Survival in Nuclear Waste, Extreme Resistance, and Potential Applications Gleaned from the Genome Sequence of Kineococcus radiotolerans SRS30216

Bagwell, Christopher E.; Bhat, Swapna; Hawkins, Gary M.; Smith, Bryan W.; Biswas, Tapan; Hoover, Timothy R.; Saunders, Elizabeth; Han, Cliff; Tsodikov, Oleg V.; Shimkets, Lawrence J.

doi:10.1371/journal.pone.0003878

Cited by 63 publications

(46 citation statements)

References 60 publications

(72 reference statements)

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“…Further studies are needed to elucidate the roles of the 7-deazaguanine derivatives in bacterial and phage DNA, with potential functions varying among R-M systems, antirestriction systems, epigenetic marks, and unforeseen protective roles, as these modifications were found in organisms like K. radiotolerans that can resist radiation stress (48). We foresee that the molecular characterization of the enzymes involved in the synthesis, recognition, and cleavage of 7-deazaguanine derivatives in DNA could open the door to both biotechnological and antibacterial applications.…”

Section: 46)mentioning

confidence: 99%

Novel genomic island modifies DNA with 7-deazaguanine derivatives

Thiaville

Kellner

Yuan

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

155

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The discovery of ∼20-kb gene clusters containing a family of paralogs of tRNA guanosine transglycosylase genes, called tgtA5, alongside 7-cyano-7-deazaguanine (preQ 0 ) synthesis and DNA metabolism genes, led to the hypothesis that 7-deazaguanine derivatives are inserted in DNA. This was established by detecting 2'-deoxy-preQ 0 and 2'-deoxy-7-amido-7-deazaguanosine in enzymatic hydrolysates of DNA extracted from the pathogenic, Gram-negative bacteria Salmonella enterica serovar Montevideo. These modifications were absent in the closely related S. enterica serovar Typhimurium LT2 and from a mutant of S. Montevideo, each lacking the gene cluster. This led us to rename the genes of the S. Montevideo cluster as dpdA-K for 7-deazapurine in DNA. Similar gene clusters were analyzed in ∼150 phylogenetically diverse bacteria, and the modifications were detected in DNA from other organisms containing these clusters, including Kineococcus radiotolerans, Comamonas testosteroni, and Sphingopyxis alaskensis. Comparative genomic analysis shows that, in Enterobacteriaceae, the cluster is a genomic island integrated at the leuX locus, and the phylogenetic analysis of the TgtA5 family is consistent with widespread horizontal gene transfer. Comparison of transformation efficiencies of modified or unmodified plasmids into isogenic S. Montevideo strains containing or lacking the cluster strongly suggests a restriction-modification role for the cluster in Enterobacteriaceae. Another preQ 0 derivative, 2'-deoxy-7-formamidino-7-deazaguanosine, was found in the Escherichia coli bacteriophage 9g, as predicted from the presence of homologs of genes involved in the synthesis of the archaeosine tRNA modification. These results illustrate a deep and unexpected evolutionary connection between DNA and tRNA metabolism.DNA modification | restriction-modification | 7-deazaguanine | comparative genomics | queuosine H ypermodifications of DNA requiring more than one synthetic enzyme are not as prevalent and chemically diverse as RNA hypermodifications, but around a dozen have been identified in DNA to date (1). The functions of most DNA hypermodifications are still not known, but some have roles in protection against restriction enzymes, whereas others affect thermal stability temperature, DNA packaging, or transcription regulation (2). For example, the hypermodified DNA base β-D-glucosyl-hydroxymethyluracil, or base J, is an epigenetic factor that regulates Pol II transcription initiation in kinetoplastids of trypanosomes (3). The recently discovered phosphorothioate (PT) modification of the DNA backbone in bacteria was found to perform different functions in different organisms (4-6). In Salmonella Cerro 87, PT occurs on each strand of a GAAC/GTTC motif as part of a restriction-modification (R-M) system, whereas in Vibrio cyclitrophicus FF75, which lacks PT restriction enzymes, PT occurs on one strand of C ps CA motifs, and the function remains unclear (6). In 2013, Iyer et al. described the computational prediction of 12 novel DNA hypermodificat...

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Section: 46)mentioning

confidence: 99%

Novel genomic island modifies DNA with 7-deazaguanine derivatives

Thiaville

Kellner

Yuan

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

155

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“…UVR-resistant microorganisms have the potential to thrive in environments with high radiation levels, such as nuclear waste fields [41]. Pigmentation has been known to protect organisms against UVR.…”

Section: Tolerance and Survivability Of Uvrresistant Extremophilesmentioning

confidence: 99%

“…Microbial ability to survive in extreme UVR is reviewed to connect with their genome stability [2,41,47,49]. Several other UVR-resistant bacteria have been revealed to produce metabolites of primary and secondary metabolism in their defense [2,12].…”

Section: Introductionmentioning

confidence: 99%

Bio-signature of Ultraviolet-Radiation-Resistant Extremophiles from Elevated Land

Gabani¹,

Prakash²,

Singh³

2014

AJMR

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Microorganisms with the ability to survive high doses of radiation are known as radiation-resistant extremophiles. This study attempts to demonstrate the diversity of microorganisms resistant to ultraviolet radiation (UVR) in the natural environment in order to investigate the molecular and physiological mechanisms by which these microorganisms survive under extreme radiation. We hypothesized that topsoil from elevated land (hills) would reveal a diverse variety of UVR-resistant extremophiles with modulated proteins/enzymes.

