Extremophiles

, Volume 17, Issue 5, pp 767–774 | Cite as

An ICEBs1-like element may be associated with the extreme radiation and desiccation resistance of Bacillus pumilus SAFR-032 spores

Original Paper

Abstract

Comparisons of the genomes of Bacillus pumilus SAFR-032 and the closely related type strain, B. pumilus ATCC7061T, exposed an extended region of non-homologous genes. A detailed examination of this region revealed the presence of an ICEBs1-like integrative conjugative element in SAFR-032. A similar element was subsequently located elsewhere in the ATCC7061T genome. A detailed comparison of these elements and the ICEBs1 of B. subtilis revealed extremely rapid flux in gene content, genome organization and sequence similarity. It is not clear if the B. pumilus elements as they are currently structured are functional. However, it is clear that the past involvement of these elements has brought multiple genes of unknown function to the SAFR-032 genome and these genes may be responsible for the rapid evolution that led to the extreme radiation and desiccation resistance of this organism’s spores.

Keywords

Genome analysis Comparative genomics Radiation resistance Planetary protection Integrative conjugative elements 

Abbreviations

ICE

Integrative and conjugative element

SAFR-032

Bacillus pumilus strain SAFR-032

ATCC7061T

Bacillus pumilus ATCC7061T

BSU

Bacillus subtilis

HP

Hypothetical protein

CHP

Conserved hypothetical protein

BAT

Gene locus tag number for the type strain B. pumilus ATCC7061T

BPUM

Gene locus tag number for B. pumilus SAFR-032

Supplementary material

792_2013_559_MOESM1_ESM.docx (290 kb)
Supplementary Figure S1 Supplementary Figure S2 Supplementary Table S1 (DOCX 289 kb)

