Abstract
Background
Streptomyces seoulensis has contributed to the discovery and initiation of extensive research into nickel superoxide dismutase (NiSOD), a unique type of superoxide dismutase found in actinomycetes. Still so far, there is no information about whole genome sequence of this strain.
Objective
To investigate complete genome sequence and perform bioinformatic analyses for genomic functions related with nickel-associated genes.
Methods
DNA was extracted using the Wizard Genomic DNA Purification Kit then sequenced using a Pacific Biosciences SMRT cell 8Pac V3 DNA Polymerase Binding Kit P6 with the PacBiov2 RSII platform. We assembled the PacBio long-reads with the HGAP3 pipeline.
Results
We obtained complete genome sequence of S. seoulensis, which comprises a 6,339,363 bp linear chromosome. While analyzing the genome to annotate the genomic function, we discovered the nickel-associated genes. We observed that the sodN gene encoding for NiSOD is located adjacent to the sodX gene, which encodes for the nickel-type superoxide dismutase maturation protease. In addition, several nickel-associated genes and gene clusters-nickel-responsive regulator, nickel uptake transporter, nickel–iron [NiFe]-hydrogenase and other putative genes were also detected. Strain specific genes were discovered through a comparative analysis of S. coelicolor and S. griseus. Further bioinformatic analyses revealed that this strain encodes at least 22 putative biosynthetic gene clusters, thereby implying that S. seoulensis has the potential to produce novel bioactive compounds.
Conclusion
We annotated the genome and determined nickel-associated genes and gene clusters and discovered biosynthetic gene clusters for secondary metabolites implying that S. seoulensis produces novel types of bioactive compounds.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Ahn BE, Cha J, Lee EJ, Han AR, Thompson CJ, Roe JH (2006) Nur, a nickel-responsive regulator of the Fur family, regulates superoxide dismutases and nickel transport in Streptomyces coelicolor. Mol Microbiol 59:1848–1858
Atherton JC (2006) The pathogenesis of Helicobacter pylori-induced gastro-duodenal diseases. Annu Rev Pathol 1:63–96
Aziz RK, Bartels D, Best AA, DeJongh M, Disz T, Edwards RA, Formsma K, Gerdes S, Glass EM, Kubal M et al (2008) The RAST server: rapid annotations using subsystems technology. BMC Genom 9:75
Bentley SD, Chater KF, Cerdeno-Tarraga AM, Challis GL, Thomson NR, James KD, Harris DE, Quail MA, Kieser H, Harper D et al (2002) Complete genome sequence of the model actinomycete Streptomyces coelicolor A3(2). Nature 417:141–147
Boer JL, Mulrooney SB, Hausinger RP (2014) Nickel-dependent metalloenzymes. Arch Biochem Biophys 544:142–152
Broering EP, Truong PT, Gale EM, Harrop TC (2013) Synthetic analogues of nickel superoxide dismutase: a new role for nickel in biology. Biochemistry 52:4–18
Challis GL, Hopwood DA (2003) Synergy and contingency as driving forces for the evolution of multiple secondary metabolite production by Streptomyces species. Proc Natl Acad Sci USA 100(Suppl 2):14555–14561
Chin CS, Alexander DH, Marks P, Klammer AA, Drake J, Heiner C, Clum A, Copeland A, Huddleston J, Eichler EE et al (2013) Nonhybrid, finished microbial genome assemblies from long-read SMRT sequencing data. Nat Methods 10:563–569
Chun J, Youn HD, Yim YI, Lee H, Kim MY, Hah YC, Kang SO (1997) Streptomyces seoulensis sp. nov. Int J Syst Bacteriol 47:492–498
Constant P, Chowdhury SP, Pratscher J, Conrad R (2010) Streptomycetes contributing to atmospheric molecular hydrogen soil uptake are widespread and encode a putative high-affinity [NiFe]-hydrogenase. Environ Microbiol 12:821–829
Darling AC, Mau B, Blattner FR, Perna NT (2004) Mauve: multiple alignment of conserved genomic sequence with rearrangements. Genome Res 14:1394–1403
Dufresne A, Salanoubat M, Partensky F, Artiguenave F, Axmann IM, Barbe V, Duprat S, Galperin MY, Koonin EV, Le Gall F et al (2003) Genome sequence of the cyanobacterium Prochlorococcus marinus SS120, a nearly minimal oxyphototrophic genome. Proc Natl Acad Sci USA 100:10020–10025
Dupont CL, Neupane K, Shearer J, Palenik B (2008) Diversity, function and evolution of genes coding for putative Ni-containing superoxide dismutases. Environ Microbiol 10:1831–1843
Eitinger T (2004) In vivo production of active nickel superoxide dismutase from Prochlorococcus marinus MIT9313 is dependent on its cognate peptidase. J Bacteriol 186:7821–7825
Huerta-Cepas J, Szklarczyk D, Forslund K, Cook H, Heller D, Walter MC, Rattei T, Mende DR, Sunagawa S, Kuhn M et al (2016) eggNOG 4.5: a hierarchical orthology framework with improved functional annotations for eukaryotic, prokaryotic and viral sequences. Nucleic Acids Res 44:D286–S293
