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Comparative Genomic Analysis of Food-Originated Coagulase-Negative Staphylococcus: Analysis of Conserved Core Genes and Diversity of the Pan-Genome

  • Heo, Sojeong (Department of Food and Nutrition, Dongduk Women's University) ;
  • Lee, Jung-Sug (Department of Food and Nutrition, Kookmin University) ;
  • Lee, Jong-Hoon (Department of Food Science and Biotechnology, Kyonggi University) ;
  • Jeong, Do-Won (Department of Food and Nutrition, Dongduk Women's University)
  • Received : 2019.10.22
  • Accepted : 2019.12.05
  • Published : 2020.03.28

Abstract

To shed light on the genetic differences among food-originated coagulase-negative Staphylococcus (CNS), we performed pan-genome analysis of five species: Staphylococcus carnosus (two strains), Staphylococcus equorum (two strains), Staphylococcus succinus (three strains), Staphylococcus xylosus (two strains), and Staphylococcus saprophyticus (one strain). The pan-genome size increases with each new strain and currently holds about 4,500 genes from 10 genomes. Specific genes were shown to be strain dependent but not species dependent. Most specific genes were of unknown function or encoded restriction-modification enzymes, transposases, or prophages. Our results indicate that unique genes have been acquired or lost by convergent evolution within individual strains.

Keywords

References

  1. Gotz F, Bannerman T, Schleifer K-H. 2006. The genera Staphylococcus and Macrococcus. Prokaryotes 4: 5-75.
  2. Irlinger F. 2008. Safety assessment of dairy microorganisms: coagulase-negative staphylococci. Int. J. Food Microbiol. 126: 302-310. https://doi.org/10.1016/j.ijfoodmicro.2007.08.016
  3. Coton E, Mulder N, Coton M, Pochet S, Trip H, Lolkema JS. 2010. Origin of the putrescine-producing ability of the coagulase-negative bacterium Staphylococcus epidermidis 2015B. Appl. Environ. Microbiol. 76: 5570-5576. https://doi.org/10.1128/AEM.00441-10
  4. Widerstrom M, Wistrom J, Sjostedt A, Monsen T. 2012. Coagulase-negative staphylococci: update on the molecular epidemiology and clinical presentation, with a focus on Staphylococcus epidermidis and Staphylococcus saprophyticus. Eur. J. Clin Microbiol. Infect. Dis. 31: 7-20. https://doi.org/10.1007/s10096-011-1270-6
  5. Natoli S, Fontana C, Favaro M, Bergamini A, Testore GP, Minelli S, et al. 2009. Characterization of coagulase-negative staphylococcal isolates from blood with reduced susceptibility to glycopeptides and therapeutic options. BMC Infect. Dis. 9: 83. https://doi.org/10.1186/1471-2334-9-83
  6. Kacica MA, Horgan MJ, Preston KE, Lepow M, Venezia RA. 1994. Relatedness of coagulase-negative staphylococci causing bacteremia in low-birthweight infants. Infect. Control Hosp. Epidemiol. 15: 658-662. https://doi.org/10.2307/30145277
  7. Sung JS, Chun J, Choi S, Park W. 2012. Genome sequence of the halotolerant Staphylococcus sp. strain OJ82, isolated from Korean traditional salt-fermented seafood. J. Bacteriol. 194: 6353-6354. https://doi.org/10.1128/JB.01653-12
  8. Jeong DW, Lee JH. 2017. Complete genome sequence of Staphylococcus succinus 14BME20 isolated from a traditional Korean fermented soybean good. Genome Announc. 5: e01731-16.
  9. Rosenstein R, Nerz C, Biswas L, Resch A, Raddatz G, Schuster SC, Gotz F. 2009. Genome analysis of the meat starter culture bacterium Staphylococcus carnosus TM300. Appl. Environ. Microbiol. 75: 811-822. https://doi.org/10.1128/AEM.01982-08
  10. Labrie SJ, El Haddad L, Tremblay DM, Plante PL, Wasserscheid J, Dumaresq J, et al. 2014. First complete genome sequence of Staphylococcus xylosus, a meat starter culture and a host to propagate Staphylococcus aureus phages. Genome Announc. 2: e00671-14.