References

  1. Armshaw P, Pembroke JT (2013) Generation and analysis of an ICE R391 deletion library identifies genes involved in the element encoded UV-inducible cell-sensitising function. FEMS Microbiol Lett. doi:10.1111/1574-6968.12107 PubMedGoogle Scholar
  2. Auchtung JM, Lee CA, Monson RE, Lehman AP, Grossman AD (2005) Regulation of a Bacillus subtilis mobile genetic element by intercellular signaling and the global DNA damage response. Proc Natl Acad Sci USA 102(35):12554–12559. doi:10.1073/pnas.0505835102 PubMedCrossRefGoogle Scholar
  3. Auchtung JM, Lee CA, Garrison KL, Grossman AD (2007) Identification and characterization of the immunity repressor (ImmR) that controls the mobile genetic element ICEBs1 of Bacillus subtilis. Mol Microbiol 64(6):1515–1528. doi:10.1111/j.1365-2958.2007.05748.x PubMedCrossRefGoogle Scholar
  4. Bose B, Grossman AD (2011) Regulation of horizontal gene transfer in Bacillus subtilis by activation of a conserved site-specific protease. J Bacteriol 193(1):22–29. doi:10.1128/JB.01143-10 PubMedCrossRefGoogle Scholar
  5. Bose B, Auchtung JM, Lee CA, Grossman AD (2008) A conserved anti-repressor controls horizontal gene transfer by proteolysis. Mol Microbiol 70(3):570–582. doi:10.1111/j.1365-2958.2008.06414.x PubMedCrossRefGoogle Scholar
  6. Checinska A, Burbank M, Paszczynski AJ (2012) Protection of Bacillus pumilus spores by catalases. Appl Environ Microbiol 78(18):6413–6422. doi:10.1128/AEM.01211-12 PubMedCrossRefGoogle Scholar
  7. Davis BM, Waldor MK (2013) Horizontal gene transfer: linking sex and cell fate. Curr Biol 23(3):R118–R119. doi:10.1016/j.cub.2012.12.035 PubMedCrossRefGoogle Scholar
  8. Frost LS, Koraimann G (2010) Regulation of bacterial conjugation: balancing opportunity with adversity. Future Microbiol 5(7):1057–1071. doi:10.2217/fmb.10.70 PubMedCrossRefGoogle Scholar
  9. Garcillan-Barcia MP, Francia MV, de la Cruz F (2009) The diversity of conjugative relaxases and its application in plasmid classification. FEMS Microbiol Rev 33(3):657–687PubMedCrossRefGoogle Scholar
  10. Gioia J, Yerrapragada S, Qin X, Jiang H, Igboeli OC, Muzny D, Dugan-Rocha S, Ding Y, Hawes A, Liu W, Perez L, Kovar C, Dinh H, Lee S, Nazareth L, Blyth P, Holder M, Buhay C, Tirumalai MR, Liu Y, Dasgupta I, Bokhetache L, Fujita M, Karouia F, Eswara Moorthy P, Siefert J, Uzman A, Buzumbo P, Verma A, Zwiya H, McWilliams BD, Olowu A, Clinkenbeard KD, Newcombe D, Golebiewski L, Petrosino JF, Nicholson WL, Fox GE, Venkateswaran K, Highlander SK, Weinstock GM (2007) Paradoxical DNA repair and peroxide resistance gene conservation in Bacillus pumilus SAFR-032. PLoS ONE 2(9):e928PubMedCrossRefGoogle Scholar
  11. Giorno R, Bozue J, Cote C, Wenzel T, Moody KS, Mallozzi M, Ryan M, Wang R, Zielke R, Maddock JR, Friedlander A, Welkos S, Driks A (2007) Morphogenesis of the Bacillus anthracis spore. J Bacteriol 189(3):691–705. doi:10.1128/JB.00921-06 PubMedCrossRefGoogle Scholar
  12. Guglielmini J, Quintais L, Garcillan-Barcia MP, de la Cruz F, Rocha EP (2011) The repertoire of ICE in prokaryotes underscores the unity, diversity, and ubiquity of conjugation. PLoS Genet 7(8):e1002222. doi:10.1371/journal.pgen.1002222 PubMedCrossRefGoogle Scholar
  13. Hastings PJ, Rosenberg SM, Slack A (2004) Antibiotic-induced lateral transfer of antibiotic resistance. Trends Microbiol 12(9):401–404. doi:10.1016/j.tim.2004.07.003 PubMedCrossRefGoogle Scholar
  14. Jones DT, Swindells MB (2002) Getting the most from PSI-BLAST. Trends Biochem Sci 27(3):161–164PubMedCrossRefGoogle Scholar
  15. Kempf MJ, Chen F, Kern R, Venkateswaran K (2005) Recurrent isolation of hydrogen peroxide-resistant spores of Bacillus pumilus from a spacecraft assembly facility. Astrobiology 5(3):391–405PubMedCrossRefGoogle Scholar
  16. Lazarevic V, Dusterhoft A, Soldo B, Hilbert H, Mauel C, Karamata D (1999) Nucleotide sequence of the Bacillus subtilis temperate bacteriophage SPbetac2. Microbiology 145(Pt 5):1055–1067PubMedCrossRefGoogle Scholar
  17. Lee CA, Auchtung JM, Monson RE, Grossman AD (2007) Identification and characterization of int (integrase), xis (excisionase) and chromosomal attachment sites of the integrative and conjugative element ICEBs1 of Bacillus subtilis. Mol Microbiol 66(6):1356–1369. doi:10.1111/j.1365-2958.2007.06000.x PubMedGoogle Scholar
