Skip to main content

Advertisement

SpringerLink
Log in

Comparison of Antibiotic Resistance, Biofilm Formation and Conjugative Transfer of Staphylococcus and Enterococcus Isolates from International Space Station and Antarctic Research Station Concordia

  • Environmental Microbiology
  • Published:
Microbial Ecology Aims and scope Submit manuscript

Abstract

The International Space Station (ISS) and the Antarctic Research Station Concordia are confined and isolated habitats in extreme and hostile environments. The human and habitat microflora can alter due to the special environmental conditions resulting in microbial contamination and health risk for the crew. In this study, 29 isolates from the ISS and 55 from the Antarctic Research Station Concordia belonging to the genera Staphylococcus and Enterococcus were investigated. Resistance to one or more antibiotics was detected in 75.8 % of the ISS and in 43.6 % of the Concordia strains. The corresponding resistance genes were identified by polymerase chain reaction in 86 % of the resistant ISS strains and in 18.2 % of the resistant Concordia strains. Plasmids are present in 86.2 % of the ISS and in 78.2 % of the Concordia strains. Eight Enterococcus faecalis strains (ISS) harbor plasmids of about 130 kb. Relaxase and/or transfer genes encoded on plasmids from gram-positive bacteria like pIP501, pRE25, pSK41, pGO1 and pT181 were detected in 86.2 % of the ISS and in 52.7 % of the Concordia strains. Most pSK41-homologous transfer genes were detected in ISS isolates belonging to coagulase-negative staphylococci. We demonstrated through mating experiments that Staphylococcus haemolyticus F2 (ISS) and the Concordia strain Staphylococcus hominis subsp. hominis G2 can transfer resistance genes to E. faecalis and Staphylococcus aureus, respectively. Biofilm formation was observed in 83 % of the ISS and in 92.7 % of the Concordia strains. In conclusion, the ISS isolates were shown to encode more resistance genes and possess a higher gene transfer capacity due to the presence of three vir signature genes, virB1, virB4 and virD4 than the Concordia isolates.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  1. Novikova ND, de Boever P, Poddubko S, Deshevaya E, Polikarpov N, Rakova N, Coninx I, Mergeay M (2006) Survey of environmental biocontamination on board the International Space Station. Res Microbiol 157:5–12

    Article  PubMed  Google Scholar 

  2. Van Houdt R, De Boever P, Coninx I, Le Calvez C, Dicasillati R, Mahillon J, Mergeay M, Leys N (2009) Evaluation of the airborne bacterial population in the periodically confined Antarctic base Concordia. Microb Ecol 57:640–648

    Article  PubMed  Google Scholar 

  3. Van Houdt R, Mijnendonckx K, Leys N (2012) Microbial contamination monitoring and control during human space missions. Planet Space Sci 60:115–120

    Article  Google Scholar 

  4. Augustowska M, Dutkiewicz J (2006) Variability of airborne microflora in a hospital ward within a period of one year. Ann Agric Environ Med 13:99–106

    PubMed  Google Scholar 

  5. Bouillard L, Michel O, Dramaix M, Devleeschouwer M (2005) Bacterial contamination of indoor air, surfaces, and settled dust, and related dust endotoxin concentrations in healthy office buildings. Ann Agric Environ Med 12:187–192

    PubMed  Google Scholar 

  6. Gorny RL, Dutkiewicz J (2002) Bacterial and fungal aerosols in indoor environment in Central and Eastern European countries. Ann Agric Environ Med 9:17–23

    PubMed  Google Scholar 

  7. Gu J (2007) Microbial colonization of polymeric materials for space applications and mechanisms of biodeterioration: a review. Int Biodeterior Biodegra 59:170–179

    Article  CAS  Google Scholar 

  8. Matin A, Lynch SV (2005) Investigating the threat of bacteria grown in space. ASM News 71:235–240

    Google Scholar 

  9. Mauclaire L, Egli M (2010) Effect of simulated microgravity on growth and production of exopolymeric substances of Micrococcus luteus space and earth isolates. FEMS Immunol Med Microbiol 59:350–356

