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Long-read sequencing reveals increased occurrence of genomic variants and adenosine methylation in Bacillus pumilus SAFR-032 after long-duration flight exposure onboard the International Space Station

Published online by Cambridge University Press:  16 November 2021

Samantha M. Waters Open the ORCID record for Samantha M. Waters [Opens in a new window] ,
S. Marshall Ledford ,
Amanda Wacker ,
Sonali Verma ,
Bianca Serda ,
Jordan McKaig Open the ORCID record for Jordan McKaig [Opens in a new window] ,
Joseph Varelas ,
Patrick M. Nicoll ,
Kasthuri Venkateswaran  and
David J. Smith
Samantha M. Waters*
Affiliation:
Universities Space Research Association, Columbia, CA, USA NASA Ames Research Center, Space Biosciences Research Division, Moffett Field, CA, USA
S. Marshall Ledford
Affiliation:
Vassar College, Poughkeepsie, NY, USA
Amanda Wacker
Affiliation:
University of California San Diego, La Jolla, CA, USA
Sonali Verma
Affiliation:
NASA Ames Research Center, Space Biosciences Research Division, Moffett Field, CA, USA
Bianca Serda
Affiliation:
Department of Biology, University of New Mexico, Albuquerque, NM, USA Current: Department of Biochemistry and Molecular Biology, MSU-DOE Plant Research Laboratory Michigan State University, East Lansing, MI, USA
Jordan McKaig
Affiliation:
Department of Earth and Atmospheric Sciences, Georgia Institute of Technology, Atlanta, GA, USA
Joseph Varelas
Affiliation:
Universities Space Research Association, Columbia, CA, USA
Patrick M. Nicoll
Affiliation:
NASA Ames Research Center, Space Biosciences Research Division, Moffett Field, CA, USA Blue Marble Space Institute of Science, Moffett Field, CA, USA Current: Department of Psychology, University of Victoria, Victoria, BC, Canada
Kasthuri Venkateswaran
Affiliation:
Biotechnology and Planetary Protection Group, NASA Jet Propulsion Laboratories, California Institute of Technology, Pasadena, CA, USA
David J. Smith
Affiliation:
NASA Ames Research Center, Space Biosciences Research Division, Moffett Field, CA, USA
*
Author for correspondence: Samantha M. Waters, E-mail: Samantha.m.waters@gmail.com
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Abstract

Bacillus pumilus SAFR-032, an endospore-forming bacterial strain, was investigated to determine its methylation pattern (methylome) change, compared to ground control, after direct exposure to space conditions onboard the International Space Station (ISS) for 1.5 years. The resulting ISS-flown and non-flown strains were sequenced using the Nanopore MinION and an in-house method and pipeline to identify methylated positions in the genome. Our analysis indicated genomic variants and m6A methylation increased in the ISS-flown SAFR-032. To complement the broader omics investigation and explore phenotypic changes, ISS-flown and non-flown strains were compared in a series of laboratory-based chamber experiments using an X-ray irradiation source (doses applied at 250, 500, 750, 1000 and 1250 Gy); results show a potentially higher survival fraction of ISS-flown DS2 at the two highest exposures. Taken together, results from this study document lasting changes to the genome by methylation, potentially triggered by conditions in spaceflight, with functional consequences for the resistance of bacteria to stressors expected on long-duration missions beyond low Earth orbit.

