The origin and impeded dissemination of the DNA phosphorothioation system in prokaryotes
1.Eckstein, F. Phosphorothioation of DNA in bacteria. Nat. Chem. Biol. 3, 689–690 (2007).CAS
PubMed
Article
Google Scholar
2.Wang, L. et al. Phosphorothioation of DNA in bacteria by dnd genes. Nat. Chem. Biol. 3, 709–710 (2007).CAS
PubMed
Article
Google Scholar
3.Zhou, X. et al. A novel DNA modification by sulphur. Mol. Microbiol. 57, 1428–1438 (2005).CAS
PubMed
Article
Google Scholar
4.Chen, S., Wang, L. & Deng, Z. Twenty years hunting for sulfur in DNA. Protein cell 1, 14–21 (2010).PubMed
PubMed Central
Article
CAS
Google Scholar
5.Xu, T. et al. DNA phosphorothioation in Streptomyces lividans: mutational analysis of the dnd locus. BMC Microbiol. 9, 41 (2009).PubMed
PubMed Central
Article
CAS
Google Scholar
6.You, D., Wang, L., Yao, F., Zhou, X. & Deng, Z. A novel DNA modification by sulfur: DndA is a NifS-like cysteine desulfurase capable of assembling DndC as an iron-sulfur cluster protein in Streptomyces liVidans. Biochemistry 46, 6126–6133 (2007).CAS
PubMed
Article
Google Scholar
7.Chen, F. et al. Crystal structure of the cysteine desulfurase DndA from Streptomyces lividans which is involved in DNA phosphorothioation. PLoS ONE 7, e36635 (2012).ADS
CAS
PubMed
PubMed Central
Article
Google Scholar
8.An, X. et al. A novel target of IscS in Escherichia coli: participating in DNA phosphorothioation. PLoS ONE 7, e51265 (2012).ADS
CAS
PubMed
PubMed Central
Article
Google Scholar
9.Wang, L., Jiang, S., Deng, Z., Dedon, P. C. & Chen, S. DNA phosphorothioate modification-a new multi-functional epigenetic system in bacteria. FEMS Microbiol. Rev. 43, 109–122 (2019).CAS
PubMed
Article
Google Scholar
10.Yao, F., Xu, T., Zhou, X., Deng, Z. & You, D. Functional analysis of spfD gene involved in DNA phosphorothioation in Pseudomonas fluorescens Pf0-1. FEBS Lett. 583, 729–733 (2009).CAS
PubMed
Article
PubMed Central
Google Scholar
11.Hu, W. et al. Structural insights into DndE from Escherichia coli B7A involved in DNA phosphorothioation modification. Cell Res. 22, 1203–1206 (2012).ADS
CAS
PubMed
PubMed Central
Article
Google Scholar
12.Cheng, Q. et al. Regulation of DNA phosphorothioate modifications by the transcriptional regulator DptB in Salmonella. Mol. Microbiol. 97, 1186–1194 (2015).CAS
PubMed
Article
PubMed Central
Google Scholar
13.Xiong, W., Zhao, G., Yu, H. & He, X. Interactions of Dnd proteins involved in bacterial DNA phosphorothioate modification. Front. Microbiol. 6, 1139 (2015).PubMed
PubMed Central
Google Scholar
14.Dai, D. et al. DNA phosphorothioate modification plays a role in peroxides resistance in Streptomyces lividans. Front. Microbiol. 7, 1380 (2016).PubMed
PubMed Central
Google Scholar
15.Xie, X. et al. Phosphorothioate DNA as an antioxidant in bacteria. Nucleic Acids Res. 40, 9115–9124 (2012).CAS
PubMed
PubMed Central
Article
Google Scholar
16.Yang, Y. et al. DNA backbone sulfur-modification expands microbial growth range under multiple stresses by its anti-oxidation function. Sci. Rep. 7 (2017).17.Xu, T., Yao, F., Zhou, X., Deng, Z. & You, D. A novel host-specific restriction system associated with DNA backbone S-modification in Salmonella. Nucleic Acids Res. 38, 7133–7141 (2010).CAS
PubMed
PubMed Central