    PubMed  CAS  Google Scholar 

  10. Horneck G, Klaus DM, Mancinelli RL (2010) Space Microbiology. Microbiol Mol Biol Rev 74:121–156

    Article  PubMed  CAS  Google Scholar 

  11. Vukanti R, Model M, Leff L (2012) Effect of modeled reduced gravity conditions on bacterial morphology and physiology. BMC Microbiol 12:4–14

    Article  PubMed  CAS  Google Scholar 

  12. Frost LS, Leplae R, Summers AO, Toussaint A (2005) Mobile genetic elements: the agents of open source evolution. Nat Rev Micro 3:722–732

    Article  CAS  Google Scholar 

  13. Hacker J, Hentschel U, Dobrindt U (2003) Prokaryotic chromosomes and disease. Science 301:790–793

    Article  PubMed  CAS  Google Scholar 

  14. Hegstad K, Mikalsen T, Coque TM, Werner G, Sundsfjord A (2010) Mobile genetic elements and their contribution to the emergence of antimicrobial resistant Enterococcus faecalis and Enterococcus faecium. Clin Microbiol Infect 16:541–554

    Article  PubMed  CAS  Google Scholar 

  15. Palmer KL, Kos VN, Gilmore MS (2010) Horizontal gene transfer and the genomics of enterococcal antibiotic resistance. Curr Opin Microbiol 13:632–639

    Article  PubMed  CAS  Google Scholar 

  16. Witte W, Cuny C, Klare I, Nübel U, Strommenger B, Werner G (2008) Emergence and spread of antibiotic-resistant gram-positive bacterial pathogens. Int J Med Microbiol 298:365–377

    Article  PubMed  CAS  Google Scholar 

  17. Abajy MY, Kopeć J, Schiwon K, Burzynski M, Döring M, Bohn C, Grohmann E (2007) A type IV-secretion-like system is required for conjugative DNA transport of broad-host-range plasmid pIP501 in gram-positive bacteria. J Bacteriol 189:2487–2496

    Article  PubMed  CAS  Google Scholar 

  18. Li CS, Lin YC (2001) Storage effects on bacterial concentration: determination of impinger and filter samples. Sci Total Environ 278:231–237

    Article  PubMed  CAS  Google Scholar 

  19. Schwarz FV, Perreten V, Teuber M (2001) Sequence of the 50-kb conjugative multiresistance plasmid pRE25 from Enterococcus faecalis RE25. Plasmid 46:170–187

    Article  PubMed  CAS  Google Scholar 

  20. Caryl JA, O’Neill AJ (2009) Complete nucleotide sequence of pGO1, the prototype conjugative plasmid from the staphylococci. Plasmid 62:35–38

    Article  PubMed  CAS  Google Scholar 

  21. Firth N, Skurray RA (2006) Genetics: accessory elements and genetic exchange. In: Fischetti VA, Novick RP, Ferretti JJ (eds) Gram-positive pathogens, 2nd edn. ASM Press, Washington, DC, pp 413–426

    Google Scholar 

  22. Perez-Roth E, Kwong SM, Alcoba-Florez J, Firth N, Mendez-Alvarez S (2010) Complete nucleotide sequence and comparative analysis of pPR9, a 41.7-Kilobase conjugative staphylococcal multiresistance plasmid conferring high-level mupirocin resistance. Antimicrob Agents Chemother 54:2252–2257

    Article  PubMed  CAS  Google Scholar 

  23. Woodford N, Morrison D, Cookson B, George RC (1993) Comparison of high-level gentamicin-resistant Enterococcus faecium isolates from different continents. Antimicrob Agents Chemother 37:681–684

    Article  PubMed  CAS  Google Scholar 

  24. Werner G, Klare I, Witte W (1999) Large conjugative vanA plasmids in vancomycin-resistant Enterococcus faecium. J Clin Microbiol 37:2383–2384

    PubMed  CAS  Google Scholar 

  25. Birnboim HC, Doly J (1979) A rapid alkaline extraction procedure for screening recombinant plasmid DNA. Nucleic Acids Res 7:1513–1523

