Genome sequence and annotation of Streptomyces tendae UTMC 3329, acid and alkaline tolerant actinobacterium
Abstract
Background and Objectives: Streptomyces tendae is one of the most prolific actinobacteria with a wide range of biotechnological applications. Genomic data can help in better understanding and exploration of important microorganisms, however, there is a few genomic information available for this species.
Materials and Methods: Molecular identification, pH and salt tolerance of an actinobacterium, designated Streptomyces tendae UTMC 3329, isolated from a tea field soil were done. Also, genomic DNA was extracted and sequenced using Illumina platform with MPS (massively parallel sequencing) Illumina technology. Gene annotation and bioinformatic analysis were done using appropriate software and servers.
Results: The draft genome is ~8.7 megabase pairs, containing 7557 predicted coding sequences. The strain was able to grow at pH 5-12 and 0-10% NaCl. The maximum growth rate of the bacterium was obtained at pH 7. The gene clusters involved in central carbon metabolism, phosphate regulation, transport system, stress responses were revealed. It was shown the presence of gene clusters of polyketides, ribosomally and non-ribosomally synthesized peptides. Various genes were found in xenobiotic degradation pathways and heavy metal resistance.
Conclusion: The current genomic information which reveals biological features, as well as the biotechnological potential of this acid and alkaline tolerant actinobacterium, can be implemented for further research on the species.
1. Kämpfer P, Glaeser SP, Parkes L, van Keulen G, Dyson P (2014). The Family Streptomycetaceae. In: The Prokaryotes: A Handbook of the Biology of Bacteria, Eds, E Rosenberg, EF DeLong, S Lory, E Stackebrandt, F Thompson. Springer, 538-604.
2. Aderem A. Systems biology: its practice and challenges. Cell 2005;121:511-513.
3. de Lima Procópio RE, da Silva IR, Martins MK, de Azevedo JL, de Araújo JM. Antibiotics produced by Streptomyces. Braz J Infect Dis 2012;16:466-471.
4. Baltz R. Antibiotic discovery from actinomycetes: will a renaissance follow the decline and fall? Sim News 2005;55:186-196.
5. Lee N, Kim W, Hwang S, Lee Y, Cho S, Palsson B, et al. Thirty complete Streptomyces genome sequences for mining novel secondary metabolite biosynthetic gene clusters. Sci Data 2020;7:55.
6. Hamedi J, Poorinmohammad N, Wink J (2017). The Role of Actinobacteria in Biotechnology. In: Biology and Biotechnology of Actinobacteria, Eds, J Wink, F Mohammadipanah and J Hamedi. Springer, pp. 269-328.
7. Gomez-Escribano J, Alt S, Bibb M. Next generation sequencing of actinobacteria for the discovery of novel natural products. Mar Drugs 2016;14:78.
8. Yoon S-H, Ha S-M, Kwon S, Lim J, Kim Y, Seo H, et al. Introducing EzBioCloud: a taxonomically united database of 16S rRNA gene sequences and whole-genome assemblies. Int J Syst Evol Microbiol 2017;67:1613-1617.
9. Ishaque NM, Burgsdorf I, Limlingan Malit JJ, Saha S, Teta R, Ewe D, et al. Isolation, genomic and metabolomic characterization of Streptomyces tendae VITAKN with quorum sensing inhibitory activity from southern India. Microorganisms 2020;8:121.
10. Ettlinger L, Corbaz R, Hutter R. Species classification of the genus Streptomyces Waksman et Henrici. Experientia 1958;14:334-335.
11. Eftekharivah L, Hamedi J, Zarrini G, Bakhtiari R. Introducing acidophilic and acid tolerant actinobacteria as new sources of antimicrobial agents against Helicobacter pylori. Arch Razi Inst 2020; 76: 1-23.