Article
Google Scholar
18.Liu, G. et al. Cleavage of phosphorothioated DNA and methylated DNA by the Type IV restriction endonuclease ScoMcrA. PLoS Genet. 6, e1001253 (2010).CAS
PubMed
PubMed Central
Article
Google Scholar
19.Tong, T. et al. Occurrence, evolution, and functions of DNA phosphorothioate epigenetics in bacteria. Proc. Natl Acad. Sci. USA 115, E2988–E2996 (2018).CAS
PubMed
PubMed Central
Article
Google Scholar
20.Xiong, L. et al. A new type of DNA phosphorothioation-based antiviral system in archaea. Nat. Commun. 10 (2019).21.Xiong, X. et al. SspABCD-SspE is a phosphorothioation-sensing bacterial defence system with broad anti-phage activities. Nat. Microbiol. 5, 917–928 (2020).CAS
PubMed
Article
PubMed Central
Google Scholar
22.Dai, D., Pu, T., Liang, J., Wang, Z. & Tang, A. Regulation of dndB gene expression in Streptomyces lividans. Front. Microbiol. 9, 2387 (2018).PubMed
PubMed Central
Article
Google Scholar
23.Zhou, X., Deng, Z., Firmin, J. L., Hopwood, D. A. & Kieser, T. Site-specific degradation of Streptomyces lividans DNA during electrophoresis in buffers contaminated with ferrous iron. Nucleic Acids Res. 16, 4341–4352 (1988).CAS
PubMed
PubMed Central
Article
Google Scholar
24.Sun, Y. et al. DNA phosphorothioate modifications are widely distributed in the human microbiome. Biomolecules 10, 1175 (2020).CAS
PubMed Central
Article
Google Scholar
25.Khan, H. et al. DNA phosphorothioate modification facilitates the dissemination of mcr-1 and blaNDM-1 in drinking water supply systems. Environ. Pollut. 268, 115799 (2021).CAS
PubMed
Article
PubMed Central
Google Scholar
26.Wang, L. et al. DNA phosphorothioation is widespread and quantized in bacterial genomes. Proc. Natl Acad. Sci. USA 108, 2963–2968 (2011).ADS
CAS
PubMed
PubMed Central
Article
Google Scholar
27.Blow, M. J. et al. The epigenomic landscape of prokaryotes. PLoS Genet. 12, e1005854 (2016).PubMed
PubMed Central
Article
CAS
Google Scholar
28.Yang, X., Jian, H. & Wang, F. pSW2, a novel low-temperature-inducible gene expression vector based on a filamentous phage of the deep-sea bacterium Shewanella piezotolerans WP3. Appl. Environ. Microbiol. 81, 5519–5526 (2015).ADS
CAS
PubMed
PubMed Central
Article
Google Scholar
29.Cao, B. et al. Genomic mapping of phosphorothioates reveals partial modification of short consensus sequences. Nat. Commun. 5, 3951 (2014).ADS
CAS
PubMed
Article
PubMed Central
Google Scholar
30.Jian, H. et al. Multiple mechanisms are involved in repression of filamentous phage SW1 transcription by the DNA-binding protein FpsR. J. Mol. Biol. 431, 1113–1126 (2019).CAS
PubMed
Article
Google Scholar
31.Lai, C. et al. In vivo mutational characterization of DndE involved in DNA phosphorothioate modification. PLoS ONE 9, e107981 (2014).ADS
PubMed
PubMed Central
Article
CAS
Google Scholar
32.Schoemaker, J. M., Gayda, R. C. & Markovitz, A. Regulation of cell division in Escherichia coli: SOS induction and cellular location of the SulA protein, a key to lon-associated filamentation and death. J. Bacteriol. 158, 551–561 (1984).CAS
PubMed
PubMed Central
Article
Google Scholar
33.Jian, H., Xiong, L., Xu, G., Xiao, X. & Wang, F. Long 5′ untranslated regions regulate the RNA stability of the deep-sea filamentous phage SW1. Sci. Rep. 6, 21908 (2016).ADS