    Article  PubMed  CAS  Google Scholar 

  26. Sambrook J, Russel DW (2001) Preparation of plasmid DNA by alkaline lysis with SDS. In: Irwin N (ed) Molecular cloning. A laboratory manual. Cold Spring Harbor Laboratory Press, New York, pp 31–34

    Google Scholar 

  27. Barton BM, Harding GP, Zuccarelli AJ (1995) A general method for detecting and sizing large plasmids. Anal Biochem 226:235–240

    Article  PubMed  CAS  Google Scholar 

  28. Freitas AR, Tedim AP, Novais C, Ruiz-Garbajosa P, Werner G, Laverde-Gomez JA, Canton R, Peixe L, Baquero F, Coque TM (2010) Global spread of the colonization-virulence hyl Efm gene in megaplasmids of CC17 Enterococcus faecium polyclonal sub-cluster. Antimicrob Agents Chemother 54:2660–2665

    Article  PubMed  CAS  Google Scholar 

  29. Francia MV, Varsaki A, Garcillán-Barcia MP, Latorre A, Drainas C, de la Cruz F (2004) A classification scheme for mobilization regions of bacterial plasmids. FEMS Microbiol Rev 28:79–100

    Article  PubMed  CAS  Google Scholar 

  30. Garcillán-Barcia MP, Francia MV, de La Cruz F (2009) The diversity of conjugative relaxases and its application in plasmid classification. FEMS Microbiol Rev 33:657–687

    Article  PubMed  Google Scholar 

  31. Smillie C, Garcillán-Barcia MP, Francia MV, Rocha EPC, de la Cruz F (2010) Mobility of plasmids. Microbiol Mol Biol Rev 74:434–452

    Article  PubMed  CAS  Google Scholar 

  32. Higgins DG, Thompson JD, Gibson TJ (1996) Using CLUSTAL for multiple sequence alignments. Methods Enzymol 266:383–402

    Article  PubMed  CAS  Google Scholar 

  33. Christensen GD, Simpson A, Younger JJ, Baddour LM, Barrett FF, Melton DM, Beachey EH (1985) Adherence of coagulase-negative staphylococci to plastic tissue culture plates: a quantitative model for the adherence of staphylococci to medical devices. J Clin Microbiol 22:996–1006

    PubMed  CAS  Google Scholar 

  34. Klingenberg C, Aarag E, Rønnestad A, Sollid JE, Abrahamsen TG, Kjeldsen G, Flægstad T (2005) Coagulase-negative staphylococcal sepsis in neonates: association between antibiotic resistance, biofilm formation and the host inflammatory response. Pediatr Infect Dis J 24:817–822

    Article  PubMed  Google Scholar 

  35. Camilli R, Pantosti A, Baldassarri L (2011) Contribution of serotype and genetic background to biofilm formation by Streptococcus pneumoniae. Eur J Clin Microbiol Infect Dis 30:97–102

    Article  PubMed  CAS  Google Scholar 

  36. Di Rosa R, Creti R, Venditti M, D'Amelio R, Arciola CR, Montanaro L, Baldassarri L (2006) Relationship between biofilm formation, the enterococcal surface protein (Esp) and gelatinase in clinical isolates of Enterococcus faecalis and Enterococcus faecium. FEMS Microbiol Lett 256:145–150

    Article  PubMed  Google Scholar 

  37. Djordjevic D, Wiedmann M, McLandsborough LA (2002) Microtiter plate assay for assessment of Listeria monocytogenes biofilm formation. Appl Environ Microbiol 68:2950–2958

    Article  PubMed  CAS  Google Scholar 

  38. Ong CY, Beatson SA, McEwan AG, Schembri MA (2009) Conjugative plasmid transfer and adhesion dynamics in an Escherichia coli biofilm. Appl Environ Microbiol 75:6783–6791

    Article  PubMed  CAS  Google Scholar 

  39. Timmery S, Hu X, Mahillon J (2011) Characterization of bacilli isolated from the confined environments of the Antarctic Concordia station and the International Space Station. Astrobiology 11:323–334