12. Wink J. Compendium of Actinobacteria from Dr. Joachim M. Wink, University of Braunschweig, an electronic manual including the important bacterial group of the actinomycetes. 2012 Available online at: https://www.dsmz.de/collection/catalogue/microorganisms/special-groups-of-organisms/compendium-of-actinobacteria
13. Rostamza M, Noohi A, Hamedi J. Enhancement in production of erythromycin by Saccharopolyspora erythraea by the use of suitable industrial seeding media. DARU 2008;16:13-17.
14. Hamada M, Shibata C, Tamura T, Suzuki K-i. Agromyces marinus sp. nov., a novel actinobacterium isolated from sea sediment. J Antibiot (Tokyo) 2014;67:703-706.
15. Overbeek R, Olson R, Pusch GD, Olsen GJ, Davis JJ, Disz T, et al. The SEED and the rapid annotation of microbial genomes using subsystems technology (RAST). Nucleic Acids Res 2014;42: D206-D214.
16. Kumar S, Stecher G, Li M, Knyaz C, Tamura K. MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 2018;35:1547-1549.
17. Luo R, Liu B, Xie Y, Li Z, Huang W, Yuan J, et al. SOAPdenovo2: an empirically improved memory-efficient short-read de novo assembler. GigaScience 2012;1:18.
18. Andrews S. FastQC: a quality control tool for high throughput sequence data. Babraham Bioinformatics, Babraham Institute, Cambridge, United Kingdom; 2010. Available online at: http://www.bioinformatics.babraham.ac.uk/projects/fastqc
19. Besemer J, Lomsadze A, Borodovsky M. GeneMarkS: a self-training method for prediction of gene starts in microbial genomes. Implications for finding sequence motifs in regulatory regions. Nucleic Acids Res 2001;29:2607-2618.
20. Tarailo-Graovac M, Chen N. Using repeat masker to identify repetitive elements in genomic sequences. Curr Protoc Bioinformatics 2009;Chapter 4:Unit 4.10.
21. Benson G. Tandem repeats finder: a program to analyze DNA sequences. Nucleic Acids Res 1999;27:573-580.
22. Lowe TM, Chan PP. tRNAscan-SE On-line: integrating search and context for analysis of transfer RNA genes. Nucleic Acids Res 2016;44: W54-W57.
23. Lagesen K, Hallin P, Rødland EA, Stærfeldt H-H, Rognes T, Ussery DW. RNAmmer: consistent and rapid annotation of ribosomal RNA genes. Nucleic Acids Res 2007;35:3100-3108.
24. Griffiths-Jones S, Moxon S, Marshall M, Khanna A, Eddy SR, Bateman A. Rfam: annotating non-coding RNAs in complete genomes. Nucleic Acids Res 2005;33:D121-124.
25. Grissa I, Vergnaud G, Pourcel C. CRISPRFinder: a web tool to identify clustered regularly interspaced short palindromic repeats. Nucleic Acids Res 2007;35: W52-W57.
26. Aziz RK, Bartels D, Best AA, DeJongh M, Disz T, Edwards RA, et al. The RAST Server: rapid annotations using subsystems technology. BMC Genomics 2008;9:75.
27. Greenbaum DS (2004). Clusters of Orthologous Groups (COG), in Dictionary of Bioinformatics and Computational Biology. Ed, J Hancock and M Zvelebil, John Wiley & Sons, Inc.
28. Emms DM, Kelly S. OrthoFinder: solving fundamental biases in whole genome comparisons dramatically improves orthogroup inference accuracy. Genome Biol 2015;16:157.
29. Wang Y, Coleman-Derr D, Chen G, Gu YQ. OrthoVenn: a web server for genome wide comparison and annotation of orthologous clusters across multiple species. Nucleic Acids Res 2015;43:W78-84.
30. van Heel AJ, de Jong A, Song C, Viel JH, Kok J, Kuipers OP. BAGEL4: a user-friendly web server to thoroughly mine RiPPs and bacteriocins. Nucleic Acids Res 2018;46: W278-W281.
