High-quality genome sequence of the radioresistant bacterium Deinococcus ficus KS 0460

Matrosova, Vera Y.; Gaidamakova, Elena K.; Makarova, Kira S.; Grichenko, Olga; Klimenkova, Polina; Volpe, Robert P.; Tkavc, Rok; Ertem, Gözen; Conze, Isabel H.; Brambilla, Evelyne; Huntemann, Marcel; Clum, Alicia; Pillay, Manoj; Palaniappan, Krishnaveni; Varghese, Neha; Mikhailova, Natalia; Stamatis, Dimitrios; Reddy, TBK; Daum, Chris; Shapiro, Nicole; Ivanova, Natalia; Kyrpides, Nikos; Woyke, Tanja; Daligault, Hajnalka; Davenport, Karen; Erkkila, Tracy; Goodwin, Lynne A.; Gu, Wei; Munk, Christine; Teshima, Hazuki; Xu, Yan; Chain, Patrick; Woolbert, Michael; Gunde-Cimerman, Nina; Wolf, Yuri I.; Grebenc, Tine; Gostinčar, Cene; Daly, Michael J.

doi:10.1186/s40793-017-0258-y

Title: High-quality genome sequence of the radioresistant bacterium Deinococcus ficus KS 0460

Journal Article · 28 July 2017 · Standards in Genomic Sciences

DOI: https://doi.org/10.1186/s40793-017-0258-y · OSTI ID:1618976

Matrosova, Vera Y.; Gaidamakova, Elena K.; Makarova, Kira S.; Grichenko, Olga; Klimenkova, Polina; Volpe, Robert P.; Tkavc, Rok; Ertem, Gözen; Conze, Isabel H.; Brambilla, Evelyne; Huntemann, Marcel; Clum, Alicia; Pillay, Manoj; Palaniappan, Krishnaveni; Varghese, Neha; Mikhailova, Natalia; Stamatis, Dimitrios; Reddy, TBK; Daum, Chris; Shapiro, Nicole more »

Abstract The genetic platforms of Deinococcus species remain the only systems in which massive ionizing radiation (IR)-induced genome damage can be investigated in vivo at exposures commensurate with cellular survival. We report the whole genome sequence of the extremely IR-resistant rod-shaped bacterium Deinococcus ficus KS 0460 and its phenotypic characterization. Deinococcus ficus KS 0460 has been studied since 1987, first under the name Deinobacter grandis , then Deinococcus grandis . The D. ficus KS 0460 genome consists of a 4.019 Mbp sequence (69.7% GC content and 3894 predicted genes) divided into six genome partitions, five of which are confirmed to be circular. Circularity was determined manually by mate pair linkage. Approximately 76% of the predicted proteins contained identifiable Pfam domains and 72% were assigned to COGs. Of all D. ficus KS 0460 proteins, 79% and 70% had homologues in Deinococcus radiodurans ATCC BAA-816 and Deinococcus geothermalis DSM 11300, respectively. The most striking differences between D. ficus KS 0460 and D. radiodurans BAA-816 identified by the comparison of the KEGG pathways were as follows: (i) D. ficus lacks nine enzymes of purine degradation present in D. radiodurans , and (ii) D. ficus contains eight enzymes involved in nitrogen metabolism, including nitrate and nitrite reductases, that D. radiodurans lacks. Moreover, genes previously considered to be important to IR resistance are missing in D. ficus KS 0460, namely, for the Mn-transporter nramp , and proteins DdrF, DdrJ and DdrK, all of which are also missing in Deinococcus deserti . Otherwise, D. ficus KS 0460 exemplifies the Deinococcus lineage.