    Article  PubMed  CAS  Google Scholar 

  40. Chi MC, Li CS (2006) Analysis of bioaerosols from chicken houses by culture and non-culture method. Aerosol Sci Technol 40:1071–1079

    Article  CAS  Google Scholar 

  41. Yao M, Mainelis G (2007) Analysis of portable impactor performance for enumeration of viable bioaerosols. J Occup Environ Hyg 4:514–524

    Article  PubMed  Google Scholar 

  42. Novikova ND (2004) Review of the knowledge of microbial contamination of the Russian manned spacecraft. Microbial Ecol 47:127–132

    Article  CAS  Google Scholar 

  43. Bonetta S, Bonetta S, Mosso S, Sampò S, Carraro E (2010) Assessment of microbiological indoor air quality in an Italian office building equipped with an HVAC system. Environ Monit Assess 161:473–483

    Article  PubMed  Google Scholar 

  44. Dybwad M, Granum PE, Bruheim P, Blatny JM (2012) Characterization of airborne bacteria at an underground subway station. Appl Environ Microbiol 78:1917–1929

    Article  PubMed  CAS  Google Scholar 

  45. Malachowa N, DeLeo F (2010) Mobile genetic elements of Staphylococcus aureus. Cellular and Molecular Life Sciences 67:3057-3071

    Google Scholar 

  46. Otto M (2010) Staphylococcus colonization of the skin and antimicrobial peptides. Expert Rev Dermatol 5:183–195

    Article  PubMed  CAS  Google Scholar 

  47. Piette A, Verschraegen G (2009) Role of coagulase-negative staphylococci in human disease. Vet Microbiol 134:45–54

    Article  PubMed  CAS  Google Scholar 

  48. Solheim M, Brekke M, Snipen L, Willems R, Nes I, Brede D (2011) Comparative genomic analysis reveals significant enrichment of mobile genetic elements and genes encoding surface structure-proteins in hospital-associated clonal complex 2 Enterococcus faecalis. BMC Microbiol 11:3–14

    Article  PubMed  CAS  Google Scholar 

  49. Kleine B, Gatermann S, Sakinc T (2010) Genotypic and phenotypic variation among Staphylococcus saprophyticus from human and animal isolates. BMC Res Notes 3:163–167

    Article  PubMed  Google Scholar 

  50. Frank KL, del Pozo JL, Patel R (2008) From clinical microbiology to infection pathogenesis: How daring to be different works for Staphylococcus lugdunensis. Clin Microbiol Rev 21:111–133

    Article  PubMed  CAS  Google Scholar 

  51. Aponte VM, Finch DS, Klaus DM (2006) Considerations for non-invasive in-flight monitoring of astronaut immune status with potential use of MEMS and NEMS devices. Life Sci 79:1317–1333

    Article  PubMed  CAS  Google Scholar 

  52. Crucian B, Lee P, Stowe R, Jones J, Effenhauser R, Widen R, Sams C (2007) Immune system changes during simulated planetary exploration on Devon Island, high Arctic. BMC Immunol 8:7–19

    Article  PubMed  Google Scholar 

  53. Rykova MP, Antropova EN, Larina IM, Morukov BV (2008) Humoral and cellular immunity in cosmonauts after the ISS missions. Acta Astro 63:697–705

    Article  Google Scholar 

  54. Schwarz S, Feßler AT, Hauschild T, Kehrenberg C, Kadlec K (2011) Plasmid-mediated resistance to protein biosynthesis inhibitors in staphylococci. Ann N Y Acad Sci 1241:82–103

    Article  PubMed  CAS  Google Scholar 

  55. Zmantar T, Kouidhi B, Miladi H, Bakhrouf A (2011) Detection of macrolide and disinfectant resistance genes in clinical Staphylococcus aureus and coagulase-negative staphylococci. BMC Res Notes 4:453–461

    Article  PubMed  CAS  Google Scholar 

  56. Gryczan T, Israeli-Reches M, Del Bue M, Dubnau D (1984) DNA sequence and regulation of ermD, a macrolide-lincosamide-streptogramin B resistance element from Bacillus licheniformis. Mol Gen Genet 194:349–356