Keywords

Bacillusionizing radiationISSmethylationsequencing
Type
Research Article
Information
International Journal of Astrobiology , Volume 20 , Issue 6 , December 2021 , pp. 435 - 444
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Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press

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References

Allen, CC, Morris, RV, Jager, KM, Golden, D, Lindstrom, DJ, Lindstrom, MM and Lockwood, JP (1998) Martian regolith simulant JSC Mars-1. Presented at the Lunar and planetary science conference, p. 1690.Google Scholar
Barrick, JE, Yu, DS, Yoon, SH, Jeong, H, Oh, TK, Schneider, D, Lenski, RE and Kim, JF (2009) Genome evolution and adaptation in a long-term experiment with Escherichia coli. Nature 461, 1243–1247.CrossRefGoogle Scholar
Beaulaurier, J, Zhang, X-S, Zhu, S, Sebra, R, Rosenbluh, C, Deikus, G, Shen, N, Munera, D, Waldor, MK, Chess, A, Blaser, MJ, Schadt, EE and Fang, G (2015) Single molecule-level detection and long read-based phasing of epigenetic variations in bacterial methylomes. Nature Communications 6, 7438.CrossRefGoogle ScholarPubMed
Behe, MJ (2010) Experimental evolution, loss-of-function mutations, and “the first rule of adaptive evolution”. The Quarterly Review of Biology 85, 419–445.CrossRefGoogle Scholar
Blaby, IK, Lyons, BJ, Wroclawska-Hughes, E, Phillips, GC, Pyle, TP, Chamberlin, SG, Benner, SA, Lyons, TJ, de Crécy-Lagard, V and de Crécy, E (2012) Experimental evolution of a facultative thermophile from a mesophilic ancestor. Applied and Environmental Microbiology 78, 144–155.CrossRefGoogle ScholarPubMed
Blank, D, Wolf, L, Ackermann, M and Silander, OK (2014) The predictability of molecular evolution during functional innovation. Proceedings of the National Academy of Sciences of the USA 111, 3044–3049.CrossRefGoogle ScholarPubMed
Blow, MJ, Clark, TA, Daum, CG, Deutschbauer, AM, Fomenkov, A, Fries, R, Froula, J, Kang, DD, Malmstrom, RR and Morgan, RD (2016) The epigenomic landscape of prokaryotes. PLoS Genetics 12, e1005854.CrossRefGoogle ScholarPubMed
Blyn, LB, Braaten, BA and Low, DA (1990) Regulation of pap pilin phase variation by a mechanism involving differential dam methylation states. The EMBO Journal 9, 4045–4054.CrossRefGoogle ScholarPubMed
Brendel, M, Khan, N and Haynes, R (1970) Common steps in the repair of alkylation and radiation damage in yeast. Molecular and General Genetics MGG 106, 289–295.CrossRefGoogle ScholarPubMed
Brown, BL, Watson, M, Minot, SS, Rivera, MC and Franklin, RB (2017) MinIONTM nanopore sequencing of environmental metagenomes: a synthetic approach. Gigascience 6, gix007.CrossRefGoogle Scholar
Brüssow, H, Canchaya, C and Hardt, W-D (2004) Phages and the evolution of bacterial pathogens: from genomic rearrangements to lysogenic conversion. Microbiology and Molecular Biology Reviews 68, 560–602.CrossRefGoogle ScholarPubMed
Bueno, A, Villanueva, JR and Villa, TG (1986) Methylation of spore DNA in Bacillus coagulans strain 26. Microbiology 132, 2899–2905.CrossRefGoogle ScholarPubMed
Burton, AS, Stahl, SE, John, KK, Jain, M, Juul, S, Turner, DJ, Harrington, ED, Stoddart, D, Paten, B and Akeson, M (2020) Off earth identification of bacterial populations using 16S rDNA nanopore sequencing. Genes 11, 76.CrossRefGoogle ScholarPubMed
Casadesús, J and Low, D (2006) Epigenetic gene regulation in the bacterial world. Microbiology and Molecular Biology Reviews 70, 830–856.CrossRefGoogle ScholarPubMed