View Journal Article

Cite

Export

Save

Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: USDOE; USDOE Office of Science (SC)

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1618976

Alternate ID(s):: OSTI ID: 1627072

Journal Information:: Standards in Genomic Sciences, Journal Name: Standards in Genomic Sciences Vol. 12 Journal Issue: 1; ISSN 1944-3277

Publisher:: Springer Science + Business MediaCopyright Statement

Country of Publication:: United Kingdom

Language:: English

Citation Metrics:

Cited by: 11 works

Citation information provided by
Web of Science

References (57)

Regulation of MntH by a Dual Mn(II)- and Fe(II)-Dependent Transcriptional Repressor (DR2539) in Deinococcus radiodurans Sun, Hongxing; Li, Mingfeng; Xu, Guangzhi PLoS ONE, Vol. 7, Issue 4 https://doi.org/10.1371/journal.pone.0035057	journal	April 2012
Development and Validation of a Microplate-based .BETA.-carotene Bleaching Assay and Comparison of Antioxidant Activity (AOA) in Several Crops Measured by .BETA.-carotene Bleaching, DPPH and ORAC Assays Mikami, Ichiho; Yamaguchi, Minako; Shinmoto, Hiroshi Food Science and Technology Research, Vol. 15, Issue 2 https://doi.org/10.3136/fstr.15.171	journal	January 2009
Protein Oxidation Implicated as the Primary Determinant of Bacterial Radioresistance Daly, Michael J.; Gaidamakova, Elena K.; Matrosova, Vera Y. PLoS Biology, Vol. 5, Issue 4, Article No. e92 https://doi.org/10.1371/journal.pbio.0050092	journal	March 2007
Genome of the Extremely Radiation-Resistant Bacterium Deinococcus radiodurans Viewed from the Perspective of Comparative Genomics Makarova, K. S.; Aravind, L.; Wolf, Y. I. Microbiology and Molecular Biology Reviews, Vol. 65, Issue 1 https://doi.org/10.1128/MMBR.65.1.44-79.2001	journal	March 2001
Phylum BIV. “Deinococcus-Thermus” Garrity, George M.; Holt, John G.; Battista, John R. Bergey’s Manual® of Systematic Bacteriology https://doi.org/10.1007/978-0-387-21609-6_21	book	January 2001
Small-Molecule Antioxidant Proteome-Shields in Deinococcus radiodurans Daly, Michael J.; Gaidamakova, Elena K.; Matrosova, Vera Y. PLoS ONE, Vol. 5, Issue 9, Article No. e12570 https://doi.org/10.1371/journal.pone.0012570	journal	September 2010
The standard operating procedure of the DOE-JGI Microbial Genome Annotation Pipeline (MGAP v.4) Huntemann, Marcel; Ivanova, Natalia N.; Mavromatis, Konstantinos Standards in Genomic Sciences, Vol. 10, Issue 1 https://doi.org/10.1186/s40793-015-0077-y	journal	October 2015
Radiation response in D einococcus deserti : IrrE is a metalloprotease that cleaves repressor protein DdrO: Radiation response in Deinococcus deserti Ludanyi, Monika; Blanchard, Laurence; Dulermo, Rémi Molecular Microbiology, Vol. 94, Issue 2 https://doi.org/10.1111/mmi.12774	journal	September 2014
A new perspective on radiation resistance based on Deinococcus radiodurans Daly, Michael J. Nature Reviews Microbiology, Vol. 7, Issue 3 https://doi.org/10.1038/nrmicro2073	journal	January 2009
Manganese Complexes: Diverse Metabolic Routes to Oxidative Stress Resistance in Prokaryotes and Yeast Culotta, Valeria C.; Daly, Michael J. Antioxidants & Redox Signaling, Vol. 19, Issue 9 https://doi.org/10.1089/ars.2012.5093	journal	September 2013
Engineering Deinococcus radiodurans for metal remediation in radioactive mixed waste environments Brim, Hassan; McFarlan, Sara C.; Fredrickson, James K. Nature Biotechnology, Vol. 18, Issue 1 https://doi.org/10.1038/71986	journal	January 2000