    Article  PubMed  CAS  Google Scholar 

  57. Monod M, Mohan S, Dubnau D (1987) Cloning and analysis of ermG, a new macrolide-lincosamide-streptogramin B resistance element from Bacillus sphaericus. J Bacteriol 169:340–350

    PubMed  CAS  Google Scholar 

  58. Van Hoek AHAM, Mevius D, Guerra B, Mullany P, Roberts AP, Aarts HJM (2011) Acquired antibiotic resistance genes: an overview. Front Microbiol 2:203–228

    PubMed  Google Scholar 

  59. Roberts MC (2008) Update on macrolide–lincosamide–streptogramin, ketolide, and oxazolidinone resistance genes. FEMS Microbiol Lett 282:147–159

    Article  PubMed  CAS  Google Scholar 

  60. Wang Y, Wang G, Shoemaker NB, Whitehead TR, Salyers AA (2005) Distribution of the ermG gene among bacterial isolates from porcine intestinal contents. Appl Environ Microbiol 71:4930–4934

    Article  PubMed  CAS  Google Scholar 

  61. Grohmann E, Muth G, Espinosa M (2003) Conjugative plasmid transfer in gram-positive bacteria. Microbiol Mol Biol Rev 67:277–301

    Article  PubMed  CAS  Google Scholar 

  62. Diep BA, Gill SR, Chang RF, Phan TH, Chen JH, Davidson MG, Lin F, Lin J, Carleton HA, Mongodin EF, Sensabaugh GF, Perdreau-Remington F (2006) Complete genome sequence of USA300, an epidemic clone of community-acquired methicillin-resistant Staphylococcus aureus. Lancet 367:731–739

    Article  PubMed  CAS  Google Scholar 

  63. Chopra I, Roberts M (2001) Tetracycline antibiotics: mode of action, applications, molecular biology, and epidemiology of bacterial resistance. Microbiol Mol Biol Rev 65:232–260

    Article  PubMed  CAS  Google Scholar 

  64. Roberts MC, Sutcliffe J, Courvalin P, Jensen LB, Rood J, Seppala H (1999) Nomenclature for macrolide and macrolide-lincosamide-streptogramin B resistance determinants. Antimicrob Agents Chemother 43:2823–2830

    PubMed  CAS  Google Scholar 

  65. Zhu W, Murray PR, Huskins WC, Jernigan JA, McDonald LC, Clark NC, Anderson KF, McDougal LK, Hageman JC, Olsen-Rasmussen M, Frace M, Alangaden GJ, Chenoweth C, Zervos MJ, Robinson-Dunn B, Schreckenberger PC, Reller LB, Rudrik JT, Patel JB (2010) Dissemination of an Enterococcus Inc18-Like vanA plasmid associated with vancomycin-resistant Staphylococcus aureus. Antimicrob Agents Chemother 54:4314–4320

    Article  PubMed  CAS  Google Scholar 

  66. De Boever P, Mergeay M, Ilyin V, Forget-Hanus D, van der Auwera G, Mahillon J (2007) Conjugation-mediated plasmid exchange between bacteria grown under space flight conditions. Microgravity Sci Technol 19:138–144

    Article  Google Scholar 

  67. Beuls E, Van Houdt R, Leys N, Dijkstra C, Larkin O, Mahillon J (2009) Bacillus thuringiensis conjugation in simulated microgravity. Astrobiol 9:797–805

    Article  CAS  Google Scholar 

  68. Storrs-Mabilat M (2001) Study of a microbial detection system for space applications. Second Workshop on Advanced Life Support, Noordwijk, The Netherlands

  69. Wilson JW, Ott CM, Zu Bentrup KH, Ramamurthy R, Quick L, Porwollik S, Cheng P, McClelland M, Tsaprailis G, Radabaugh T, Hunt A, Fernandez D, Richter E, Shah M, Kilcoyne M, Joshi L, Nelman-Gonzalez M, Hing S, Parra M, Dumars P, Norwood K, Bober R, Devich J, Ruggles A, Goulart C, Rupert M, Stodieck L, Stafford P, Catella L, Schurr MJ, Buchanan K, Morici L, McCracken J, Allen P, Baker-Coleman C, Hammond T, Vogel J, Nelson R, Pierson DL, Stefanyshyn-Piper HM, Nickerson CA (2007) Space flight alters bacterial gene expression and virulence and reveals a role for global regulator Hfq. Proc Natl Acad Sci USA 104:16299–16304