Chancellor, JC, Scott, GB and Sutton, JP (2014) Space radiation: the number one risk to astronaut health beyond low earth orbit. Life 4, 491–510.CrossRefGoogle ScholarPubMed
Chhotaray, C, Wang, S, Tan, Y, Ali, A, Shehroz, M, Fang, C, Liu, Y, Lu, Z, Cai, X and Hameed, HA (2020) Comparative analysis of whole-genome and methylome profiles of a smooth and a rough Mycobacterium abscessus clinical strain. G3: Genes, Genomes, Genetics 10, 13–22.CrossRefGoogle Scholar
Chi, H-C, Tsai, C-Y, Tsai, M-M and Lin, K-H (2018) Impact of DNA and RNA methylation on radiobiology and cancer progression. International Journal of Molecular Sciences 19, 555.CrossRefGoogle ScholarPubMed
Chiang, AJ, Mohan, GBM, Singh, NK, Vaishampayan, PA, Kalkum, M and Venkateswaran, K (2019) Alteration of proteomes in first-generation cultures of Bacillus pumilus spores exposed to outer space. Msystems 4.CrossRefGoogle ScholarPubMed
Cohen, NR, Ross, CA, Jain, S, Shapiro, RS, Gutierrez, A, Belenky, P, Li, H and Collins, JJ (2016) A role for the bacterial GATC methylome in antibiotic stress survival. Nature Genetics 48, 581–586.CrossRefGoogle ScholarPubMed
Couturier, M and Lindås, A-C (2018) The DNA methylome of the hyperthermoacidophilic crenarchaeon Sulfolobus acidocaldarius. Frontiers in Microbiology 9, 137.CrossRefGoogle ScholarPubMed
Coy, SR, Gann, ER, Papoulis, SE, Holder, ME, Ajami, NJ, Petrosino, JF, Zinser, ER, Van Etten, JL and Wilhelm, SW (2020) SMRT Sequencing of Paramecium bursaria chlorella virus-1 reveals diverse methylation stability in adenines targeted by restriction-modification systems. Frontiers in Microbiology 11, 887.CrossRefGoogle ScholarPubMed
Deshpande, SV, Reed, TM, Sullivan, RF, Kerkhof, LJ, Beigel, KM and Wade, MM (2019) Offline next-generation metagenomics sequence analysis using MinION detection software (MINDS). Genes 10, 578.CrossRefGoogle Scholar
Dilthey, AT, Jain, C, Koren, S and Phillippy, AM (2019) Strain-level metagenomic assignment and compositional estimation for long reads with MetaMaps. Nature Communications 10, 1–12.CrossRefGoogle ScholarPubMed
Dingman, DW (1990) Presence of N6-methyladenine in GATC sequences of Bacillus popilliae and Bacillus lentimorbus KLN2. Journal of Bacteriology 172, 6156.CrossRefGoogle ScholarPubMed
Estibariz, I, Ailloud, F, Woltemate, S, Bunk, B, Spröer, C, Overmann, J, Aebischer, T, Meyer, TF, Josenhans, C and Suerbaum, S (2020) In vivo genome and methylome adaptation of cag-negative Helicobacter pylori during experimental human infection. Mbio 11.CrossRefGoogle ScholarPubMed
Fang, G, Munera, D, Friedman, DI, Mandlik, A, Chao, MC, Banerjee, O, Feng, Z, Losic, B, Mahajan, MC and Jabado, OJ (2012) Genome-wide mapping of methylated adenine residues in pathogenic Escherichia coli using single-molecule real-time sequencing. Nature Biotechnology 30, 1232–1239.CrossRefGoogle ScholarPubMed
Flusberg, BA, Webster, DR, Lee, JH, Travers, KJ, Olivares, EC, Clark, TA, Korlach, J and Turner, SW (2010) Direct detection of DNA methylation during single-molecule, real-time sequencing. Nature Methods 7, 461–465.CrossRefGoogle ScholarPubMed
Forde, BM, McAllister, LJ, Paton, JC, Paton, AW and Beatson, SA (2019) SMRT Sequencing reveals differential patterns of methylation in two O111: H-STEC isolates from a hemolytic uremic syndrome outbreak in Australia. Scientific Reports 9, 1–11.CrossRefGoogle ScholarPubMed
Foster, PL (2005) Stress responses and genetic variation in bacteria. Mutation Research/Fundamental and Molecular Mechanisms of Mutagenesis 569, 3–11.CrossRefGoogle Scholar