31. Blin K, Wolf T, Chevrette MG, Lu X, Schwalen CJ, Kautsar SA, et al. anti SMASH 4.0—improvements in chemistry prediction and gene cluster boundary identification. Nucleic Acids Res 2017;45:W36-W41.
32. Lounes A, Lebrihi A, Benslimane C, Lefebvre G, Germain P. Regulation of spiramycin synthesis in Streptomyces ambofaciens: effects of glucose and inorganic phosphate. Appl Microbiol Biotechnol 1996;45:204-211.
33. Santos-Beneit F, Rodriguez-Garcia A, Franco-Dominguez E, Martin JF. Phosphate-dependent regulation of the low-and high-affinity transport systems in the model actinomycete Streptomyces coelicolor. Microbiology 2008;154:2356-2370.
34. Barreiro C, Martínez-Castro M. Regulation of the phosphate metabolism in Streptomyces genus: impact on the secondary metabolites. Appl Microbiol Biotechnol 2019;103:1643-1658.
35. Dyson P (2011). Streptomyces: molecular biology and biotechnology: Horizon Scientific Press.
36. Nouwen N, Driessen AJ. Inactivation of protein translocation by cold-sensitive mutations in the yajC-secDF operon. J Bacteriol 2005;187:6852-6855.
37. Nakajo K, Iwami Y, Komori R, Ishikawa S, Ueno T, Suzuki Y. Resistance to acidic and alkaline environments in the endodontic pathogen Enterococcus faecalis. Oral Microbiol Immunol 2006;21: 283-288.
38. Gunnarsson N, Mortensen UH, Sosio M, Nielsen J. Identification of the Entner–Doudoroff pathway in an antibiotic producing actinomycete species. Mol Microbiol 2004;52:895-902.
39. Borodina I, Schöller C, Eliasson A, Nielsen J. Metabolic network analysis of Streptomyces tenebrarius, a Streptomyces species with an active Entner-Doudoroff pathway. Appl Environ Microbiol 2005;71:2294-2302.
40. Gunnarsson N, Bruheim P, Nielsen J. Glucose metabolism in the antibiotic producing actinomycete Nonomuraea sp. ATCC 39727. Biotechnol Bioeng 2004;88:652-663.
41. van Keulen G, Siebring J, Dijkhuizen L (2011). Central carbon metabolic pathways in Streptomyces. In: Streptomyces: Molecular Biology and Biotechnology. Ed, Dyson P. First ed. Caister Academic Press, Norfolk, UK, Vol. 1. pp. 105-124.
42. Ohnishi Y, Ishikawa J, Hara H, Suzuki H, Ikenoya M, Ikeda H, et al. Genome sequence of the streptomycin-producing microorganism Streptomyces griseus IFO 13350. J Bacteriol 2008;190:4050-4060.
43. Bentley SD, Chater KF, Cerdeño-Tárraga A-M, Challis GL, Thomson N, James KD, et al. Complete genome sequence of the model actinomycete Streptomyces coelicolor A3 (2). Nature 2002;417:141-147.
44. Viollier PH, Kelemen GH, Dale GE, Nguyen KT, Buttner MJ, Thompson CJ. Specialized osmotic stress response systems involve multiple SigB-like sigma factors in Streptomyces coelicolor. Mol Microbiol 2003;47:699-714.
45. Sadeghi A, Soltani BM, Nekouei MK, Jouzani GS, Mirzaei HH, Sadeghizadeh M. Diversity of the ectoines biosynthesis genes in the salt tolerant Streptomyces and evidence for inductive effect of ectoines on their accumulation. Microbiol Res 2014;169:699-708.
46. Van-Thuoc D, Hashim SO, Hatti-Kaul R, Mamo G. Ectoine-mediated protection of enzyme from the effect of pH and temperature stress: a study using Bacillus halodurans xylanase as a model. Appl Microbiol Biotechnol 2013;97:6271-6278.