  11. Irlinger F, Loux V, Bento P, Gibrat JF, Straub C, Bonnarme P, et al. 2012. Genome sequence of Staphylococcus equorum subsp. equorum Mu2, isolated from a French smear-ripened cheese. J. Bacteriol. 194: 5141-5142. https://doi.org/10.1128/JB.01038-12
  12. Jeong DW, Na H, Ryu S, Lee JH. 2016. Complete genome sequence of Staphylococcus equorum KS1039 isolated from Saeu-jeotgal, Korean high-salt-fermented seafood. J. Biotechnol. 219: 88-89. https://doi.org/10.1016/j.jbiotec.2015.12.025
  13. Hammes WP, Hertel C. 1998. New developments in meat starter cultures. Meat Sci. 49S1: S125-138. https://doi.org/10.1016/S0309-1740(98)90043-2
  14. Fulladosa E, Garriga M, Martin B, Guardia MD, Garcia-Regueiro JA, Arnau J. 2010. Volatile profile and microbiological characterization of hollow defect in dry-cured ham. Meat Sci. 86: 801-807. https://doi.org/10.1016/j.meatsci.2010.06.025
  15. Berdague JL, Monteil P, Montel MC, Talon R. 1993. Effects of starter cultures on the formation of flavour compounds in dry sausage. Meat Sci. 35: 275-287. https://doi.org/10.1016/0309-1740(93)90033-E
  16. Sondergaard AK, Stahnke LH. 2002. Growth and aroma production by Staphylococcus xylosus, S. carnosus and S. equorum-a comparative study in model systems. Int. J. Food Microbiol. 75: 99-109. https://doi.org/10.1016/S0168-1605(01)00729-2
  17. Stahnke LH. 1994. Aroma components from dried sausages fermented with Staphylococcus xylosus. Meat Sci. 38: 39-53. https://doi.org/10.1016/0309-1740(94)90094-9
  18. Talon R, Leroy S, Lebert I, Giammarinaro P, Chacornac JP, Latorre-Moratalla M, et al. 2008. Safety improvement and preservation of typical sensory qualities of traditional dry fermented sausages using autochthonous starter cultures. Int. J. Food Microbiol. 126: 227-234. https://doi.org/10.1016/j.ijfoodmicro.2008.05.031
  19. Seitter M, Geng B, Hertel C. 2011. Binding to extracellular matrix proteins and formation of biogenic amines by food-associated coagulase-negative staphylococci. Int. J. Food Microbiol. 145: 483-487. https://doi.org/10.1016/j.ijfoodmicro.2011.01.026
  20. Seitter M, Nerz C, Rosenstein R, Gotz F, Hertel C. 2011. DNA microarray based detection of genes involved in safety and technologically relevant properties of food associated coagulase-negative staphylococci. Int. J. Food Microbiol. 145: 449-458. https://doi.org/10.1016/j.ijfoodmicro.2011.01.021
  21. Marty E, Bodenmann C, Buchs J, Hadorn R, Eugster-Meier E, Lacroix C, et al. 2012. Prevalence of antibiotic resistance in coagulase-negative staphylococci from spontaneously fermented meat products and safety assessment for new starters. Int. J. Food Microbiol. 159: 74-83. https://doi.org/10.1016/j.ijfoodmicro.2012.07.025
  22. Marino M, Frigo F, Bartolomeoli I, Maifreni M. 2011. Safety-related properties of staphylococci isolated from food and food environments. J. Appl. Microbiol. 110: 550-561. https://doi.org/10.1111/j.1365-2672.2010.04909.x
  23. Jeong DW, Lee B, Her JY, Lee KG, Lee JH. 2016. Safety and technological characterization of coagulase-negative staphylococci isolates from traditional Korean fermented soybean foods for starter development. Int. J. Food Microbiol. 236: 9-16. https://doi.org/10.1016/j.ijfoodmicro.2016.07.011