Gießelmann, P, Brändl, B, Raimondeau, E, Bowen, R, Rohrandt, C, Tandon, R, Kretzmer, H, Assum, G, Galonska, C, Siebert, R, Ammerpohl, O, Heron, A, Schneider, SA, Ladewig, J, Koch, P, Schuldt, BM, Graham, JE, Meissner, A and Müller, F-J (2018) Repeat expansion and methylation state analysis with nanopore sequencing. bioRxiv, 480285. https://doi.org/10.1101/480285.Google Scholar
Giesselmann, P, Brändl, B, Raimondeau, E, Bowen, R, Rohrandt, C, Tandon, R, Kretzmer, H, Assum, G, Galonska, C and Siebert, R (2019) Analysis of short tandem repeat expansions and their methylation state with nanopore sequencing. Nature Biotechnology 37, 1478–1481.CrossRefGoogle ScholarPubMed
Gigante, S, Gouil, Q, Lucattini, A, Keniry, A, Beck, T, Tinning, M, Gordon, L, Woodruff, C, Speed, TP, Blewitt, ME and Ritchie, ME (2019) Using long-read sequencing to detect imprinted DNA methylation. Nucleic Acids Research 47, e46–e46. https://doi.org/10.1093/nar/gkz107.CrossRefGoogle ScholarPubMed
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 and Weinstock, GM (2007) Paradoxical DNA repair and peroxide resistance gene conservation in Bacillus pumilus SAFR-032. PLoS One 2, e928.CrossRefGoogle ScholarPubMed
Gupta, PK (2008) Single-molecule DNA sequencing technologies for future genomics research. Trends in Biotechnology 26, 602–611.CrossRefGoogle ScholarPubMed
Hagemann, M, Gärtner, K, Scharnagl, M, Bolay, P, Lott, SC, Fuss, J, Huettel, B, Reinhardt, R, Klähn, S and Hess, WR (2018) Identification of the DNA methyltransferases establishing the methylome of the cyanobacterium Synechocystis sp. PCC 6803. DNA Research 25, 343–352.CrossRefGoogle ScholarPubMed
Hattman, S, Keister, T and Gottehrer, A (1978) Sequence specificity of DNA methylases from Bacillus amyloliquefaciens and Bacillus brevis. Journal of Molecular Biology 124, 701–711.CrossRefGoogle ScholarPubMed
Holliday, R and Grigg, G (1993) DNA methylation and mutation. Mutation Research/Fundamental and Molecular Mechanisms of Mutagenesis 285, 61–67.CrossRefGoogle ScholarPubMed
Holliday, R and Pugh, JE (1975) DNA Modification mechanisms and gene activity during development. Science 187, 226–232.CrossRefGoogle ScholarPubMed
Horneck, G, Rettberg, P, Reitz, G, Wehner, J, Eschweiler, U, Strauch, K, Panitz, C, Starke, V and Baumstark-Khan, C (2001) Protection of bacterial spores in space, a contribution to the discussion on panspermia. Origins of Life and Evolution of the Biosphere 31, 527–547.CrossRefGoogle Scholar
Horneck, G, Klaus, DM and Mancinelli, RL (2010) Space microbiology. Microbiology and Molecular Biology Reviews 74, 121–156.CrossRefGoogle ScholarPubMed
Horneck, G, Moeller, R, Cadet, J, Douki, T, Mancinelli, RL, Nicholson, WL, Panitz, C, Rabbow, E, Rettberg, P and Spry, A (2012) Resistance of bacterial endospores to outer space for planetary protection purposes—experiment PROTECT of the EXPOSE-E mission. Astrobiology 12, 445–456.CrossRefGoogle ScholarPubMed
Jain, M, Koren, S, Miga, KH, Quick, J, Rand, AC, Sasani, TA, Tyson, JR, Beggs, AD, Dilthey, AT, Fiddes, IT, Malla, S, Marriott, H, Nieto, T, O'Grady, J, Olsen, HE, Pedersen, BS, Rhie, A, Richardson, H, Quinlan, AR, Snutch, TP, Tee, L, Paten, B, Phillippy, AM, Simpson, JT, Loman, NJ and Loose, M (2018) Nanopore sequencing and assembly of a human genome with ultra-long reads. Nature Biotechnology 36, 338–345.CrossRefGoogle ScholarPubMed
