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

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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.

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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

References

  • 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

    PubMed  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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):657–687

    Article  PubMed  CAS  Google Scholar 

  • 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):e928

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Jones DT, Swindells MB (2002) Getting the most from PSI-BLAST. Trends Biochem Sci 27(3):161–164

    Article  PubMed  CAS  Google Scholar 

  • 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):391–405

    Article  PubMed  CAS  Google Scholar 

  • 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):1055–1067

    Article  PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Lee CA, Babic A, Grossman AD (2010) Autonomous plasmid-like replication of a conjugative transposon. Mol Microbiol 75(2):268–279

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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):159–163

    Article  PubMed  CAS  Google Scholar 

  • 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):D115–22

  • 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):3103–3111

    Article  PubMed  CAS  Google Scholar 

  • 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):8147–8156

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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):1735–1740

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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):e1003198

    Article  PubMed  CAS  Google Scholar 

  • 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

  • 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):311–320

    Article  PubMed  CAS  Google Scholar 

  • 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):165–172

    Article  PubMed  CAS  Google Scholar 

  • 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):377–390

    PubMed  CAS  Google Scholar 

  • Viswanath L, Lu Y, Fox GE (2007) Genome display tool: visualizing features in complex data sets. Source Code Biol Med 2:1

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported in part by grants from the Institute of Space Systems Operations at the University of Houston, the Center for Bio-nanotechnology and Environmental Research at Texas Southern University (NASA Cooperative agreement NNX08B4A47A), and the Center for Ribosomal Evolution and Adaptation at the Georgia Institute of Technology (NASA Cooperative Agreement NNA09DA78A).

Conflict of interest

The authors declare that they have no conflict of interest.

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All work described in this manuscript was performed in accordance with current laws in the United States of America.

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Authors and Affiliations

  1. Department of Biology and Biochemistry, University of Houston, Houston, TX, 77204-5001, USA

    Madhan R. Tirumalai & George E. Fox

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  1. Madhan R. Tirumalai
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  2. George E. Fox
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Correspondence to George E. Fox.

Additional information

Communicated by H. Atomi.

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Supplementary Figure S1 Supplementary Figure S2 Supplementary Table S1 (DOCX 289 kb)

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Tirumalai, M.R., Fox, G.E. An ICEBs1-like element may be associated with the extreme radiation and desiccation resistance of Bacillus pumilus SAFR-032 spores. Extremophiles 17, 767–774 (2013). https://doi.org/10.1007/s00792-013-0559-z

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  • DOI: https://doi.org/10.1007/s00792-013-0559-z

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