  24. Even S, Leroy S, Charlier C, Zakour NB, Chacornac JP, Lebert I, et al. 2010. Low occurrence of safety hazards in coagulase negative staphylococci isolated from fermented foodstuffs. Int. J. Food Microbiol. 139: 87-95. https://doi.org/10.1016/j.ijfoodmicro.2010.02.019
  25. Guan L, Cho KH, Lee JH. 2011. A nalysis of the c ultivable bacterial community in jeotgal, a Korean salted and fermented seafood, and identification of its dominant bacteria. Food Microbiol. 28: 101-113. https://doi.org/10.1016/j.fm.2010.09.001
  26. Jeong DW, Kim HR, Jung G, Han S, Kim CT, Lee JH. 2014. Bacterial community migration in the ripening of doenjang, a traditional Korean fermented soybean food. J. Microbiol Biotechnol. 24: 648-660. https://doi.org/10.4014/jmb.1401.01009
  27. Jung JY, Lee SH, Lee HJ, Jeon CO. 2013. Microbial succession and metabolite changes during fermentation of saeu-jeot: traditional Korean salted seafood. Food Microbiol. 34: 360-368. https://doi.org/10.1016/j.fm.2013.01.009
  28. Jung JY, Lee SH, Jeon CO. 2014. Microbial community dynamics during fermentation of doenjang-meju, traditional Korean fermented soybean. Int. J. Food Microbiol. 185: 112-120. https://doi.org/10.1016/j.ijfoodmicro.2014.06.003
  29. Nam YD, Lee SY, Lim SI. 2012. Microbial community analysis of Korean soybean pastes by next-generation sequencing. Int. J. Food Microbiol. 155: 36-42. https://doi.org/10.1016/j.ijfoodmicro.2012.01.013
  30. Jeong DW, Heo S, Lee B, Lee H, Jeong K, Her JY, et al. 2017. Effects of the predominant bacteria from meju and doenjang on the production of volatile compounds during soybean fermentation. Int. J. Food Microbiol. 262: 8-13. https://doi.org/10.1016/j.ijfoodmicro.2017.09.011
  31. Jeong DW, Lee H, Jeong K, Kim CT, Shim ST, Lee JH. 2019. Effects of starter candidates and NaCl on the production of volatile compounds during soybean fermentation. J. Microbiol. Biotechnol. 29: 8-13.
  32. Muller A, Klumpp J, Schmidt H, Weiss A. 2016. Complete genome sequence of Staphylococcus carnosus LTH 3730. Genome Announc. 4: e01038-16.
  33. Megaw J, Gilmore BF. 2016. Draft genome sequence of Staphylococcus succinus strain CSM-77, a moderately halophilic bacterium isolated from a triassic salt mine. Genome Announc. 4: e00532-00516.
  34. Zhou H, Yao Z, Shi H, Wang B, Li D, Hou J, et al. 2017. Draft genome sequence of Staphylococcus succinus subsp. succinus type strain DSM 14617, isolated from plant and soil inclusions within 25- to 35-million-year-old dominican amber. Genome Announc. 5: e01521-16.
  35. Dordet-Frisoni E, Talon R, Leroy S. 2007. Physical and genetic map of the Staphylococcus xylosus C2a chromosome. FEMS Microbiol. Lett. 266: 184-193. https://doi.org/10.1111/j.1574-6968.2006.00538.x
  36. Kuroda M, Yamashita A, Hirakawa H, Kumano M, Morkawa K, Higashide M, et al. 2005. Whole genome sequence of Staphylococcus saprophyticus reveals the pathogenesis of uncomplicated urinary tract infection. Proc. Natl. Acad. Sci. USA 102: 13272-13277. https://doi.org/10.1073/pnas.0502950102
  37. Ma AP, Jiang J, Tun HM, Mauroo NF, Yuen CS, Leung FC. 2014. Complete genome sequence of Staphylococcus xylosus HKUOPL8, a potential opportunistic pathogen of mammals. Genome Announc. 2: e00653-14.