Khodadad, CL, Wong, GM, James, LM, Thakrar, PJ, Lane, MA, Catechis, JA and Smith, DJ (2017) Stratosphere conditions inactivate bacterial endospores from a Mars spacecraft assembly facility. Astrobiology 17, 337–350.CrossRefGoogle ScholarPubMed
Krebes, J, Morgan, RD, Bunk, B, Spröer, C, Luong, K, Parusel, R, Anton, BP, König, C, Josenhans, C and Overmann, J (2014) The complex methylome of the human gastric pathogen Helicobacter pylori. Nucleic Acids Research 42, 2415–2432.CrossRefGoogle ScholarPubMed
Lanfear, R, Schalamun, M, Kainer, D, Wang, W and Schwessinger, B (2019) MinIONQC: fast and simple quality control for MinION sequencing data. Bioinformatics 35, 523–525.CrossRefGoogle ScholarPubMed
Lee, H, Gurtowski, J, Yoo, S, Nattestad, M, Marcus, S, Goodwin, S, McCombie, WR and Schatz, MC (2016) Third-generation sequencing and the future of genomics. BioRxiv, 048603.Google Scholar
Leidenfrost, RM, Pöther, D-C, Jäckel, U and Wünschiers, R (2020) Benchmarking the minion: evaluating long reads for microbial profiling. Scientific Reports 10, 1–10.CrossRefGoogle ScholarPubMed
Lenhart, JS, Schroeder, JW, Walsh, BW and Simmons, LA (2012) DNA Repair and genome maintenance in Bacillus subtilis. Microbiology and Molecular Biology Reviews 76, 530–564.CrossRefGoogle ScholarPubMed
Li, S and Tollefsbol, TO (2020) DNA Methylation methods: global DNA methylation and methylomic analyses. Methods 187, 28–43.CrossRefGoogle ScholarPubMed
Li, H, Handsaker, B, Wysoker, A, Fennell, T, Ruan, J, Homer, N, Marth, G, Abecasis, G and Durbin, R (2009) The sequence alignment/map format and SAMtools. Bioinformatics 25, 2078–2079.CrossRefGoogle ScholarPubMed
Link, L, Sawyer, J, Venkateswaran, K and Nicholson, W (2004) Extreme spore UV resistance of Bacillus pumilus isolates obtained from an ultraclean spacecraft assembly facility. Microbial Ecology 47, 159–163.CrossRefGoogle ScholarPubMed
Lister, R, Pelizzola, M, Dowen, RH, Hawkins, RD, Hon, G, Tonti-Filippini, J, Nery, JR, Lee, L, Ye, Z and Ngo, Q-M (2009) Human DNA methylomes at base resolution show widespread epigenomic differences. Nature 462, 315–322.CrossRefGoogle ScholarPubMed
Liu, H, Begik, O, Lucas, MC, Ramirez, JM, Mason, CE, Wiener, D, Schwartz, S, Mattick, JS, Smith, MA and Novoa, EM (2019a) Accurate detection of m 6 A RNA modifications in native RNA sequences. Nature Communications 10, 1–9.Google Scholar
Liu, L, Zhang, Y, Jiang, D, Du, S, Deng, Z, Wang, L and Chen, S (2019b) Recent advances in the genomic profiling of bacterial epigenetic modifications. Biotechnology Journal 14, 1800001.CrossRefGoogle Scholar
Liu, G, Jiang, Y-M, Liu, Y-C, Han, L-L and Feng, H (2020) A novel DNA methylation motif identified in Bacillus pumilus BA06 and possible roles in the regulation of gene expression. Applied Microbiology and Biotechnology 104, 3445–3457.CrossRefGoogle ScholarPubMed
Lluch-Senar, M, Luong, K, Lloréns-Rico, V, Delgado, J, Fang, G, Spittle, K, Clark, TA, Schadt, E, Turner, SW, Korlach, J and Serrano, L (2013) Comprehensive methylome characterization of Mycoplasma genitalium and Mycoplasma pneumoniae at single-base resolution. PLoS Genetics 9, e1003191–e1003191.CrossRefGoogle ScholarPubMed
Loman, NJ, Quick, J and Simpson, JT (2015) A complete bacterial genome assembled de novo using only nanopore sequencing data. Nature Methods 12, 733–735.CrossRefGoogle ScholarPubMed
Löser, DA, Shibata, A, Shibata, AK, Woodbine, LJ, Jeggo, PA and Chalmers, AJ (2010) Sensitization to radiation and alkylating agents by inhibitors of poly(ADP-ribose) polymerase is enhanced in cells deficient in DNA double-strand break repair. Molecular Cancer Therapeutics 9, 1775.CrossRefGoogle ScholarPubMed
