9321 (2010). (PMID: 10.1371/journal.pone.0009321)
Kolenbrander, P. E. et al. Communication among oral bacteria. Microbiol. Mol. Biol. Rev. 66, 486–505 (2002). (PMID: 10.1128/MMBR.66.3.486-505.2002)
Mann, E. E. et al. Modulation of eDNA release and degradation affects Staphylococcus aureus biofilm maturation. PLoS ONE 4, e5822 (2009). (PMID: 10.1371/journal.pone.0005822)
Nascimento, M. M. et al. The effect of arginine on oral biofilm communities. Mol. Oral. Microbiol. 29, 45–54 (2014). (PMID: 10.1111/omi.12044)
Belda-Ferre, P. et al. The oral metagenome in health and disease. ISME J. 6, 46–56 (2012). (PMID: 10.1038/ismej.2011.85)
Marsh, P. D. Microbiology of dental plaque biofilms and their role in oral health and caries. Dent. Clin. North Am. 54, 441–454 (2010). (PMID: 10.1016/j.cden.2010.03.002)
Vos, T. et al. Global, regional, and national incidence, prevalence, and years lived with disability for 328 diseases and injuries for 195 countries, 1990–2016: a systematic analysis for the Global Burden of Disease Study 2016. Lancet 390, 1211–1259 (2017). (PMID: 10.1016/S0140-6736(17)32154-2)
Marsh, P. D. Microbial ecology of dental plaque and its significance in health and disease. Adv. Dent. Res. 8, 263–271 (1994). (PMID: 10.1177/08959374940080022001)
Marsh, P. D. & Zaura, E. Dental biofilm: ecological interactions in health and disease. J. Clin. Periodontol. 44(Suppl 18), S12–s22 (2017). (PMID: 10.1111/jcpe.12679)
Simón-Soro, A. & Mira, A. Solving the etiology of dental caries. Trends Microbiol. 23, 76–82 (2015). (PMID: 10.1016/j.tim.2014.10.010)
Serrage, H. J., Jepson, M. A., Rostami, N., Jakubovics, N. S. & Nobbs, A. H. Understanding the matrix: the role of extracellular DNA in oral biofilms. Front Oral Health 2, https://doi.org/10.3389/froh.2021.640129 (2021).
Liu, Y.-L., Nascimento, M. & Burne, R. A. Progress toward understanding the contribution of alkali generation in dental biofilms to inhibition of dental caries. Int. J. Oral. Sci. 4, 135–140 (2012). (PMID: 10.1038/ijos.2012.54)
Jakubovics, N. S. et al. Critical roles of arginine in growth and biofilm development by Streptococcus gordonii. Mol. Microbiol. 97, 281–300 (2015). (PMID: 10.1111/mmi.13023)
Nascimento, M. M. et al. Oral arginine metabolism may decrease the risk for dental caries in children. J. Dent. Res. 92, 604–608 (2013). (PMID: 10.1177/0022034513487907)
Huang, X., Schulte, R. M., Burne, R. A. & Nascimento, M. M. Characterization of the arginolytic microflora provides insights into pH homeostasis in human oral biofilms. Caries Res. 49, 165–176 (2015). (PMID: 10.1159/000365296)
Kreth, J., Zhang, Y. & Herzberg, M. C. Streptococcal antagonism in oral biofilms: Streptococcus sanguinis and Streptococcus gordonii interference with Streptococcus mutans. J. Bacteriol. 190, 4632–4640 (2008). (PMID: 10.1128/JB.00276-08)
Firestone, A. R., Schmid, R. & Mühlemann, H. R. Cariogenic effects of cooked wheat starch alone or with sucrose and frequency-controlled feedings in rats. Arch. Oral. Biol. 27, 759–763 (1982). (PMID: 10.1016/0003-9969(82)90026-7)
Liao, S. et al. Streptococcus mutans extracellular DNA is upregulated during growth in biofilms, actively released via membrane vesicles, and influenced by components of the protein secretion machinery. J. Bacteriol. 196, 2355–2366 (2014). (PMID: 10.1128/JB.01493-14)
Perry, J. A., Cvitkovitch, D. G. & Lévesque, C. M. Cell death in Streptococcus mutans biofilms: a link between CSP and extracellular DNA. FEMS Microbiol. Lett. 299, 261–266 (2009). (PMID: 10.1111/j.1574-6968.2009.01758.x)
Klein, M. I. et al. Dynamics of Streptococcus mutans transcriptome in response to starch and sucrose during biofilm development. PLoS ONE 5, e13478 (2010). (PMID: 10.1371/journal.pone.0013478)
