Conjugative transfer of ICESde3396 between three β-hemolytic streptococcal species

BMC Research Notes

David J McMillan²  Kadaba S Sriprakash³  Celia L McNeilly³  Ainslie Cameron³  Michelle J Bauer³  Josephine Shera³  Danielle J Smyth¹ 

[1] Current affiliation: Institute of Immunology and Infection Research, University of Edinburgh, Ashworth Laboratories, West Mains Road, Edinburgh EH9 3JT, UK;Inflammation and Healing Research Cluster, School of Health and Sport Sciences, University of the Sunshine Coast, Maroochydore, Queensland 4558, Australia;Bacterial Pathogenesis Laboratory, QIMR Berghofer Medical Research Institute, 300 Herston Rd, Herston, QLD 4006, Australia

关键词: Streptococcus agalactiae;    Streptococcus pyogenes;    Streptococcus dysgalactiae subsp. equisimilis;    Conjugation;    Integrative conjugative element;   

Others  :  1130550
DOI  :  10.1186/1756-0500-7-521

 received in 2014-04-02, accepted in 2014-07-31,  发布年份 2014

【 摘 要 】

Background

Integrative conjugative elements (ICEs) are mobile genetic elements (MGEs) that possess all genes necessary for excision, transfer and integration into recipient genome. They also carry accessory genes that impart new phenotypic features to recipient strains. ICEs therefore play an important role in genomic plasticity and population structure. We previously characterised ICESde3396, the first ICE identified in the β-hemolytic Streptococcus dysgalactiae subsp equisimilis (SDSE) and demonstrated its transfer to single isolates of Streptococcus pyogenes (group A streptococcus, GAS) and Streptococcus agalactiae (group B streptococcus, GBS). While molecular studies found the ICE in multiple SDSE and GBS isolates, it was absent in all GAS isolates examined.

Results

Here we demonstrate that ICESde3396:km is transferable from SDSE to multiple SDSE, GAS and GBS isolates. However not all strains of these species were successful recipients under the same growth conditions. To address the role that host factors may have in conjugation we also undertook conjugation experiments in the presence of A549 epithelial cells and DMEM. While Horizontal Gene Transfer (HGT) occurred, conjugation efficiencies were no greater than when similar experiments were conducted in DMEM. Additionally transfer to GAS NS235 was successful in the presence of DMEM but not in Todd Hewitt Broth suggesting that nutritional factors may also influence HGT. The GAS and GBS transconjugants produced in this study are also able to act as donors of the ICE.

Conclusion

We conclude that ICEs are major sources of interspecies HGT between β-hemolytic streptococci, and by introducing accessory genes imparting novel phenotypic characteristics, have the potential to alter the population structure of these species.

【 授权许可】

   
2014 Smyth et al.; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

Figure 2.

Figure 3.