Low, M, Read, EL and Borek, E (1976) Methylation of DNA in HeLa cells after ultraviolet irradiation. International Journal of Radiation Oncology*Biology*Physics 1, 289–294.CrossRefGoogle ScholarPubMed
Maddamsetti, R, Hatcher, PJ, Green, AG, Williams, BL, Marks, DS and Lenski, RE (2017) Core genes evolve rapidly in the long-term evolution experiment with Escherichia coli. Genome Biology and Evolution 9, 1072–1083.CrossRefGoogle ScholarPubMed
Maurer, RH, Fraeman, ME, Martin, MN and Roth, DR (2008) Harsh environments: space radiation. Johns Hopkins APL Technical Digest 28, 17.Google Scholar
McIntyre, AB, Alexander, N, Grigorev, K, Bezdan, D, Sichtig, H, Chiu, CY and Mason, CE (2019) Single-molecule sequencing detection of N 6-methyladenine in microbial reference materials. Nature Communications 10, 1–11.CrossRefGoogle Scholar
Miga, KH, Koren, S, Rhie, A, Vollger, MR, Gershman, A, Bzikadze, A, Brooks, S, Howe, E, Porubsky, D and Logsdon, GA (2019) Telomere-to-telomere assembly of a complete human X chromosome. BioRxiv, 735928.Google Scholar
Miousse, IR, Kutanzi, KR and Koturbash, I (2017) Effects of ionizing radiation on DNA methylation: from experimental biology to clinical applications. Null 93, 457–469.Google ScholarPubMed
Moeller, R, Rohde, M and Reitz, G (2010) Effects of ionizing radiation on the survival of bacterial spores in artificial Martian regolith. Icarus 206, 783–786.CrossRefGoogle Scholar
Nicholson, WL (2009) Ancient micronauts: interplanetary transport of microbes by cosmic impacts. Trends in Microbiology 17, 243–250.CrossRefGoogle ScholarPubMed
Nicholson, WL, Schuerger, AC and Race, MS (2009) Migrating microbes and planetary protection. Trends in Microbiology 17, 389–392.CrossRefGoogle ScholarPubMed
Nicholson, TL, Brunelle, BW, Bayles, DO, Alt, DP and Shore, SM (2018) Comparative genomic and methylome analysis of non-virulent D74 and virulent Nagasaki Haemophilus parasuis isolates. PLoS One 13, e0205700.CrossRefGoogle ScholarPubMed
Nye, TM, Jacob, KM, Holley, EK, Nevarez, JM, Dawid, S, Simmons, LA and Watson, ME Jr (2019) DNA Methylation from a type I restriction-modification system influences gene expression and virulence in Streptococcus pyogenes. PLoS Pathogens 15, e1007841.CrossRefGoogle ScholarPubMed
Nye, TM, van Gijtenbeek, LA, Stevens, AG, Schroeder, JW, Randall, JR, Matthews, LA and Simmons, LA (2020) Methyltransferase DnmA is responsible for genome-wide N6-methyladenosine modifications at non-palindromic recognition sites in Bacillus subtilis. Nucleic Acids Research 48, 5332–5348.CrossRefGoogle ScholarPubMed
Osman, S, Peeters, Z, La Duc, MT, Mancinelli, R, Ehrenfreund, P and Venkateswaran, K (2008) Effect of shadowing on survival of bacteria under conditions simulating the Martian atmosphere and UV radiation. Applied and Environmental Microbiology 74, 959–970.CrossRefGoogle ScholarPubMed
Payelleville, A, Legrand, L, Ogier, J-C, Roques, C, Roulet, A, Bouchez, O, Mouammine, A, Givaudan, A and Brillard, J (2018) The complete methylome of an entomopathogenic bacterium reveals the existence of loci with unmethylated adenines. Scientific Reports 8, 12091.CrossRefGoogle ScholarPubMed
Poole, A, Penny, D and Sjöberg, B-M (2001) Confounded cytosine! tinkering and the evolution of DNA. Nature Reviews Molecular Cell Biology 2, 147–151.CrossRefGoogle ScholarPubMed