CAS
PubMed
PubMed Central
Article
Google Scholar
34.Chen, C. et al. Convergence of DNA methylation and phosphorothioation epigenetics in bacterial genomes. Proc. Natl Acad. Sci. USA 114, 4501–4506 (2017).CAS
PubMed
PubMed Central
Article
Google Scholar
35.Maleki, F., Khosravi, A., Nasser, A., Taghinejad, H. & Azizian, M. Bacterial heat shock protein activity. J. Clin. Diagnostic Res. 10, BE01–BE03 (2016).CAS
Google Scholar
36.Knoll, A. H. Paleobiological perspectives on early microbial evolution. Cold Spring Harb. Perspect. Biol. 7, a018093 (2015).PubMed
PubMed Central
Article
Google Scholar
37.Schirrmeister, B. E., Gugger, M. & Donoghue, P. C. Cyanobacteria and the great oxidation event: evidence from genes and fossils. Palaeontology 58, 769–785 (2015).PubMed
PubMed Central
Article
Google Scholar
38.Luo, G. et al. Rapid oxygenation of Earth’s atmosphere 2.33 billion years ago. Sci. Adv. 2, e1600134 (2016).ADS
PubMed
PubMed Central
Article
CAS
Google Scholar
39.Wacey, D., Kilburn, M. R., Saunders, M., Cliff, J. & Brasier, M. D. Microfossils of sulphur-metabolizing cells in 3.4-billion-year-old rocks of Western Australia. Nat. Geosci. 4, 698–702 (2011).ADS
CAS
Article
Google Scholar
40.Bontognali, T. R. R. et al. Sulfur isotopes of organic matter preserved in 3.45-billion-year-old stromatolites reveal microbial metabolism. Proc. Natl Acad. Sci. USA 109, 15146–15151 (2012).ADS
CAS
PubMed
PubMed Central
Article
Google Scholar
41.Schirrmeister, B. E., Vos, J. M. D., Antonelli, A. & Bagheri, H. C. Evolution of multicellularity coincided with increased diversification of cyanobacteria and the great oxidation event. Proc. Natl Acad. Sci. USA 110, 1791–1796 (2013).ADS
CAS
PubMed
PubMed Central
Article
Google Scholar
42.Pang, K. et al. Nitrogen-fixing heterocystous Cyanobacteria in the tonian period. Curr. Biol. 28, 616–622 (2018).CAS
PubMed
Article
Google Scholar
43.Demoulin, C. F. et al. Cyanobacteria evolution: Insight from the fossil record. Free Radic. Biol. Med. in press (2021).44.Soo, R. M., Hemp, J., Parks, D. H., Fischer, W. W. & Hugenholtz, P. On the origins of oxygenic photosynthesis and aerobic respiration in Cyanobacteria. Science 355, 1436–1440 (2017).ADS
CAS
PubMed
Article
Google Scholar
45.Ou, H.-Y. et al. dndDB: a database focused on phosphorothioation of the DNA backbone. PLoS ONE 4, e5132 (2009).ADS
PubMed
PubMed Central
Article
CAS
Google Scholar
46.Janda, J. M. & Abbott, S. L. The genus Shewanella: from the briny depths below to human pathogen. Crit. Rev. Microbiol. 40, 293–312 (2014).PubMed
Article
Google Scholar
47.Fredrickson, J. K. et al. Towards environmental systems biology of Shewanella. Nat. Rev. Microbiol. 6, 592–603 (2008).CAS
PubMed
Article
Google Scholar
48.Hau, H. H. & Gralnick, J. A. Ecology and biotechnology of the genus Shewanella. Annu. Rev. Microbiol. 61, 237–258 (2007).CAS
PubMed
Article
Google Scholar
49.Nealson, K. H. & Scott, J. Ecophysiology of the Genus Shewanella. Prokaryotes 6, 1133–1151 (2006).Article
Google Scholar
50.Roux, S. et al. Cryptic inoviruses revealed as pervasive in bacteria and archaea across Earth’s biomes. Nat. Microbiol. 4, 1895–1906 (2019).CAS
PubMed
PubMed Central
Article
Google Scholar