47. Wang W, Qiu Z, Tan H, Cao L. Siderophore production by actinobacteria. Biometals 2014;27:623-631.
48. Dimkpa C, Merten D, Svatoš A, Büchel G, Kothe E. Siderophores mediate reduced and increased uptake of cadmium by Streptomyces tendae F4 and sunflower (Helianthus annuus), respectively. J Appl Microbiol 2009;107:1687-1696.
49. Imbert M, Béchet M, Blondeau R. Comparison of the main siderophores produced by some species of Streptomyces. Curr Microbiol 1995;31:129-133.
2. Aderem A. Systems biology: its practice and challenges. Cell 2005;121:511-513.
3. de Lima Procópio RE, da Silva IR, Martins MK, de Azevedo JL, de Araújo JM. Antibiotics produced by Streptomyces. Braz J Infect Dis 2012;16:466-471.
4. Baltz R. Antibiotic discovery from actinomycetes: will a renaissance follow the decline and fall? Sim News 2005;55:186-196.
5. Lee N, Kim W, Hwang S, Lee Y, Cho S, Palsson B, et al. Thirty complete Streptomyces genome sequences for mining novel secondary metabolite biosynthetic gene clusters. Sci Data 2020;7:55.
6. Hamedi J, Poorinmohammad N, Wink J (2017). The Role of Actinobacteria in Biotechnology. In: Biology and Biotechnology of Actinobacteria, Eds, J Wink, F Mohammadipanah and J Hamedi. Springer, pp. 269-328.
7. Gomez-Escribano J, Alt S, Bibb M. Next generation sequencing of actinobacteria for the discovery of novel natural products. Mar Drugs 2016;14:78.
8. Yoon S-H, Ha S-M, Kwon S, Lim J, Kim Y, Seo H, et al. Introducing EzBioCloud: a taxonomically united database of 16S rRNA gene sequences and whole-genome assemblies. Int J Syst Evol Microbiol 2017;67:1613-1617.
9. Ishaque NM, Burgsdorf I, Limlingan Malit JJ, Saha S, Teta R, Ewe D, et al. Isolation, genomic and metabolomic characterization of Streptomyces tendae VITAKN with quorum sensing inhibitory activity from southern India. Microorganisms 2020;8:121.
10. Ettlinger L, Corbaz R, Hutter R. Species classification of the genus Streptomyces Waksman et Henrici. Experientia 1958;14:334-335.
11. Eftekharivah L, Hamedi J, Zarrini G, Bakhtiari R. Introducing acidophilic and acid tolerant actinobacteria as new sources of antimicrobial agents against Helicobacter pylori. Arch Razi Inst 2020; 76: 1-23.
12. Wink J. Compendium of Actinobacteria from Dr. Joachim M. Wink, University of Braunschweig, an electronic manual including the important bacterial group of the actinomycetes. 2012 Available online at: https://www.dsmz.de/collection/catalogue/microorganisms/special-groups-of-organisms/compendium-of-actinobacteria
13. Rostamza M, Noohi A, Hamedi J. Enhancement in production of erythromycin by Saccharopolyspora erythraea by the use of suitable industrial seeding media. DARU 2008;16:13-17.
14. Hamada M, Shibata C, Tamura T, Suzuki K-i. Agromyces marinus sp. nov., a novel actinobacterium isolated from sea sediment. J Antibiot (Tokyo) 2014;67:703-706.
15. Overbeek R, Olson R, Pusch GD, Olsen GJ, Davis JJ, Disz T, et al. The SEED and the rapid annotation of microbial genomes using subsystems technology (RAST). Nucleic Acids Res 2014;42: D206-D214.
16. Kumar S, Stecher G, Li M, Knyaz C, Tamura K. MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 2018;35:1547-1549.
17. Luo R, Liu B, Xie Y, Li Z, Huang W, Yuan J, et al. SOAPdenovo2: an empirically improved memory-efficient short-read de novo assembler. GigaScience 2012;1:18.