    Article  PubMed  CAS  Google Scholar 

  70. Smith MS, Yang RK, Knapp CW, Niu Y, Peak N, Hanfelt MM, Galland JC, Graham DW (2004) Quantification of tetracycline resistance genes in feedlot lagoons by real-time PCR. Appl Environ Microbiol 70:7372–7377

    Article  PubMed  CAS  Google Scholar 

  71. Perreten V, Vorlet-Fawer L, Slickers P, Ehricht R, Kuhnert P, Frey J (2005) Microarray-based detection of 90 antibiotic resistance genes of gram-positive bacteria. J Clin Microbiol 43:2291–2302

    Article  PubMed  CAS  Google Scholar 

  72. Tomich PK, An FY, Damle SP, Clewell DB (1979) Plasmid-related transmissibility and multiple drug resistance in Streptococcus faecalis subsp. zymogenes strain DS16. Antimicrob Agents Chemother 15:828–830

    Article  PubMed  CAS  Google Scholar 

  73. Paulsen IT, Banerjei L, Myers GSA, Nelson KE, Seshadri R, Read TD, Fouts DE, Eisen JA, Gill SR, Heidelberg JF, Tettelin H, Dodson RJ, Umayam L, Brinkac L, Beanan M, Daugherty S, DeBoy RT, Durkin S, Kolonay J, Madupu R, Nelson W, Vamathevan J, Tran B, Upton J, Hansen T, Shetty J, Khouri H, Utterback T, Radune D, Ketchum KA, Dougherty BA, Fraser CM (2003) Role of mobile DNA in the evolution of vancomycin-resistant Enterococcus faecalis. Science 299:2071–2074

    Article  PubMed  CAS  Google Scholar 

  74. Jacob AE, Hobbs SJ (1974) Conjugal transfer of plasmid-borne multiple antibiotic resistance in S. faecalis var. zymogenes. J Bacteriol 117:360–372

    PubMed  CAS  Google Scholar 

  75. Evans RP Jr, Macrina FL (1983) Streptococcal R plasmid pIP501: endonuclease site map, resistance determinant location, and construction of novel derivatives. J Bacteriol 154:1347–1355

    PubMed  CAS  Google Scholar 

  76. Ike Y, Craig RA, White BA, Yagi Y, Clewell DB (1983) Modification of Streptococcus faecalis sex pheromones after acquisition of plasmid DNA. Proc Natl Acad Sci USA 80:5369–5373

    Article  PubMed  CAS  Google Scholar 

  77. Garcia-Migura L, Hasman H, Jensen L (2009) Presence of pRI1: a small cryptic mobilizable plasmid isolated from Enterococcus faecium of human and animal origin. Curr Microbiol 58:95–100

    Article  PubMed  CAS  Google Scholar 

  78. Khan SA, Carleton SM, Novick RP (1981) Replication of plasmid pT181 DNA in vitro: requirement for a plasmid-encoded product. Proc Natl Acad Sci USA 78:4902–4906

    Article  PubMed  CAS  Google Scholar 

  79. Firth N, Ridgway KP, Byrne ME, Fink PD, Johnson L, Paulsen IT, Skurray RA (1993) Analysis of a transfer region from the staphylococcal conjugative plasmid pSK41. Gene 136:13–25

    Article  PubMed  CAS  Google Scholar 

  80. Horinouchi S, Weisblum B (1982) Nucleotide sequence and functional map of pC194, a plasmid that specifies inducible chloramphenicol resistance. J Bacteriol 150:815–825

    PubMed  CAS  Google Scholar 

  81. Vakulenko SB, Donabedian SM, Voskresenskiy AM, Zervos MJ, Lerner SA, Chow JW (2003) Multiplex PCR for detection of aminoglycoside resistance genes in enterococci. Antimicrob Agents Chemother 47:1423–1426