Rand, AC, Jain, M, Eizenga, JM, Musselman-Brown, A, Olsen, HE, Akeson, M and Paten, B (2017) Mapping DNA methylation with high-throughput nanopore sequencing. Nature Methods 14, 411–413.CrossRefGoogle ScholarPubMed
Ray, S, Gebre, S, Fogle, H, Berrios, DC, Tran, PB, Galazka, JM and Costes, SV (2019) GeneLab: omics database for spaceflight experiments. Bioinformatics 35, 1753–1759.CrossRefGoogle ScholarPubMed
Reik, W (2007) Stability and flexibility of epigenetic gene regulation in mammalian development. Nature 447, 425–432.CrossRefGoogle ScholarPubMed
Reva, ON, Swanevelder, DZ, Mwita, LA, Mwakilili, AD, Muzondiwa, D, Joubert, M, Chan, WY, Lutz, S, Ahrens, CH and Avdeeva, LV (2019) Genetic, epigenetic and phenotypic diversity of four Bacillus velezensis strains used for plant protection or as probiotics. Frontiers in Microbiology 10, 2610.CrossRefGoogle ScholarPubMed
Reva, ON, Larisa, SA, Mwakilili, AD, Tibuhwa, D, Lyantagaye, S, Chan, WY, Lutz, S, Ahrens, CH, Vater, J and Borriss, R (2020) Complete genome sequence and epigenetic profile of Bacillus velezensis UCMB5140 used for plant and crop protection in comparison with other plant-associated Bacillus strains. Applied Microbiology and Biotechnology 104, 7643–7656.CrossRefGoogle ScholarPubMed
Ritchie, MD, Holzinger, ER, Li, R, Pendergrass, SA and Kim, D (2015) Methods of integrating data to uncover genotype–phenotype interactions. Nature Reviews Genetics 16, 85–97.CrossRefGoogle ScholarPubMed
Sanderson, ND, Street, TL, Foster, D, Swann, J, Atkins, BL, Brent, AJ, McNally, MA, Oakley, S, Taylor, A and Peto, TE (2018) Real-time analysis of nanopore-based metagenomic sequencing from infected orthopaedic devices. BMC Genomics 19, 714.CrossRefGoogle ScholarPubMed
Schaeffer, P, Millet, J and Aubert, J-P (1965) Catabolic repression of bacterial sporulation. Proceedings of the National Academy of Sciences 54, 704–711.CrossRefGoogle ScholarPubMed
Schuerger, AC and Nicholson, WL (2006) Interactive effects of hypobaria, low temperature, and CO2 atmospheres inhibit the growth of mesophilic Bacillus spp. Under simulated Martian conditions. Icarus 185, 143–152.CrossRefGoogle Scholar
Schuerger, AC, Mancinelli, RL, Kern, RG, Rothschild, LJ and McKay, CP (2003) Survival of endospores of Bacillus subtilis on spacecraft surfaces under simulated Martian environments:: implications for the forward contamination of Mars. Icarus 165, 253–276.CrossRefGoogle ScholarPubMed
Selker, EU and Stevens, JN (1985) DNA methylation at asymmetric sites is associated with numerous transition mutations. Proceedings of the National Academy of Sciences 82, 8114–8118.CrossRefGoogle ScholarPubMed
Shaiwale, NS, Basu, B, Deobagkar, DD, Deobagkar, DN and Apte, SK (2015) DNA adenine hypomethylation leads to metabolic rewiring in Deinococcus radiodurans. Journal of Proteomics 126, 131–139.CrossRefGoogle ScholarPubMed
Simonsen, LC, Nealy, JE, Townsend, LW and Wilson, JW (1990) Radiation Exposure for Manned Mars Surface Missions.Google Scholar
Simpson, JT, Workman, RE, Zuzarte, P, David, M, Dursi, L and Timp, W (2017) Detecting DNA cytosine methylation using nanopore sequencing. Nature Methods 14, 407–410.CrossRefGoogle ScholarPubMed
Sović, I, Šikić, M, Wilm, A, Fenlon, SN, Chen, S and Nagarajan, N (2016) Fast and sensitive mapping of nanopore sequencing reads with GraphMap. Nature Communications 7, 11307.CrossRefGoogle ScholarPubMed
Szopa-Comley, A (2013) DNA Sequencing: Latest Developments In Next-Generation Sequencing.Google Scholar