Base-Calling of Automated Sequencer Traces Using Phred. I. Accuracy Assessment Ewing, Brent; Hillier, LaDeana; Wendl, Michael C. Genome Research, Vol. 8, Issue 3 https://doi.org/10.1101/gr.8.3.175	journal	March 1998
GET_HOMOLOGUES, a Versatile Software Package for Scalable and Robust Microbial Pangenome Analysis Contreras-Moreira, Bruno; Vinuesa, Pablo Applied and Environmental Microbiology, Vol. 79, Issue 24 https://doi.org/10.1128/AEM.02411-13	journal	October 2013
A Radiation-Resistant Rod-Shaped Bacterium, Deinobacter grandis gen. nov., sp. nov., with Peptidoglycan Containing Ornithine Oyaizu, H.; Stackebrandt, E.; Schleifer, K. H. International Journal of Systematic Bacteriology, Vol. 37, Issue 1 https://doi.org/10.1099/00207713-37-1-62	journal	January 1987
Phylogenetic Diversity of the Deinococci as Determined by 16S Ribosomal DNA Sequence Comparison Rainey, F. A.; Nobre, M. F.; Schumann, P. International Journal of Systematic Bacteriology, Vol. 47, Issue 2 https://doi.org/10.1099/00207713-47-2-510	journal	April 1997
SignalP 4.0: discriminating signal peptides from transmembrane regions Petersen, Thomas Nordahl; Brunak, Søren; von Heijne, Gunnar Nature Methods, Vol. 8, Issue 10 https://doi.org/10.1038/nmeth.1701	journal	September 2011
Solexa Ltd Bennett, Simon Pharmacogenomics, Vol. 5, Issue 4 https://doi.org/10.1517/14622416.5.4.433	journal	June 2004
BUSCO: assessing genome assembly and annotation completeness with single-copy orthologs Simão, Felipe A.; Waterhouse, Robert M.; Ioannidis, Panagiotis Bioinformatics, Vol. 31, Issue 19 https://doi.org/10.1093/bioinformatics/btv351	journal	June 2015
FastTree 2 – Approximately Maximum-Likelihood Trees for Large Alignments Price, Morgan N.; Dehal, Paramvir S.; Arkin, Adam P. PLoS ONE, Vol. 5, Issue 3 https://doi.org/10.1371/journal.pone.0009490	journal	March 2010
Gene Ontology: tool for the unification of biology Ashburner, Michael; Ball, Catherine A.; Blake, Judith A. Nature Genetics, Vol. 25, Issue 1 https://doi.org/10.1038/75556	journal	May 2000
BlastKOALA and GhostKOALA: KEGG Tools for Functional Characterization of Genome and Metagenome Sequences Kanehisa, Minoru; Sato, Yoko; Morishima, Kanae Journal of Molecular Biology, Vol. 428, Issue 4 https://doi.org/10.1016/j.jmb.2015.11.006	journal	February 2016
Towards a natural system of organisms: proposal for the domains Archaea, Bacteria, and Eucarya. Woese, C. R.; Kandler, O.; Wheelis, M. L. Proceedings of the National Academy of Sciences, Vol. 87, Issue 12 https://doi.org/10.1073/pnas.87.12.4576	journal	June 1990
Accumulation of Mn(II) in Deinococcus radiodurans Facilitates Gamma-Radiation Resistance Daly, M. J.; Gaidamakova, E. K.; Matrosova, V. Y. Science, Vol. 306, Issue 5698, p. 1025-1028 https://doi.org/10.1126/science.1103185	journal	November 2004
How radiation kills cells: Survival of and under oxidative stress Ghosal, D.; Omelchenko, M.; Gaidamakova, E. FEMS Microbiology Reviews, Vol. 29, Issue 2 https://doi.org/10.1016/j.femsre.2004.12.007	journal	April 2005
Prodigal: prokaryotic gene recognition and translation initiation site identification Hyatt, Doug; Chen, Gwo-Liang; LoCascio, Philip F. BMC Bioinformatics, Vol. 11, Issue 1 https://doi.org/10.1186/1471-2105-11-119	journal	March 2010
MDP: A Deinococcus Mn2+-Decapeptide Complex Protects Mice from Ionizing Radiation Gupta, Paridhi; Gayen, Manoshi; Smith, Joan T. PLOS ONE, Vol. 11, Issue 8 https://doi.org/10.1371/journal.pone.0160575	journal	August 2016