【 参考文献 】

• [1]Chhatwal GS, McMillan DJ, Talay SR: Pathogenicity Factors in Group C and G Streptococci. In Gram-Positive Pathogens. 2nd edition. Edited by Fischetti VA, Novick RP, Ferretti JJ, Portnoy DA, Rood JI. Washington D.C: ASM Press; 2006:213-221.
• [2]Cunningham MW: Pathogenesis of group A streptococcal infections. Clin Microbiol Rev 2000, 13(3):470-511.
• [3]Dermer P, Lee C, Eggert J, Few B: A history of neonatal group B streptococcus with its related morbidity and mortality rates in the United States. J Pediatr Nurs 2004, 19(5):357-363.
• [4]Skoff TH, Farley MM, Petit S, Craig AS, Schaffner W, Gershman K, Harrison LH, Lynfield R, Mohle-Boetani J, Zansky S, Albanese BA, Stefonek K, Zell ER, Jackson D, Thompson T, Shrag SJ: Increasing burden of invasive group B streptococcal disease in nonpregnant adults, 1990–2007. Clin Infect Dis 2009, 49(1):85-92.
• [5]Tettelin H, Masignani V, Cieslewicz MJ, Donati C, Medini D, Ward NL, Angiuoli SV, Crabtree J, Jones AL, Durkin AS, Debroy RT, Davidsen RT, Mora M, Scarselli M, Margarit y Ros I, Peterson JD, Hauser CR, Sundarum JP, Nelson WC, Madupu R, Brinkac LM, Dodson RJ, Rosovitz MJ, Sullivan SA, Daugherty SC, Haft DH, Selengut J, Gwinn ML, Zhou L, et al.: Genome analysis of multiple pathogenic isolates of Streptococcus agalactiae: implications for the microbial “pan-genome”. Proc Natl Acad Sci U S A 2005, 102(39):13950-13955.
• [6]Beres SB, Musser JM: Contribution of exogenous genetic elements to the group A Streptococcus metagenome. PLoS ONE 2007, 2(8):e800.
• [7]Ferretti JJ, McShan WM, Ajdic D, Savic DJ, Savic G, Lyon K, Primeaux C, Sezate S, Suvorov AN, Kenton S, Lai HS, Lin SP, Qian Y, Jia HG, Najar FZ, Ren Q, Zhu H, Song L, White J, Yuan J, Yuan X, Clifton SW, Roe BA, McLaughlin R: Complete genome sequence of an M1 strain of Streptococcus pyogenes. Proc Natl Acad Sci U S A 2001, 98(8):4658-4663.
• [8]Green NM, Zhang S, Porcella SF, Nagiec MJ, Barbian KD, Beres SB, LeFebvre RB, Musser JM: Genome sequence of a serotype M28 strain of group a streptococcus: potential new insights into puerperal sepsis and bacterial disease specificity. J Infect Dis 2005, 192(5):760-770.
• [9]Suzuki H, Lefebure T, Hubisz MJ, Pavinski Bitar P, Lang P, Siepel A, Stanhope MJ: Comparative genomic analysis of the Streptococcus dysgalactiae species group: gene content, molecular adaptation, and promoter evolution. Genome Biol Evol 2011, 3:168-185.
• [10]Chuzeville S, Puymege A, Madec JY, Haenni M, Payot S: Characterization of a new CAMP factor carried by an integrative and conjugative element in Streptococcus agalactiae and spreading in Streptococci. PLoS ONE 2012, 7(11):e48918.
• [11]Brochet M, Couve E, Glaser P, Guedon G, Payot S: Integrative conjugative elements and related elements are major contributors to the genome diversity of Streptococcus agalactiae. J Bacteriol 2008, 190(20):6913-6917.
• [12]Brochet M, Rusniok C, Couve E, Dramsi S, Poyart C, Trieu-Cuot P, Kunst F, Glaser P: Shaping a bacterial genome by large chromosomal replacements, the evolutionary history of Streptococcus agalactiae. Proc Natl Acad Sci U S A 2008, 105(41):15961-15966.
• [13]Shimomura Y, Okumura K, Murayama SY, Yagi J, Ubukata K, Kirikae T, Miyoshi-Akiyama T: Complete genome sequencing and analysis of a Lancefield group G Streptococcus dysgalactiae subsp. equisimilis strain causing streptococcal toxic shock syndrome (STSS). BMC Genomics 2011, 12:17.
• [14]Davies MR, McMillan DJ, Beiko RG, Barroso V, Geffers R, Sriprakash KS, Chhatwal GS: Virulence profiling of Streptococcus dysgalactiae subspecies equisimilis isolated from infected humans reveals 2 distinct genetic lineages that do not segregate with their phenotypes or propensity to cause diseases. Clin Infect Dis 2007, 44(11):1442-1454.
• [15]Davies MR, Shera J, Van Domselaar GH, Sriprakash KS, McMillan DJ: A novel integrative conjugative element mediates genetic transfer from group G Streptococcus to other beta-hemolytic Streptococci. J Bacteriol 2009, 191(7):2257-2265.
• [16]Broudy TB, Pancholi V, Fischetti VA: Induction of lysogenic bacteriophage and phage-associated toxin from group a streptococci during coculture with human pharyngeal cells. Infect Immun 2001, 69(3):1440-1443.
• [17]Klockgether J, Wurdemann D, Reva O, Wiehlmann L, Tummler B: Diversity of the abundant pKLC102/PAGI-2 family of genomic islands in Pseudomonas aeruginosa. J Bacteriol 2007, 189(6):2443-2459.
• [18]Aziz RK, Edwards RA, Taylor WW, Low DE, McGeer A, Kotb M: Mosaic prophages with horizontally acquired genes account for the emergence and diversification of the globally disseminated M1T1 clone of Streptococcus pyogenes. J Bacteriol 2005, 187(10):3311-3318.
• [19]Walker MJ, Hollands A, Sanderson-Smith ML, Cole JN, Kirk JK, Henningham A, McArthur JD, Dinkla K, Aziz RK, Kansal RG, Simpson AJ, Buchanan JT, Chhatwal GS, Kotb M, Nizet V: DNase Sda1 provides selection pressure for a switch to invasive group A streptococcal infection. Nat Med 2007, 13(8):981-985.
• [20]Haenni M, Saras E, Bertin S, Leblond P, Madec JY, Payot S: Diversity and mobility of integrative and conjugative elements in bovine isolates of Streptococcus agalactiae, S. dysgalactiae subsp. dysgalactiae, and S. uberis. Appl Environ Microbiol 2010, 76(24):7957-7965.
• [21]Wozniak RA, Waldor MK: Integrative and conjugative elements: mosaic mobile genetic elements enabling dynamic lateral gene flow. Nat Rev Microbiol 2010, 8(8):552-563.
• [22]Lin A, Jimenez J, Derr J, Vera P, Manapat ML, Esvelt KM, Villanueva L, Liu DR, Chen IA: Inhibition of bacterial conjugation by phage M13 and its protein g3p: quantitative analysis and model. PLoS ONE 2011, 6(5):e19991.
• [23]Palmieri C, Magi G, Mingoia M, Bagnarelli P, Ripa S, Varaldo PE, Facinelli B: Characterization of a Streptococcus suis tet (O/W/32/O)-carrying element transferable to major streptococcal pathogens. Antimicrob Agents Chemother 2012, 56(9):4697-4702.
• [24]Palmieri C, Varaldo PE, Facinelli B: Streptococcus suis, an emerging drug resistant animal and human pathogen. Front Microbiol 2011, 2:235.
• [25]Davies MR, Tran TN, McMillan DJ, Gardiner DL, Currie BJ, Sriprakash KS: Inter-species genetic movement may blur the epidemiology of streptococcal diseases in endemic regions. Microbes Infect 2005, 7(9–10):1128-1138.
• [26]Delvecchio A, Currie BJ, McArthur JD, Walker MJ, Sriprakash KS: Streptococcus pyogenes prtFII, but not sfbI, sfbII or fbp54, is represented more frequently among invasive-disease isolates of tropical Australia. Epidemiol Infect 2002, 128(3):391-396.