    Google Scholar 

  82. Böckelmann U, Dorries H, Ayuso-Gabella MN, de Salgot Marcay M, Tandoi V, Levantesi C, Masciopinto C, van Houtte E, Szewzyk U, Wintgens T, Grohmann E (2009) Quantitative PCR monitoring of antibiotic resistance genes and bacterial pathogens in three European artificial groundwater recharge systems. Appl Environ Microbiol 75:154–163

    Article  PubMed  Google Scholar 

  83. Tenover FC, Rasheed JK (2004) Detection of antimicrobial resistance genes and mutations associated with antimicrobial resistance in microorganisms. In: Persing DH, Tenover FG, Versalovic J, Tang YUER, Relman WTJ (eds) Molecular microbiology: diagnostics principles and practice, vol 1. ASM Press, Washington DC, pp 391–406

    Google Scholar 

  84. Miele A, Bandera M, Goldstein BP (1995) Use of primers selective for vancomycin resistance genes to determine van genotype in enterococci and to study gene organization in VanA isolates. Antimicrob Agents Chemother 39:1772–1778

    Article  PubMed  CAS  Google Scholar 

  85. Depardieu F, Perichon B, Courvalin P (2004) Detection of the van Alphabet and identification of enterococci and staphylococci at the species level by multiplex PCR. J Clin Microbiol 42:5857–5860

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by grants Microbial ISS Gene Exchange and Concordia microbial dynamics from BMWi/DLR (to E.G.) and from Belspo/PRODEX (to R.V.H.). Support of the European Space Agency (ESA) as well as the French Polar Institute (IPEV) and the Italian Antarctic Programme (PNRA) are acknowledged. We thank Vacheslav Ilyin for providing crew samples and all MISSEX and COMICS partners for their constant support and advice. Skillful technical assistance of Christine Bohn and Carola Fleige is highly acknowledged. Special thanks to Prof. Dr. Vincent Perreten for providing the strains E. casseliflavus UC73, E. faecalis RE25, E. faecium SF11770, Enterococcus gallinarum SF9117, L. lactis K214 and S. haemolyticus VPS617, and to Prof. David Dubnau for Bacillus subtilis BP662 and B. subtilis BD1156.

Author information

Author notes

  1. Karsten Arends

    Present address: Robert Koch-Institute, DGZ-Ring 1, 13086, Berlin, Germany

Authors and Affiliations

  1. Department of Environmental Microbiology/Genetics, Technical University, Ernst-Reuter-Platz 1, 10587, Berlin, Germany

    Katarzyna Schiwon, Karsten Arends, Katja Marie Rogowski, Svea Fürch, Katrin Prescha & Elisabeth Grohmann

  2. Division of Infectious Diseases, University Medical Centre Freiburg, Hugstetter Strasse 55, 79106, Freiburg, Germany

    Türkan Sakinc & Elisabeth Grohmann

  3. Unit of Microbiology, Belgian Nuclear Research Centre (SCK•CEN), 2400, Mol, Belgium

    Rob Van Houdt

  4. Natl. Reference Centre for Staphylococci and Enterococci, Division FG 13 Nosocomial Infections, Robert Koch Institute, Wernigerode Branch, Burgstr. 37, 38855, Wernigerode, Germany

    Guido Werner

Authors
  1. Katarzyna Schiwon
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Karsten Arends
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Katja Marie Rogowski
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Svea Fürch
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Katrin Prescha
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Türkan Sakinc
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Rob Van Houdt
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Guido Werner
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Elisabeth Grohmann
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Elisabeth Grohmann.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Schiwon, K., Arends, K., Rogowski, K.M. et al. Comparison of Antibiotic Resistance, Biofilm Formation and Conjugative Transfer of Staphylococcus and Enterococcus Isolates from International Space Station and Antarctic Research Station Concordia. Microb Ecol 65, 638–651 (2013). https://doi.org/10.1007/s00248-013-0193-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00248-013-0193-4

Keywords

Search

Navigation