  38. Jeong DW, Han S, Lee JH. 2014. Safety and technological characterization of Staphylococcus equorum isolates from jeotgal, a Korean high-salt-fermented seafood, for starter development. Int. J. Food Microbiol. 188: 108-115. https://doi.org/10.1016/j.ijfoodmicro.2014.07.022
  39. Goris J, Konstantinidis KT, Klappenbach JA, Coenye T, Vandamme P, Tiedje JM. 2007. DNA-DNA hybridization values and their relationship to whole-genome sequence similarities. Int. J. Syst. Evol. Microbiol. 57: 81-91. https://doi.org/10.1099/ijs.0.64483-0
  40. Blom J, Albaum SP, Doppmeier D, Puhler A, Vorholter FJ, Zakrzewski M, et al. 2009. EDGAR: a software framework for the comparative analysis of prokaryotic genomes. BMC Bioinformatics 10: 154. https://doi.org/10.1186/1471-2105-10-154
  41. Blom J, Kreis J, Spanig S, Juhre T, Bertelli C, Ernst C, et al. 2016. EDGAR 2.0: an enhanced software platform for comparative gene content analyses. Nucleic Acids Res. 44: W22-28. https://doi.org/10.1093/nar/gkw255
  42. Lerat E, Daubin V, Moran NA. 2003. From gene trees to organismal phylogeny in prokaryotes: the case of the gamma-Proteobacteria. PLoS Biol. 1: 101-109.
  43. Alikhan NF, Petty NK, Ben Zakour NL, Beatson SA. 2011. BLAST Ring Image Generator (BRIG): simple prokaryote genome comparisons. BMC Genomics. 12: 402. https://doi.org/10.1186/1471-2164-12-402
  44. Arndt D, Marcu A, Liang Y, Wishart DS. 2017. PHAST, PHASTER and PHASTEST: Tools for finding prophage in bacterial genomes. Brief Bioinform. 20: 1560-1567.
  45. Sullivan MJ, Petty NK, Beatson SA. 2011. Easyfig: a genome comparison visualizer. Bioinformatics 27: 1009-1010. https://doi.org/10.1093/bioinformatics/btr039
  46. Jeong DW, Kim HR, Lee JH. 2014. Genetic diversity of Staphylococcus equorum isolates from Saeu-jeotgal evaluated by multilocus sequence typing. Antonie. Van. Leeuwenhoek 106: 795-808. https://doi.org/10.1007/s10482-014-0249-6
  47. Medini D, Donati C, Tettelin H, Masignani V, Rappuoli R. 2005. The microbial pan-genome. Curr. Opin. Genet. Dev. 15: 589-594. https://doi.org/10.1016/j.gde.2005.09.006
  48. Novakova D, Sedlacek I, Pantucek R, Stetina V, Svec P, Petras P. 2006. Staphylococcus equorum and Staphylococcus succinus isolated from human clinical specimens. J. Med. Microbiol. 55: 523-528. https://doi.org/10.1099/jmm.0.46246-0
  49. Kwan T, Liu J, DuBow M, Gros P, Pelletier J. 2005. The complete genomes and proteomes of 27 Staphylococcus aureus bacteriophages. Proc. Natl. Acad. Sci. USA 102: 5174-5179. https://doi.org/10.1073/pnas.0501140102
  50. Zhang R, Ou HY, Gao F, Luo H. 2014. Identification of horizontally-transferred genomic islands and genome segmentation points by using the GC profile method. Curr. Genomics 15: 113-121. https://doi.org/10.2174/1389202915999140328163125
  51. Zhang R, Zhang CT. 2005. Genomic islands in the corynebacterium efficiens genome. Appl. Environ. Microbiol. 71: 3126-3130. https://doi.org/10.1128/AEM.71.6.3126-3130.2005
  52. Cuecas A, Kanoksilapatham W, Gonzalez JM. 2017. Evidence of horizontal gene transfer by transposase gene analyses in fervidobacterium species. PLoS One 12: e0173961. https://doi.org/10.1371/journal.pone.0173961
  53. Margos G, Hepner S, Mang C, Marosevic D, Reynolds SE, Krebs S, et al. 2017. Lost in plasmids: next generation sequencing and the complex genome of the tick-borne pathogen borrelia burgdorferi. BMC Genomics 18: 422. https://doi.org/10.1186/s12864-017-3804-5
  54. Arredondo-Alonso S, Willems RJ, van Schaik W, Schurch AC. 2016. On the (im)possibility of reconstructing plasmids from whole-genome short-read sequencing data. BioRxiv. 3: e000128.
  55. Haaber J, Penades JR, Ingmer H. 2017. Transfer of antibiotic resistance in Staphylococcus aureus. Trends Microbiol. 25: 893-905. https://doi.org/10.1016/j.tim.2017.05.011