Deinococcus ficus sp. nov., isolated from the rhizosphere of Ficus religiosa L. Lai, Wei-An; Kämpfer, Peter; Arun, A. B. International Journal of Systematic and Evolutionary Microbiology, Vol. 56, Issue 4 https://doi.org/10.1099/ijs.0.64007-0	journal	April 2006
Microbial species delineation using whole genome sequences Varghese, Neha J.; Mukherjee, Supratim; Ivanova, Natalia Nucleic Acids Research, Vol. 43, Issue 14 https://doi.org/10.1093/nar/gkv657	journal	July 2015
Deinococcus geothermalis: The Pool of Extreme Radiation Resistance Genes Shrinks Makarova, Kira S.; Omelchenko, Marina V.; Gaidamakova, Elena K. PLoS ONE, Vol. 2, Issue 9 https://doi.org/10.1371/journal.pone.0000955	journal	September 2007
Velvet: Algorithms for de novo short read assembly using de Bruijn graphs Zerbino, D. R.; Birney, E. Genome Research, Vol. 18, Issue 5 https://doi.org/10.1101/gr.074492.107	journal	February 2008
Base-Calling of Automated Sequencer Traces Using Phred. II. Error Probabilities Ewing, Brent; Green, Phil Genome Research, Vol. 8, Issue 3 https://doi.org/10.1101/gr.8.3.186	journal	March 1998
Death by protein damage in irradiated cells Daly, Michael J. DNA Repair, Vol. 11, Issue 1, p. 12-21 https://doi.org/10.1016/j.dnarep.2011.10.024	journal	January 2012
Expanded microbial genome coverage and improved protein family annotation in the COG database Galperin, Michael Y.; Makarova, Kira S.; Wolf, Yuri I. Nucleic Acids Research, Vol. 43, Issue D1 https://doi.org/10.1093/nar/gku1223	journal	November 2014
ARB: a software environment for sequence data Ludwig, W. Nucleic Acids Research, Vol. 32, Issue 4 https://doi.org/10.1093/nar/gkh293	journal	February 2004
Comparative Genomics of Stress Response Systems in Deinococcus Bacteria Makarova, Kira S.; Daly, Michael J. Bacterial Stress Responses https://doi.org/10.1128/9781555816841.ch27	book	January 2011
Transcriptome dynamics of Deinococcus radiodurans recovering from ionizing radiation Liu, Y.; Zhou, J.; Omelchenko, M. V. Proceedings of the National Academy of Sciences, Vol. 100, Issue 7 https://doi.org/10.1073/pnas.0630387100	journal	March 2003
Consed: A Graphical Tool for Sequence Finishing Gordon, David; Abajian, Chris; Green, Phil Genome Research, Vol. 8, Issue 3 https://doi.org/10.1101/gr.8.3.195	journal	March 1998
Basic local alignment search tool Altschul, Stephen F.; Gish, Warren; Miller, Webb Journal of Molecular Biology, Vol. 215, Issue 3, p. 403-410 https://doi.org/10.1016/S0022-2836(05)80360-2	journal	October 1990
MUSCLE: a multiple sequence alignment method with reduced time and space complexity Edgar, Robert C. BMC Bioinformatics, Vol. 5, Issue 1, p. 113 https://doi.org/10.1186/1471-2105-5-113	journal	August 2004
The minimum information about a genome sequence (MIGS) specification Field, Dawn; Garrity, George; Gray, Tanya Nature Biotechnology, Vol. 26, Issue 5 https://doi.org/10.1038/nbt1360	journal	May 2008
Geomicrobiology of High-Level Nuclear Waste-Contaminated Vadose Sediments at the Hanford Site, Washington State Fredrickson, J. K.; Zachara, J. M.; Balkwill, D. L. Applied and Environmental Microbiology, Vol. 70, Issue 7 https://doi.org/10.1128/AEM.70.7.4230-4241.2004	journal	July 2004
Engineering radiation-resistant bacteria for environmental biotechnology Daly, Michael J. Current Opinion in Biotechnology, Vol. 11, Issue 3 https://doi.org/10.1016/S0958-1669(00)00096-3	journal	June 2000
Complete genome sequence of Truepera radiovictrix type strain (RQ-24T) Ivanova, Natalia; Rohde, Christine; Munk, Christine Standards in Genomic Sciences, Vol. 4, Issue 1 https://doi.org/10.4056/sigs.1563919	journal	February 2011