Muto, Y. & Goto, S. Transformation by extracellular DNA produced by Pseudomonas aeruginosa. FEMS Microbiol. Immunol. 30, 621–628 (1986). (PMID: 10.1111/j.1348-0421.1986.tb02989.x)
Jakubovics, N. S., Shields, R. C., Rajarajan, N. & Burgess, J. G. Life after death: the critical role of extracellular DNA in microbial biofilms. Lett. Appl. Microbiol. 57, 467–475 (2013). (PMID: 10.1111/lam.12134)
Whitchurch, C. B., Tolker-Nielsen, T., Ragas, P. C. & Mattick, J. S. Extracellular DNA required for bacterial biofilm formation. Science 295, 1487 (2002). (PMID: 10.1126/science.295.5559.1487)
Flemming, H.-C. & Wingender, J. The biofilm matrix. Nat. Rev. Microbiol. 8, 623–633 (2010). (PMID: 10.1038/nrmicro2415)
Dragoš, A. & Kovács, Á. T. The peculiar functions of the bacterial extracellular matrix. Trends Microbiol. 25, 257–266 (2017). (PMID: 10.1016/j.tim.2016.12.010)
Rostami, N. et al. A critical role for extracellular DNA in dental plaque formation. J. Dent. Res. 96, 208–216 (2017). (PMID: 10.1177/0022034516675849)
Schlafer, S., Meyer, R. L., Dige, I. & Regina, V. R. Extracellular DNA contributes to dental biofilm stability. Caries Res. 51, 436–442 (2017). (PMID: 10.1159/000477447)
Porschen, R. K. & Sonntag, S. Extracellular deoxyribonuclease production by anaerobic bacteria. Appl. Microbiol. 27, 1031–1033 (1974). (PMID: 10.1128/am.27.6.1031-1033.1974)
Palmer, L. J., Chapple, I. L. C., Wright, H. J., Roberts, A. & Cooper, P. R. Extracellular deoxyribonuclease production by periodontal bacteria. J. Periodontal Res. 47, 439–445 (2012). (PMID: 10.1111/j.1600-0765.2011.01451.x)
Mulcahy, H., Charron-Mazenod, L. & Lewenza, S. Extracellular DNA chelates cations and induces antibiotic resistance in Pseudomonas aeruginosa biofilms. PLoS Pathog. 4, e1000213 (2008). (PMID: 10.1371/journal.ppat.1000213)
Mulcahy, H., Charron-Mazenod, L. & Lewenza, S. Pseudomonas aeruginosa produces an extracellular deoxyribonuclease that is required for utilization of DNA as a nutrient source. Environ. Microbiol. 12, 1621–1629 (2010).
Binnenkade, L., Kreienbaum, M. & Thormann, K. M. Characterization of ExeM, an extracellular nuclease of Shewanella oneidensis MR-1. Front. Microbiol. 9, 1761 (2018).
Hannan, S. et al. Transfer of antibiotic resistance by transformation with eDNA within oral biofilms. FEMS Immunol. Med. Microbiol. 59, 345–349 (2010). (PMID: 10.1111/j.1574-695X.2010.00661.x)
Sumby, P. et al. Extracellular deoxyribonuclease made by group A Streptococcus assists pathogenesis by enhancing evasion of the innate immune response. Proc. Natl Acad. Sci. USA 102, 1679–1684 (2005). (PMID: 10.1073/pnas.0406641102)
Berends, E. T. et al. Nuclease expression by Staphylococcus aureus facilitates escape from neutrophil extracellular traps. J. Innate Immun. 2, 576–586 (2010). (PMID: 10.1159/000319909)
Morita, C. et al. Cell wall-anchored nuclease of Streptococcus sanguinis contributes to escape from neutrophil extracellular trap-mediated bacteriocidal activity. PLoS ONE 9, e103125 (2014). (PMID: 10.1371/journal.pone.0103125)
Fontaine, M. C., Perez-Casal, J. & Willson, P. J. Investigation of a novel DNase of Streptococcus suis Serotype 2. Infect. Immun. 72, 774–781 (2004). (PMID: 10.1128/IAI.72.2.774-781.2004)
Tong, H., Zeng, L. & Burne, R. A. The EIIABMan phosphotransferase system permease regulates carbohydrate catabolite repression in Streptococcus gordonii. Appl. Environ. Microbiol. 77, 1957–1965 (2011). (PMID: 10.1128/AEM.02385-10)
Yang, W. Nucleases: diversity of structure, function and mechanism. Q. Rev. Biophys. 44, 1–93 (2011). (PMID: 10.1017/S0033583510000181)
Podbielski, A., Zarges, I., Flosdorff, A. & Weber-Heynemann, J. Molecular characterization of a major serotype M49 group A streptococcal DNase gene (sdaD). Infect. Immun. 64, 5349–5356 (1996).