18. Andrews S. FastQC: a quality control tool for high throughput sequence data. Babraham Bioinformatics, Babraham Institute, Cambridge, United Kingdom; 2010. Available online at: http://www.bioinformatics.babraham.ac.uk/projects/fastqc
19. Besemer J, Lomsadze A, Borodovsky M. GeneMarkS: a self-training method for prediction of gene starts in microbial genomes. Implications for finding sequence motifs in regulatory regions. Nucleic Acids Res 2001;29:2607-2618.
20. Tarailo-Graovac M, Chen N. Using repeat masker to identify repetitive elements in genomic sequences. Curr Protoc Bioinformatics 2009;Chapter 4:Unit 4.10.
21. Benson G. Tandem repeats finder: a program to analyze DNA sequences. Nucleic Acids Res 1999;27:573-580.
22. Lowe TM, Chan PP. tRNAscan-SE On-line: integrating search and context for analysis of transfer RNA genes. Nucleic Acids Res 2016;44: W54-W57.
23. Lagesen K, Hallin P, Rødland EA, Stærfeldt H-H, Rognes T, Ussery DW. RNAmmer: consistent and rapid annotation of ribosomal RNA genes. Nucleic Acids Res 2007;35:3100-3108.
24. Griffiths-Jones S, Moxon S, Marshall M, Khanna A, Eddy SR, Bateman A. Rfam: annotating non-coding RNAs in complete genomes. Nucleic Acids Res 2005;33:D121-124.
25. Grissa I, Vergnaud G, Pourcel C. CRISPRFinder: a web tool to identify clustered regularly interspaced short palindromic repeats. Nucleic Acids Res 2007;35: W52-W57.
26. Aziz RK, Bartels D, Best AA, DeJongh M, Disz T, Edwards RA, et al. The RAST Server: rapid annotations using subsystems technology. BMC Genomics 2008;9:75.
27. Greenbaum DS (2004). Clusters of Orthologous Groups (COG), in Dictionary of Bioinformatics and Computational Biology. Ed, J Hancock and M Zvelebil, John Wiley & Sons, Inc.
28. Emms DM, Kelly S. OrthoFinder: solving fundamental biases in whole genome comparisons dramatically improves orthogroup inference accuracy. Genome Biol 2015;16:157.
29. Wang Y, Coleman-Derr D, Chen G, Gu YQ. OrthoVenn: a web server for genome wide comparison and annotation of orthologous clusters across multiple species. Nucleic Acids Res 2015;43:W78-84.
30. van Heel AJ, de Jong A, Song C, Viel JH, Kok J, Kuipers OP. BAGEL4: a user-friendly web server to thoroughly mine RiPPs and bacteriocins. Nucleic Acids Res 2018;46: W278-W281.
31. Blin K, Wolf T, Chevrette MG, Lu X, Schwalen CJ, Kautsar SA, et al. anti SMASH 4.0—improvements in chemistry prediction and gene cluster boundary identification. Nucleic Acids Res 2017;45:W36-W41.
32. Lounes A, Lebrihi A, Benslimane C, Lefebvre G, Germain P. Regulation of spiramycin synthesis in Streptomyces ambofaciens: effects of glucose and inorganic phosphate. Appl Microbiol Biotechnol 1996;45:204-211.
33. Santos-Beneit F, Rodriguez-Garcia A, Franco-Dominguez E, Martin JF. Phosphate-dependent regulation of the low-and high-affinity transport systems in the model actinomycete Streptomyces coelicolor. Microbiology 2008;154:2356-2370.
34. Barreiro C, Martínez-Castro M. Regulation of the phosphate metabolism in Streptomyces genus: impact on the secondary metabolites. Appl Microbiol Biotechnol 2019;103:1643-1658.
35. Dyson P (2011). Streptomyces: molecular biology and biotechnology: Horizon Scientific Press.
36. Nouwen N, Driessen AJ. Inactivation of protein translocation by cold-sensitive mutations in the yajC-secDF operon. J Bacteriol 2005;187:6852-6855.