51.Hay, I. D. & Lithgow, T. Filamentous phages: masters of a microbial sharing economy. EMBO Rep. 20, e47427 (2019).PubMed
PubMed Central
Article
CAS
Google Scholar
52.Mai-Prochnow, A. et al. ‘Big things in small packages: the genetics of filamentous phage and effects on fitness of their host’. FEMS Microbiol. Rev. 39, 465–487 (2015).PubMed
Article
PubMed Central
Google Scholar
53.Middelboe, M., Glud, R. N. & Finster, K. Distribution of viruses and bacteria in relation to diagenetic activity in an estuarine sediment. Limnol. Oceanogr. 48, 1447–1456 (2003).ADS
Article
Google Scholar
54.Engelhardt, T., Orsi, W. D. & Jørgensen, B. B. Viral activities and life cycles in deep subseafloor sediments. Environ. Microbiol. Rep. 7, 868–873 (2015).CAS
PubMed
Article
PubMed Central
Google Scholar
55.Dell’Anno, A., Corinaldesi, C. & Danovaro, R. Virus decomposition provides an important contribution to benthic deep-sea ecosystem functioning. Proc. Natl Acad. Sci. USA 112, E2014–E2019 (2015).ADS
PubMed
PubMed Central
Article
CAS
Google Scholar
56.Rakonjac, J. Filamentous Bacteriophages: Biology and Applications. eLS (2012).57.Güemes, A. G. C. et al. Viruses as winners in the game of life. Annu. Rev. Virol. 3, 197–214 (2016).Article
CAS
Google Scholar
58.Breitbart, M. Marine viruses: truth or dare. Annu. Rev. Mar. Sci. 4, 425–448 (2012).ADS
Article
Google Scholar
59.Danovaro, R. et al. Marine viruses and global climate change. FEMS Microbiol. Rev. 35, 993–1034 (2011).CAS
PubMed
Article
PubMed Central
Google Scholar
60.Rohwer, F. & Thurber, R. V. Viruses manipulate the marine environment. Nature 459, 207–212 (2009).ADS
CAS
PubMed
Article
PubMed Central
Google Scholar
61.Touchon, M., Bernheim, A. & Rocha, E. P. Genetic and life-history traits associated with the distribution of prophages in bacteria. ISME J. 10, 2744–2754 (2016).CAS
PubMed
PubMed Central
Article
Google Scholar
62.Harrison, E. & Brockhurst, M. A. Ecological and evolutionary benefits of temperate phage: what does or doesn’t kill you makes you stronger. Bioessays 39, 201700112 (2017).Article
Google Scholar
63.Paul, J. H. Prophages in marine bacteria: dangerous molecular time bombs or the key to survival in the seas? ISME J. 2, 579–589 (2008).CAS
PubMed
Article
PubMed Central
Google Scholar
64.Wu, X. et al. Epigenetic competition reveals density-dependent regulation and target site plasticity of phosphorothioate epigenetics in bacteria. PNAS 117, 14322–14330 (2020).CAS
PubMed
PubMed Central
Google Scholar
65.Willbanks, A. et al. The evolution of epigenetics: from prokaryotes to humans and its biological consequences. Genet. Epigenet. 8, 25–36 (2016).PubMed
PubMed Central
Article
Google Scholar
66.Razin, A. & Cedar, H. DNA methylation and gene expression. Microbiol. Rev. 55, 451–458 (1991).CAS
PubMed
PubMed Central
Article
Google Scholar
67.Casadesús, J. & Low, D. Epigenetic gene regulation in the bacterial world. Microbiol. Mol. Biol. Rev. 70, 830–856 (2006).PubMed
PubMed Central
Article
CAS
Google Scholar
68.Iyer, L. M., Abhiman, S. & Aravind, L. Natural history of eukaryotic DNA methylation systems. Prog. Mol. Biol. Transl. Sci. 101, 25–104 (2011).CAS
PubMed
Article
PubMed Central
Google Scholar
69.Weiss, M. C. et al. The physiology and habitat of the last universal common ancestor. Nat. Microbiol. 1, 16116 (2016).CAS