Sriskandan, S., Unnikrishnan, M., Krausz, T. & Cohen, J. Mitogenic factor (MF) is the major DNase of serotype M89 Streptococcus pyogenes. Microbiology 146, 2785–2792 (2000). (PMID: 10.1099/00221287-146-11-2785)
Remmington, A. & Turner, C. E. The DNases of pathogenic Lancefield streptococci. Microbiology 164, 242–250 (2018). (PMID: 10.1099/mic.0.000612)
Liu, J. et al. A nuclease from Streptococcus mutans facilitates biofilm dispersal and escape from killing by neutrophil extracellular traps. Front Cell Infect. Microbiol 7, 97 (2017). (PMID: 10.3389/fcimb.2017.00097)
Dlakić, M. Functionally unrelated signalling proteins contain a fold similar to Mg dependent endonucleases. Trends Biochem. Sci. 25, 272–273 (2000).
Maddi, A., Haase, E. & Scannapieco, F. Mass spectrometric analysis of whole secretome and amylase-precipitated secretome proteins from Streptococcus gordonii. J. Proteom. Bioinform. 7, 287–295 (2014).
Shelburne, S. A. 3rd et al. A direct link between carbohydrate utilization and virulence in the major human pathogen group A Streptococcus. Proc. Natl Acad. Sci. USA 105, 1698–1703 (2008).
Willenborg, J., de Greeff, A., Jarek, M., Valentin-Weigand, P. & Goethe, R. The CcpA regulon of Streptococcus suis reveals novel insights into the regulation of the streptococcal central carbon metabolism by binding of CcpA to two distinct binding motifs. Mol. Microbiol. 92, 61–83 (2014).
Zeng, L., Martino, N. C. & Burne, R. A. Two gene clusters coordinate galactose and lactose metabolism in Streptococcus gordonii. Appl. Environ. Microbiol. 78, 5597–5605 (2012).
Yasuda, T. et al. A single amino acid substitution can shift the optimum pH of DNase I for enzyme activity: biochemical and molecular analysis of the piscine DNase I family. Biochim. Biophys. Acta 1672, 174–183 (2004). (PMID: 10.1016/j.bbagen.2004.03.012)
Jang, D. S. et al. Novel high-throughput deoxyribonuclease 1 assay. J. Biomol. Screen 20, 202–211 (2015). (PMID: 10.1177/1087057114555828)
Jakubovics, N. S. Saliva as the sole nutritional source in the development of multispecies communities in dental plaque. Microbiol Spec 3, https://doi.org/10.1128/microbiolspec.MBP-0013-2014 (2015).
Shields, R. C. et al. Efficacy of a marine bacterial nuclease against biofilm forming microorganisms isolated from chronic rhinosinusitis. PLoS ONE 8, e55339 (2013). (PMID: 10.1371/journal.pone.0055339)
Sato, Y., Okamoto, K. & Kizaki, H. gbpC and pac gene mutations detected in Streptococcus mutans strain GS-5. Oral. Microbiol. Immunol. 17, 263–266 (2002).
Dong, Y., Chen, Y. Y., Snyder, J. A. & Burne, R. A. Isolation and molecular analysis of the gene cluster for the arginine deiminase system from Streptococcus gordonii DL1. Appl. Environ. Microbiol. 68, 5549–5553 (2002).