Preserving Immunogenicity of Lethally Irradiated Viral and Bacterial Vaccine Epitopes Using a Radio- Protective Mn²⁺-Peptide Complex from Deinococcus Gaidamakova, Elena K.; Myles, Ian A.; McDaniel, Dennis P. Cell Host & Microbe, Vol. 12, Issue 1, p. 117-124 https://doi.org/10.1016/j.chom.2012.05.011	journal	July 2012
DNA polymorphisms in new isolates of 'Deinococcus radiopugnans' Masters, C. I.; Murray, R. G. E.; Moseley, B. E. B. Journal of General Microbiology, Vol. 137, Issue 7 https://doi.org/10.1099/00221287-137-7-1459	journal	July 1991
Genome Sequence of the Radioresistant Bacterium Deinococcus radiodurans R1 White, O. Science, Vol. 286, Issue 5444 https://doi.org/10.1126/science.286.5444.1571	journal	November 1999
Nomenclature for "Micrococcus radiodurans" and Other Radiation-Resistant Cocci: Deinococcaceae fam. nov. and Deinococcus gen. nov., Including Five Species Brooks, B. W.; Murray, R. G. E. International Journal of Systematic Bacteriology, Vol. 31, Issue 3 https://doi.org/10.1099/00207713-31-3-353	journal	July 1981
FastTree: Computing Large Minimum Evolution Trees with Profiles instead of a Distance Matrix Price, M. N.; Dehal, P. S.; Arkin, A. P. Molecular Biology and Evolution, Vol. 26, Issue 7 https://doi.org/10.1093/molbev/msp077	journal	April 2009
PHAST: A Fast Phage Search Tool Zhou, Y.; Liang, Y.; Lynch, K. H. Nucleic Acids Research, Vol. 39, Issue suppl https://doi.org/10.1093/nar/gkr485	journal	June 2011
DdrO is an essential protein that regulates the radiation desiccation response and the apoptotic-like cell death in the radioresistant D einococcus radiodurans bacterium: DdrO-mediated regulation in Deinococcus radiodurans Devigne, Alice; Ithurbide, Solenne; Bouthier de la Tour, Claire Molecular Microbiology, Vol. 96, Issue 5 https://doi.org/10.1111/mmi.12991	journal	April 2015
IMG/M: integrated genome and metagenome comparative data analysis system Chen, I-Min A.; Markowitz, Victor M.; Chu, Ken Nucleic Acids Research, Vol. 45, Issue D1 https://doi.org/10.1093/nar/gkw929	journal	October 2016
A Simple, Fast, and Accurate Algorithm to Estimate Large Phylogenies by Maximum Likelihood Guindon, Stéphane; Gascuel, Olivier Systematic Biology, Vol. 52, Issue 5 https://doi.org/10.1080/10635150390235520	journal	October 2003
Oxidative Stress Resistance in Deinococcus radiodurans Slade, D.; Radman, M. Microbiology and Molecular Biology Reviews, Vol. 75, Issue 1 https://doi.org/10.1128/MMBR.00015-10	journal	March 2011
IMG ER: a system for microbial genome annotation expert review and curation Markowitz, Victor M.; Mavromatis, Konstantinos; Ivanova, Natalia N. Bioinformatics, Vol. 25, Issue 17 https://doi.org/10.1093/bioinformatics/btp393	journal	June 2009
GenePRIMP: a gene prediction improvement pipeline for prokaryotic genomes Pati, Amrita; Ivanova, Natalia N.; Mikhailova, Natalia Nature Methods, Vol. 7, Issue 6 https://doi.org/10.1038/nmeth.1457	journal	May 2010
The Deinococcus-Thermus Phylum and the Effect of rRNA Composition on Phylogenetic Tree Construction Weisburg, W. G.; Giovannoni, S. J.; Woese, C. R. Systematic and Applied Microbiology, Vol. 11, Issue 2 https://doi.org/10.1016/S0723-2020(89)80051-7	journal	March 1989
Deinococcus Mn 2+ -peptide complex: A novel approach to alphavirus vaccine development Gayen, Manoshi; Gupta, Paridhi; Morazzani, Elaine M. Vaccine, Vol. 35, Issue 29 https://doi.org/10.1016/j.vaccine.2017.05.016	journal	June 2017