PubMed
Article
PubMed Central
Google Scholar
70.Gan, R. et al. DNA phosphorothioate modifications influence the global transcriptional response and protect DNA from double-stranded breaks. Sci. Rep. 4, 6642 (2014).CAS
PubMed
PubMed Central
Article
Google Scholar
71.Chen, L. et al. Theoretical study on the relationship between Rp-phosphorothioation and base-step in S-DNA: based on energetic and structural analysis. J. Phys. Chem. B 119, 474–481 (2015).CAS
PubMed
Article
Google Scholar
72.Kellner, S. et al. Oxidation of phosphorothioate DNA modifications leads to lethal genomic instability. Nat. Chem. Biol. 13, 888–894 (2017).CAS
PubMed
PubMed Central
Article
Google Scholar
73.Ślesak, I., Kula, M., Ślesak, H., Miszalski, Z. & Strzałka, K. How to define obligatory anaerobiosis? An evolutionary view on the antioxidant response system and the early stages of the evolution of life on Earth. Free Radic. Biol. Med. 140, 61–73 (2019).PubMed
Article
CAS
Google Scholar
74.Brioukhanov, A. L., Thauer, R. K. & Netrusov, A. I. Catalase and superoxide dismutase in the cells of strictly anaerobic microorganisms. Microbiol. (Russ. Acad. Sci.) 71, 330–335 (2002).
Google Scholar
75.Sebaihia, M. et al. The multidrug-resistant human pathogen Clostridium difficile has a highly mobile, mosaic genome. Nat. Genet. 38, 779–786 (2006).PubMed
Article
CAS
Google Scholar
76.Kanehisa, M. et al. Data, information, knowledge and principle: back to metabolism in KEGG. Nucleic Acids Res. 42, D199–D205 (2014).CAS
PubMed
Article
Google Scholar
77.Buchfink, B., Xie, C. & Huson, D. H. Fast and sensitive protein alignment using DIAMOND. Nat. Methods 12, 59–60 (2015).CAS
PubMed
Article
Google Scholar
78.Kieft, K., Zhou, Z. & Anantharaman, K. VIBRANT: automated recovery, annotation and curation of microbial viruses, and evaluation of viral community function from genomic sequences. Microbiome 8, 90 (2020).PubMed
PubMed Central
Article
Google Scholar
79.Gregory, A. C. et al. Marine DNA viral macro- and microdiversity from pole to pole. Cell 177, 1109–1123 (2019).CAS
PubMed
PubMed Central
Article
Google Scholar
80.Katoh, K. & Standley, D. M. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol. Biol. Evol. 30, 772–780 (2013).CAS
PubMed
PubMed Central
Article
Google Scholar
81.Capella-Gutiérrez, S., Silla-Martínez, J. M. & Gabaldón, T. trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics 25, 1972–1973 (2009).PubMed
PubMed Central
Article
CAS
Google Scholar
82.Stamatakis, A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30, 1312–1313 (2014).CAS
PubMed
PubMed Central
Article
Google Scholar
83.Chaumeil, P.-A., Mussig, A. J., Hugenholtz, P. & Parks, D. H. GTDB-Tk: a toolkit to classify genomes with the genome taxonomy database. Bioinformatics 36, 1925–1927 (2020).CAS
Google Scholar
84.Price, M. N., Dehal, P. S. & Arkin, A. P. FastTree 2–approximately maximum-likelihood treesfor large alignments. PLoS ONE 5, e9490 (2010).ADS
PubMed
PubMed Central
Article
CAS
Google Scholar
85.Kumar, S., Stecher, G., Li, M., Knyaz, C. & Tamura, K. MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol. Biol. Evol. 35, 1547–1549 (2018).CAS
PubMed
PubMed Central
Article
Google Scholar
86.Letunic, I. & Bork, P. Interactive Tree Of Life (iTOL) v4: recent updates and new developments. Nucleic Acids Res. 47, W256–W259 (2019).CAS