Kawarai, T., Narisawa, N., Suzuki, Y., Nagasawa, R. & Senpuku, H. Streptococcus mutans biofilm formation is dependent on extracellular DNA in primary low pH conditions. J. Oral. Biosci. 58, 55–61 (2016). (PMID: 10.1016/j.job.2015.12.004)
Tsutsumi, K., Maruyama, M., Uchiyama, A. & Shibasaki, K. Characterisation of a sucrose-independent in vitro biofilm model of supragingival plaque. Oral. Dis. 24, 465–475 (2018). (PMID: 10.1111/odi.12779)
Kreth, J., Zhu, L., Merritt, J., Shi, W. & Qi, F. Role of sucrose in the fitness of Streptococcus mutans. Oral. Microbiol. Immunol. 23, 213–219 (2008). (PMID: 10.1111/j.1399-302X.2007.00413.x)
Petersen, F. C., Tao, L. & Scheie, A. A. DNA binding-uptake system: a link between cell-to-cell communication and biofilm formation. J. Bacteriol. 187, 4392–4400 (2005). (PMID: 10.1128/JB.187.13.4392-4400.2005)
Nur, A. et al. Effects of extracellular DNA and DNA-binding protein on the development of a Streptococcus intermedius biofilm. J. Appl. Microbiol. 115, 260–270 (2013). (PMID: 10.1111/jam.12202)
Moraes, J. J. et al. Two-component system VicRK regulates functions associated with establishment of Streptococcus sanguinis in biofilms. Infect. Immun. 82, 4941–4951 (2014). (PMID: 10.1128/IAI.01850-14)
Jakubovics, N. S. Talk of the town: interspecies communication in oral biofilms. Mol. Oral. Microbiol. 25, 4–14 (2010). (PMID: 10.1111/j.2041-1014.2009.00563.x)
Nijland, R., Hall, M. J. & Burgess, J. G. Dispersal of biofilms by secreted, matrix degrading, bacterial DNase. PLoS ONE 5, e15668 (2010). (PMID: 10.1371/journal.pone.0015668)
Rainey, K., Michalek, S. M., Wen, Z. T. & Wu, H. Glycosyltransferase-mediated biofilm matrix dynamics and virulence of Streptococcus mutans. Appl Environ. Microbiol. 85, e02247–02218 (2019). (PMID: 10.1128/AEM.02247-18)
Podbielski, A., Spellerberg, B., Woischnik, M., Pohl, B. & Lütticken, R. Novel series of plasmid vectors for gene inactivation and expression analysis in group A streptococci (GAS). Gene 177, 137–147 (1996). (PMID: 10.1016/0378-1119(96)84178-3)
Kiedrowski, M. R. et al. Nuclease modulates biofilm formation in community-associated methicillin-resistant Staphylococcus aureus. PLoS One 6, e26714 (2011). (PMID: 10.1371/journal.pone.0026714)
Robinson, J. C. et al. ArcR modulates biofilm formation in the dental plaque colonizer Streptococcus gordonii. Mol. Oral. Microbiol 33, 143–154 (2018). (PMID: 10.1111/omi.12207)
Sambrook J. R. D. Molecular cloning: a laboratory manual, 3rd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y. (2001).
Samarian, D. S., Jakubovics, N. S., Luo, T. L. & Rickard, A. H. Use of a high-throughput in vitro microfluidic system to develop oral multi-species biofilms. JoVE, 52467 (2014).
Brown, J. M., Blunk, B., Williams, P. & Hardie, K. R. Microfluidic-based growth and imaging of bacterial biofilms. Bio-Protoc. 9, e3460 (2019). (PMID: 10.21769/BioProtoc.3460)
Gale, E. F. & Folkes, J. P. The assimilation of amino-acids by bacteria. XV. Actions of antibiotics on nucleic acid and protein synthesis in Staphylococcus aureus. J. Biochem. 53, 493–498 (1953). (PMID: 10.1042/bj0530493)
Mutha, N. V. R. et al. Transcriptional responses of Streptococcus gordonii and Fusobacterium nucleatum to coaggregation. Mol. Oral. Microbiol. 33, 450–464 (2018). (PMID: 10.1111/omi.12248)
Grant Information:
R01 DE016690 United States DE NIDCR NIH HHS; BB/S006818/1 United Kingdom BB_ Biotechnology and Biological Sciences Research Council
Entry Date(s):
Date Created: 20221212 Date Completed: 20221214 Latest Revision: 20230701
Update Code:
20240105
PubMed Central ID:
PMC9744736
DOI:
10.1038/s41522-022-00359-z
PMID:
36509765
Czasopismo naukowe
Extracellular DNA (eDNA) is a key component of many microbial biofilms including dental plaque. However, the roles of extracellular deoxyribonuclease (DNase) enzymes within biofilms are poorly understood. Streptococcus gordonii is a pioneer colonizer of dental plaque. Here, we identified and characterised SsnA, a cell wall-associated protein responsible for extracellular DNase activity of S. gordonii. The SsnA-mediated extracellular DNase activity of S. gordonii was suppressed following growth in sugars. SsnA was purified as a recombinant protein and shown to be inactive below pH 6.5. SsnA inhibited biofilm formation by Streptococcus mutans in a pH-dependent manner. Further, SsnA inhibited the growth of oral microcosm biofilms in human saliva. However, inhibition was ameliorated by the addition of sucrose. Together, these data indicate that S. gordonii SsnA plays a key role in interspecies competition within oral biofilms. Acidification of the medium through sugar catabolism could be a strategy for cariogenic species such as S. mutans to prevent SsnA-mediated exclusion from biofilms.
(© 2022. The Author(s).)

Ta witryna wykorzystuje pliki cookies do przechowywania informacji na Twoim komputerze. Pliki cookies stosujemy w celu świadczenia usług na najwyższym poziomie, w tym w sposób dostosowany do indywidualnych potrzeb. Korzystanie z witryny bez zmiany ustawień dotyczących cookies oznacza, że będą one zamieszczane w Twoim komputerze. W każdym momencie możesz dokonać zmiany ustawień dotyczących cookies