Tenaillon, O, Denamur, E and Matic, I (2004) Evolutionary significance of stress-induced mutagenesis in bacteria. Trends in Microbiology 12, 264–270.CrossRefGoogle Scholar
Tirumalai, MR, Rastogi, R, Zamani, N, Williams, EO, Allen, S, Diouf, F, Kwende, S, Weinstock, GM, Venkateswaran, KJ and Fox, GE (2013) Candidate genes that may be responsible for the unusual resistances exhibited by Bacillus pumilus SAFR-032 spores. PLoS One 8, e66012.CrossRefGoogle ScholarPubMed
Townsend, LW (2005) Implications of the space radiation environment for human exploration in deep space. Radiation Protection Dosimetry 115, 44–50.CrossRefGoogle ScholarPubMed
Ullmann, R, Becker, BV, Rothmiller, S, Schmidt, A, Thiermann, H, Kaatsch, HL, Schrock, G, Müller, J, Jakobi, J, Obermair, R, Port, M and Scherthan, H (2021) Genomic adaption and mutational patterns in a HaCaT subline resistant to alkylating agents and ionizing radiation. International Journal of Molecular Sciences 22. https://doi.org/10.3390/ijms22031146.CrossRefGoogle Scholar
Vaishampayan, PA, Rabbow, E, Horneck, G and Venkateswaran, KJ (2012) Survival of Bacillus pumilus spores for a prolonged period of time in real space conditions. Astrobiology 12, 487–497.CrossRefGoogle ScholarPubMed
Venkateswaran, K, Satomi, M, Chung, S, Kern, R, Koukol, R, Basic, C and White, D (2001) Molecular microbial diversity of a spacecraft assembly facility. Systematic and Applied Microbiology 24, 311–320.CrossRefGoogle ScholarPubMed
Walsh, C and Xu, G (2006) Cytosine methylation and DNA repair. DNA Methylation: Basic Mechanisms, 283–315.Google ScholarPubMed
Waters, SM, Zeigler, DR and Nicholson, WL (2015) Experimental evolution of enhanced growth by Bacillus subtilis at low atmospheric pressure: genomic changes revealed by whole-genome sequencing. Applied and Environmental Microbiology 81, 7525–7532.CrossRefGoogle ScholarPubMed
Weirather, JL, de Cesare, M, Wang, Y, Piazza, P, Sebastiano, V, Wang, X-J, Buck, D and Au, KF (2017) Comprehensive comparison of Pacific Biosciences and Oxford Nanopore Technologies and their applications to transcriptome analysis. F1000Research 6.CrossRefGoogle ScholarPubMed
Westphal, LL, Sauvey, P, Champion, MM, Ehrenreich, IM and Finkel, SE (2016) Genomewide dam methylation in Escherichia coli during long-term stationary phase. MSystems 1.CrossRefGoogle ScholarPubMed
Whitfield, BL and Billen, D (1972) In vivo methylation of Escherichia coli DNA following ultraviolet and X-irradiation. Journal of Molecular Biology 63, 363–372.CrossRefGoogle ScholarPubMed
Zautner, AE, Goldschmidt, A-M, Thürmer, A, Schuldes, J, Bader, O, Lugert, R, Groß, U, Stingl, K, Salinas, G and Lingner, T (2015) SMRT sequencing of the Campylobacter coli BfR-CA-9557 genome sequence reveals unique methylation motifs. BMC Genomics 16, 1–12.CrossRefGoogle ScholarPubMed
Zhang, Z, Wang, H, Wang, Y, Xi, F, Wang, H, Kohnen, MV, Gao, P, Wei, W, Chen, K and Liu, X (2021) Whole-genome characterization of chronological age-associated changes in methylome and circular RNAs in moso bamboo (Phyllostachys edulis) from vegetative to floral growth. The Plant Journal 106, 435–453.CrossRefGoogle ScholarPubMed
Zhao, L, Song, Y, Li, L, Gan, N, Brand, JJ and Song, L (2018) The highly heterogeneous methylated genomes and diverse restriction-modification systems of bloom-forming Microcystis. Harmful Algae 75, 87–93.CrossRefGoogle ScholarPubMed
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