  18. Lee CA, Babic A, Grossman AD (2010) Autonomous plasmid-like replication of a conjugative transposon. Mol Microbiol 75(2):268–279PubMedCrossRefGoogle Scholar
  19. Lee CA, Thomas J, Grossman AD (2012) The Bacillus subtilis conjugative transposon ICEBs1 mobilizes plasmids lacking dedicated mobilization functions. J Bacteriol 194(12):3165–3172. doi:10.1128/JB.00301-12 PubMedCrossRefGoogle Scholar
  20. Link L, Sawyer J, Venkateswaran K, Nicholson W (2004) Extreme spore UV resistance of Bacillus pumilus isolates obtained from an ultraclean Spacecraft Assembly Facility. Microb Ecol 47(2):159–163PubMedCrossRefGoogle Scholar
  21. Markowitz VM, Chen IM, Palaniappan K, Chu K, Szeto E, Grechkin Y, Ratner A, Jacob B, Huang J, Williams P, Huntemann M, Anderson I, Mavromatis K, Ivanova NN, Kyrpides NC (2012) IMG: the Integrated Microbial Genomes database and comparative analysis system. Nucleic Acids Res 40(Database issue):D115–22Google Scholar
  22. Mizuno M, Masuda S, Takemaru K, Hosono S, Sato T, Takeuchi M, Kobayashi Y (1996) Systematic sequencing of the 283 kb 210 degrees-232 degrees region of the Bacillus subtilis genome containing the skin element and many sporulation genes. Microbiology 142(Pt 11):3103–3111PubMedCrossRefGoogle Scholar
  23. Newcombe DA, Schuerger AC, Benardini JN, Dickinson D, Tanner R, Venkateswaran K (2005) Survival of spacecraft-associated microorganisms under simulated Martian UV irradiation. Appl Environ Microbiol 71(12):8147–8156PubMedCrossRefGoogle Scholar
  24. Nicholson WL, McCoy LE, Kerney KR, Ming DW, Golden DC, Schuerger AC (2012) Aqueous extracts of a Mars analogue regolith that mimics the Phoenix landing site do not inhibit spore germination or growth of model spacecraft contaminants Bacillus subtilis 168 and Bacillus pumilus SAFR-032. Icarus 220(2):904–910. doi:10.1016/j.icarus.2012.06.033 CrossRefGoogle Scholar
  25. Satomi M, La Duc MT, Venkateswaran K (2006) Bacillus safensis sp. nov., isolated from spacecraft and assembly-facility surfaces. Int J Syst Evol Microbiol 56(Pt 8):1735–1740PubMedCrossRefGoogle Scholar
  26. Smillie C, Garcillan-Barcia MP, Francia MV, Rocha EP, de la Cruz F (2010) Mobility of plasmids. Microbiol Mol Biol Rev 74(3):434–452. doi:10.1128/MMBR.00020-10 PubMedCrossRefGoogle Scholar
  27. Thomas J, Lee CA, Grossman AD (2013) A conserved helicase processivity factor is needed for conjugation and replication of an integrative and conjugative element. PLoS Genet 9(1):e1003198PubMedCrossRefGoogle Scholar
  28. Tirumalai MR, Rastogi R, Zamani N, O’Bryant Williams E, Allen S, Diouf F, Kwende S, Weinstock GM, Venkateswaran KJ, Fox GE (2013) Candidate genes that may be responsible for the unusual resistances exhibited by B. pumilus SAFR-032 spores. PLoS One 8(6):e66012. doi:10.1371/journal.pone.0066012
  29. Venkateswaran K, Satomi M, Chung S, Kern R, Koukol R, Basic C, White D (2001) Molecular microbial diversity of a spacecraft assembly facility. Syst Appl Microbiol 24(2):311–320PubMedCrossRefGoogle Scholar
  30. Venkateswaran K, Kempf M, Chen F, Satomi M, Nicholson W, Kern R (2003) Bacillus nealsonii sp. nov., isolated from a spacecraft-assembly facility, whose spores are gamma-radiation resistant. Int J Syst Evol Microbiol 53(Pt 1):165–172PubMedCrossRefGoogle Scholar
  31. Venkateswaran K, Chung S, Allton J, Kern R (2004) Evaluation of various cleaning methods to remove bacillus spores from spacecraft hardware materials. Astrobiology 4(3):377–390PubMedGoogle Scholar
  32. Viswanath L, Lu Y, Fox GE (2007) Genome display tool: visualizing features in complex data sets. Source Code Biol Med 2:1PubMedCrossRefGoogle Scholar
  33. Wozniak RA, Waldor MK (2010) Integrative and conjugative elements: mosaic mobile genetic elements enabling dynamic lateral gene flow. Nat Rev Microbiol 8(8):552–563. doi:10.1038/nrmicro2382 PubMedCrossRefGoogle Scholar

Copyright information

© Springer Japan 2013

Authors and Affiliations

  1. 1.Department of Biology and BiochemistryUniversity of HoustonHoustonUSA

Personalised recommendations