Jiao RH, Xu H, Cui JT, Ge HM, Tan RX (2013) Neuraminidase inhibitors from marine-derived actinomycete Streptomyces seoulensis. J Appl Microbiol 114:1046–1053
Kim FJ, Kim HP, Hah YC, Roe JH (1996) Differential expression of superoxide dismutases containing Ni and Fe/Zn in Streptomyces coelicolor. Eur J Biochem 241:178–185
Kim EJ, Chung HJ, Suh B, Hah YC, Roe JH (1998) Transcriptional and post-transcriptional regulation by nickel of sodN gene encoding nickel-containing superoxide dismutase from Streptomyces coelicolor Muller. Mol Microbiol 27:187–195
Kim IK, Yim YI, Kim YM, Lee JW, Yim HS, Kang SO (2003) CbiX-homologous protein (CbiXhp), a metal-binding protein, from Streptomyces seoulensis is involved in expression of nickel-containing superoxide dismutase. FEMS Microbiol Lett 228:21–26
Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874
Lacasse MJ, Zamble DB (2016) [NiFe]-hydrogenase maturation. Biochemistry 55:1689–1701
Leclere V, Boiron P, Blondeau R (1999) News & notes: diversity of superoxide-dismutases among clinical and soil isolates of Streptomyces species. Curr Microbiol 39:365–0368
Liot Q, Constant P (2016) Breathing air to save energy–new insights into the ecophysiological role of high-affinity [NiFe]-hydrogenase in Streptomyces avermitilis. Microbiologyopen 5:47–59
Liu LK, Dai Y, Abdelwahab H, Sobrado P, Tanner JJ (2018) Structural evidence for rifampicin monooxygenase inactivating rifampicin by cleaving its ansa-bridge. Biochemistry 57:2065–2068
Maier RJ (2005) Use of molecular hydrogen as an energy substrate by human pathogenic bacteria. Biochem Soc Trans 33:83–85
Mobley HL, Hausinger RP (1989) Microbial ureases: significance, regulation, and molecular characterization. Microbiol Rev 53:85–108
Moore SJ, Warren MJ (2012) The anaerobic biosynthesis of vitamin B12. Biochem Soc Trans 40:581–586
Palenik B, Brahamsha B, Larimer FW, Land M, Hauser L, Chain P, Lamerdin J, Regala W, Allen EE, McCarren J et al (2003) The genome of a motile marine Synechococcus. Nature 424:1037–1042
Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425
Song YN, Zhang WJ, Bi SF, Jiao RH, Tan RX, Ge HM (2015) New ansamycin analogues from the mutant strain of Streptomyces seoulensis. J Antibiot (Tokyo) 68:757–759
Weber T, Blin K, Duddela S, Krug D, Kim HU, Bruccoleri R, Lee SY, Fischbach MA, Muller R, Wohlleben W et al (2015) antiSMASH 3.0-a comprehensive resource for the genome mining of biosynthetic gene clusters. Nucleic Acids Res 43:W237–W243
Wuerges J, Lee JW, Yim YI, Yim HS, Kang SO, Djinovic Carugo K (2004) Crystal structure of nickel-containing superoxide dismutase reveals another type of active site. Proc Natl Acad Sci USA 101:8569–8574
Youn HD, Yim YI, Kim K, Hah YC, Kang SO (1995) Spectral characterization and chemical modification of catalase-peroxidase from Streptomyces sp. J Biol Chem 270:13740–13747
Youn HD, Kim EJ, Roe JH, Hah YC, Kang SO (1996a) A novel nickel-containing superoxide dismutase from Streptomyces spp. Biochem J 318(Pt 3):889–896
Youn HD, Youn H, Lee JW, Yim YI, Lee JK, Hah YC, Kang SO (1996b) Unique isozymes of superoxide dismutase in Streptomyces griseus. Arch Biochem Biophys 334:341–348
Youn H, Kwak J, Youn HD, Hah YC, Kang SO (1998) Lipoamide dehydrogenase from Streptomyces seoulensis: biochemical and genetic properties. Biochim Biophys Acta 1388:405–418
Acknowledgements
This work was supported by the National Research Foundation of Korea (NRF) grant funded by the Korean government (MSIP) [National Creative Research Laboratory Program (2012R1A3A2048767 to H.-D.Y)] and by Education and Research Encouragement Fund of Seoul National University Hospital.
Author information
Authors and Affiliations
Corresponding author
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
13258_2019_878_MOESM1_ESM.pdf
Fig. S1 Phylogenetic analysis of NiSOD and hydrogenase genes. (A) Phylogenetic tree showing the similarity of S. seoulensis sodN with other sodN genes from 38 related bacterial strains. The sodN sequences of closely related species were obtained from the NCBI GenBank database. The phylogenetic tree was generated using the Neighbor-Joining method. The S. seoulensis sodN gene is indicated by an arrow. (B) Phylogenetic analysis of hydrogenase encoding genes with known sequences from other Streptomyces species. Left: hypA, Right: hypB
13258_2019_878_MOESM3_ESM.pdf
Fig. S3 Comparison of putative biosynthetic gene clusters for secondary metabolites in S. seoulensis with S. coelicolor A3(2) and S. griseus
Rights and permissions
About this article
Cite this article
Shin, J., Park, S., Lee, JS. et al. Complete genome sequence and comparative analysis of Streptomyces seoulensis, a pioneer strain of nickel superoxide dismutase. Genes Genom 42, 273–281 (2020). https://doi.org/10.1007/s13258-019-00878-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s13258-019-00878-8