PubMed
PubMed Central
Article
Google Scholar
87.Kwak, S. G. & Kim, J. H. Central limit theorem: the cornerstone of modern statistics. Korean J. Anesthesiol. 70, 144–156 (2017).PubMed
PubMed Central
Article
Google Scholar
88.Virtanen, P. et al. SciPy 1.0: fundamental algorithms for scientific computing in Python. Nat. Methods 17, 261–272 (2020).CAS
PubMed
PubMed Central
Article
Google Scholar
89.R: A language and environment for statistical computing (R Foundation for Statistical Computing, Vienna, Austria, 2013).90.Chok, N. S. Pearson’s versus Spearman’s and Kendall’s correlation coefficients for continuous data Master of Science thesis, University of Pittsburgh, (2010).91.Jian, H., Xu, G., Gai, Y., Xu, J. & Xiao, X. The histone-like nucleoid structuring protein (H-NS) is a negative regulator of the lateral flagellar system in the deep-sea bacterium Shewanella piezotolerans WP3. Appl. Environ. Microbiol. 82, 2388–2398 (2016).ADS
CAS
PubMed
PubMed Central
Article
Google Scholar
92.Wang, F. et al. Environmental adaptation: genomic analysis of the piezotolerant and psychrotolerant deep-sea iron reducing bacterium Shewanella piezotolerans WP3. PLoS ONE 3, e1937 (2008).ADS
PubMed
PubMed Central
Article
CAS
Google Scholar
93.Jian, H., Xu, J., Xiao, X. & Wang, F. Dynamic modulation of DNA replication and gene transcription in deep-sea filamentous phage SW1 in response to changes of host growth and temperature. PLoS ONE 7, e41578 (2012).ADS
CAS
PubMed
PubMed Central
Article
Google Scholar
94.Chin, C.-S. et al. Nonhybrid, finished microbial genome assemblies from long-read SMRT sequencing data. Nat. Methods 10, 563–569 (2016).Article
CAS
Google Scholar
95.Chen, S., Zhou, Y., Chen, Y. & Gu, J. fastp: an ultra-fast all-in-one FASTQ preprocessor. Bioinformatics 34, i884–i890 (2018).PubMed
PubMed Central
Article
CAS
Google Scholar
96.Kim, D., Langmead, B. & Salzberg, S. L. HISAT: a fast spliced aligner with low memory requirements. Nat. Methods 12, 357–360 (2015).CAS
PubMed
PubMed Central
Article
Google Scholar
97.Li, B. & Dewey, C. N. RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinform. 12, 323 (2011).CAS
Article
Google Scholar
98.Wang, L., Feng, Z., Wang, X., Wang, X. & Zhang, X. DEGseq: an R package for identifying differentially expressed genes from RNA-seq data. Bioinformatics 26, 136–138 (2010).PubMed
Article
CAS
PubMed Central
Google Scholar
99.Trapnell, C. et al. Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat. Biotechnol. 28, 511–515 (2010).CAS
PubMed
PubMed Central
Article
Google Scholar
100.Robinson, M. D., McCarthy, D. J. & Smyth, G. K. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26, 139–140 (2010).CAS
PubMed
PubMed Central
Article
Google Scholar
101.Gao, H. et al. Reduction of nitrate in Shewanella oneidensis depends on atypical NAP and NRF systems with NapB as a preferred electron transport protein from CymA to NapA. ISME J. 3, 966–976 (2009).CAS
PubMed
Article
PubMed Central
Google Scholar
102.Lenski, R. E., Rose, M. R., Simpson, S. C. & Tadler, S. C. Long-term experimental evolution in Escherichia coli. I. Adaptation and divergence during 2000 generations. Am. Naturalist 138, 1315–1341 (1991).Article
Google Scholar More