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“…E. coli succumbs to around 10 DSB and Shewanella oneidensis MR-1 dies after 1 DSB (based on calculations of 0.0114 DSBs / Gy / Genome; Daly et al, 2004). Remarkably, Kineococcus radiotolerans can accumulate more than 200 DSB (20kGy γ-radiation) and within 3 -4 days all DNA and cellular damage is repaired and cell division resumes (Bagwell et al, 2008a). The cellular and biomolecular phenomena underlying the extreme radioresistance phenotoype in K. radiotolerans are unknown, and have the subject of recent research efforts.…”

Section: High Level Waste Microbiologymentioning

confidence: 99%

“…In addition to many of these components, SRS HLW also contains low molecular weight organic complexants and decontamination reagents (i.e., oxalate, glycolate, citrate, and formate), which are noteworthy because they interfere with existing downstream processing of legacy HLW materials. None of these low MW organic compounds are suitable growth substrates for K. radiotolerans; however, formate and oxalate each sustained cell viability during periods of prolonged starvation (Bagwell et al, 2008a). The genome of K. radiotolerans encodes for a single formate dehydrogenase whose functionality has not be deduced; though in this capacity it may function to generate reducing equivalents for maintenance purposes by oxidizing formate to CO 2 .…”

Section: High Level Waste Microbiologymentioning

confidence: 99%

Going extreme for small solutions to big environmental challenges.

Bagwell¹

2012

Microbial Biotechnology: Energy and Environment

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Prokaryotes are the most abundant and diverse life form on planet Earth, estimates of prokaryotic numbers and productivity approach 10 30 year -1 (Whitman et al., 1998). Prokaryotes are responsible for catalyzing important biogeochemical reactions and transformations that sustain the biosphere. Prokaryotes have been evolving for 3 -4 billion years (Ernst, 1983) and during this time, have found ways to occupy every conceivable environment on the planet; including the most inhospitable habitats both nature and man have created. 'Microbial ecology is the study of microbial physiology under the worst possible conditions'T.D. Brock, 1966 Most environmental microbiologists would agree that this popular quote by Thomas Brock straightforwardly applies to the maintenance of microbial diversity and ecosystem functions amidst a complex backdrop of ever changing biological, physical, and chemical conditions in terrestrial and aquatic biomes. But does it stop there, what about the de facto 'worst possible condition?'Many of the environmental challenges outlined in this chapter are not exclusive to the United States but rather affect much of the industrialized world (Pedersen, 1999) because of past military activities and continued expansion of the military -industry complex. While not comprehensive, this chapter is devoted to the scale, scope, and specific issues confronting the cleanup and long-term disposal of the U.S. nuclear legacy generated during WWII and the Cold War Era. Furthermore, microbial interactions and metabolism in, around, and affecting existing and planned geological nuclear waste repositories are serious concerns for safe disposal, future planning, and reliable risk assessment for the environmental and human health. Nuclear Legacy WasteExtensive volumes and complex mixtures of nuclear waste are a lasting legacy of the Cold War Era. The U.S. began building the first atomic bomb in 1942. These efforts generated more than 36 million cubic meters of long-lived radioactive and toxic waste by the end of the Cold War in 1989. Irradiated fuels and past nuclear processing streams still await treatment and safe disposal in aged storage configurations. Mixtures of metals, radionuclides, hydrocarbons, and ions contaminate soils, sediments, and groundwater across the nuclear -industrial complex. The U.S. Department of Energy (DOE hereafter) is responsible for management, disposal, and long-term stewardship of this lasting legacy. Because of the prohibitive cost and inefficiencies of existing chemical and physical remedial strategies to address large volumes of contaminant mixtures, newly advanced technologies are greatly needed for reduction and treatment of nuclear legacy waste. Bioremediation is a potentially powerful and innovative technology for converting toxic pollutants to benign end products with a significant cost savings over conventional approaches. The reality, however, is that bioremediation is complicated by the unpredictability of natural ecosystems, complex interactions between co-contaminants and t...

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Survival in Nuclear Waste, Extreme Resistance, and Potential Applications Gleaned from the Genome Sequence of Kineococcus radiotolerans SRS30216

Cited by 63 publications

References 60 publications

Novel genomic island modifies DNA with 7-deazaguanine derivatives

Novel genomic island modifies DNA with 7-deazaguanine derivatives

Bio-signature of Ultraviolet-Radiation-Resistant Extremophiles from Elevated Land

Going extreme for small solutions to big environmental challenges.

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