37. Nakajo K, Iwami Y, Komori R, Ishikawa S, Ueno T, Suzuki Y. Resistance to acidic and alkaline environments in the endodontic pathogen Enterococcus faecalis. Oral Microbiol Immunol 2006;21: 283-288.
38. Gunnarsson N, Mortensen UH, Sosio M, Nielsen J. Identification of the Entner–Doudoroff pathway in an antibiotic producing actinomycete species. Mol Microbiol 2004;52:895-902.
39. Borodina I, Schöller C, Eliasson A, Nielsen J. Metabolic network analysis of Streptomyces tenebrarius, a Streptomyces species with an active Entner-Doudoroff pathway. Appl Environ Microbiol 2005;71:2294-2302.
40. Gunnarsson N, Bruheim P, Nielsen J. Glucose metabolism in the antibiotic producing actinomycete Nonomuraea sp. ATCC 39727. Biotechnol Bioeng 2004;88:652-663.
41. van Keulen G, Siebring J, Dijkhuizen L (2011). Central carbon metabolic pathways in Streptomyces. In: Streptomyces: Molecular Biology and Biotechnology. Ed, Dyson P. First ed. Caister Academic Press, Norfolk, UK, Vol. 1. pp. 105-124.
42. Ohnishi Y, Ishikawa J, Hara H, Suzuki H, Ikenoya M, Ikeda H, et al. Genome sequence of the streptomycin-producing microorganism Streptomyces griseus IFO 13350. J Bacteriol 2008;190:4050-4060.
43. Bentley SD, Chater KF, Cerdeño-Tárraga A-M, Challis GL, Thomson N, James KD, et al. Complete genome sequence of the model actinomycete Streptomyces coelicolor A3 (2). Nature 2002;417:141-147.
44. Viollier PH, Kelemen GH, Dale GE, Nguyen KT, Buttner MJ, Thompson CJ. Specialized osmotic stress response systems involve multiple SigB-like sigma factors in Streptomyces coelicolor. Mol Microbiol 2003;47:699-714.
45. Sadeghi A, Soltani BM, Nekouei MK, Jouzani GS, Mirzaei HH, Sadeghizadeh M. Diversity of the ectoines biosynthesis genes in the salt tolerant Streptomyces and evidence for inductive effect of ectoines on their accumulation. Microbiol Res 2014;169:699-708.
46. Van-Thuoc D, Hashim SO, Hatti-Kaul R, Mamo G. Ectoine-mediated protection of enzyme from the effect of pH and temperature stress: a study using Bacillus halodurans xylanase as a model. Appl Microbiol Biotechnol 2013;97:6271-6278.
47. Wang W, Qiu Z, Tan H, Cao L. Siderophore production by actinobacteria. Biometals 2014;27:623-631.
48. Dimkpa C, Merten D, Svatoš A, Büchel G, Kothe E. Siderophores mediate reduced and increased uptake of cadmium by Streptomyces tendae F4 and sunflower (Helianthus annuus), respectively. J Appl Microbiol 2009;107:1687-1696.
49. Imbert M, Béchet M, Blondeau R. Comparison of the main siderophores produced by some species of Streptomyces. Curr Microbiol 1995;31:129-133.
| Files | ||
| Issue | Vol 12 No 4 (2020) | |
| Section | Original Article(s) | |
| DOI | https://doi.org/10.18502/ijm.v12i4.3939 | |
| Keywords | ||
| Actinobacteria; Acid-tolerant; Alkaline-tolerant; Genome annotation; Genome sequencing; Genome mining; Streptomyces tendae | ||
| Rights and permissions | |
|
This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License. |
How to Cite
1.
Eftekharivash L, Hamedi J. Genome sequence and annotation of Streptomyces tendae UTMC 3329, acid and alkaline tolerant actinobacterium. Iran J Microbiol. 2020;12(4):343-352.
