1887

Abstract

Six bacterial strains, Mut1, Mut2, Alt1, Alt2, Alt3, and Alt4, were isolated from soil samples collected in parks in Gothenburg, Sweden, based on their ability to utilize the insoluble polysaccharides α−1,3-glucan (mutan; Mut strains) or the mixed-linkage α−1,3/α−1,6-glucan (alternan; Alt strains). Analysis of 16S rRNA gene sequences identified all strains as members of the genus . The genomes of the strains were sequenced and subsequent phylogenetic analyses identified Mut2 as a strain of and Alt1, Alt2 and Alt4 as strains of while Mut1 and Alt3 were most closely related to the type strains NBRC 101007 and NRRL ISP-5137, respectively. Comprehensive genomic and biochemical characterizations were conducted, highlighting typical features of , such as large genomes (8.0–9.6 Mb) with high G+C content (70.5–72.0%). All six strains also encode a wide repertoire of putative carbohydrate-active enzymes, indicating a capability to utilize various complex polysaccharides as carbon sources such as starch, mutan, and cellulose, which was confirmed experimentally. Based on phylogenetic and phenotypic characterization, our study suggests that strains Mut1 and Alt3 represent novel species in the genus for which the names sp. nov. and sp. nov. are proposed, with strains Mut1 (=DSM 117248=CCUG 77596) and Alt3 (=DSM 117252=CCUG 77600) representing the respective type strains.

Funding
This study was supported by the:
  • Adlerbertska Stiftelserna
    • Principle Award Recipient: ToveWidén
  • Adlerbertska Stiftelserna
    • Principle Award Recipient: JohanLarsbrink
  • Novo Nordisk Fonden (Award NNF20CC0035580)
    • Principle Award Recipient: EduardJ. Kerkhoven
  • Vetenskapsrådet (Award Dnr 2020-03618)
    • Principle Award Recipient: JohanLarsbrink
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License.
Loading

Article metrics loading...

/content/journal/ijsem/10.1099/ijsem.0.006514
2024-09-12
2024-11-10
Loading full text...

Full text loading...

/deliver/fulltext/ijsem/74/9/ijsem006514.html?itemId=/content/journal/ijsem/10.1099/ijsem.0.006514&mimeType=html&fmt=ahah

References

  1. Parte AC, Sardà Carbasse J, Meier-Kolthoff JP, Reimer LC, Göker M. List of Prokaryotic names with Standing in Nomenclature (LPSN) moves to the DSMZ. Int J Syst Evol Microbiol 2020; 70:5607–5612 [View Article] [PubMed]
    [Google Scholar]
  2. Nikolaidis M, Hesketh A, Frangou N, Mossialos D, Van de Peer Y et al. A panoramic view of the genomic landscape of the genus Streptomyces. Microb Genom 2023; 9:1028 [View Article] [PubMed]
    [Google Scholar]
  3. Chater KF, Biró S, Lee KJ, Palmer T, Schrempf H. The complex extracellular biology of Streptomyces. FEMS Microbiol Rev 2010; 34:171–198 [View Article] [PubMed]
    [Google Scholar]
  4. Kieser T, Bibb MJ, Buttner MJ, Chater KF, Hopwood DA. Practical Streptomyces Genetics Norwich: Innes; 2000
    [Google Scholar]
  5. Chater KF. Recent advances in understanding Streptomyces. F1000Res 2016; 5:2795 [View Article]
    [Google Scholar]
  6. Spasic J, Mandic M, Djokic L, Nikodinovic-Runic J. Streptomyces spp. in the biocatalysis toolbox. Appl Microbiol Biotechnol 2018; 102:3513–3536 [View Article] [PubMed]
    [Google Scholar]
  7. Pradeep GC, Choi YH, Choi YS, Suh SE, Seong JH et al. An extremely alkaline novel chitinase from Streptomyces sp. CS495. Process Biochem 2014; 49:223–229 [View Article]
    [Google Scholar]
  8. Beg QK, Bhushan B, Kapoor M, Hoondal GS. Production and characterization of thermostable xylanase and pectinase from Streptomyces sp. QG-11-3. J Ind Microbiol Biotechnol 2000; 24:396–402 [View Article]
    [Google Scholar]
  9. Grigorevski de Lima AL, Pires do Nascimento R, da Silva Bon EP, Coelho RRR. Streptomyces drozdowiczii cellulase production using agro-industrial by-products and its potential use in the detergent and textile industries. Enzyme Microb Technol 2005; 37:272–277 [View Article]
    [Google Scholar]
  10. Drula E, Garron M-L, Dogan S, Lombard V, Henrissat B et al. The carbohydrate-active enzyme database: functions and literature. Nucleic Acids Res 2022; 50:D571–D577 [View Article] [PubMed]
    [Google Scholar]
  11. Simpson CL, Cheetham NWH, Jacques NA. Four glucosyltransferases, GtfJ, GtfK, GtfL and GtfM, from Streptococcus salivarius ATCC 25975. Microbiology 1995; 141:1451–1460 [View Article] [PubMed]
    [Google Scholar]
  12. Koo H, Falsetta ML, Klein MI. The exopolysaccharide matrix: a virulence determinant of cariogenic biofilm. J Dent Res 2013; 92:1065–1073 [View Article] [PubMed]
    [Google Scholar]
  13. Fuglsang CC, Berka RM, Wahleithner JA, Kauppinen S, Shuster JR et al. Biochemical analysis of recombinant fungal mutanases. A new family of alpha1,3-glucanases with novel carbohydrate-binding domains. J Biol Chem 2000; 275:2009–2018 [View Article] [PubMed]
    [Google Scholar]
  14. Yano S, Wakayama M, Tachiki T. Cloning and expression of an alpha-1,3-glucanase gene from Bacillus circulans KA-304: the enzyme participates in protoplast formation of Schizophyllum commune. Biosci Biotechnol Biochem 2006; 70:1754–1763 [View Article] [PubMed]
    [Google Scholar]
  15. Suyotha W, Yano S, Itoh T, Fujimoto H, Hibi T et al. Characterization of α-1,3-glucanase isozyme from Paenibacillus glycanilyticus FH11 in a new subgroup of family 87 α-1,3-glucanase. J Biosci Bioeng 2014; 118:378–385 [View Article] [PubMed]
    [Google Scholar]
  16. Itoh T, Panti N, Hayashi J, Toyotake Y, Matsui D et al. Crystal structure of the catalytic unit of thermostable GH87 α-1,3-glucanase from Streptomyces thermodiastaticus strain HF3-3. Biochem Biophys Res Commun 2020; 533:1170–1176 [View Article] [PubMed]
    [Google Scholar]
  17. Okazaki K, Amano T, Morimoto T, Iemoto T, Kawabata T et al. Cloning and nucleotide sequence of the mycodextranase gene from Streptomyces sp. J-13-3. Biosci Biotechnol Biochem 2001; 65:1684–1687 [View Article] [PubMed]
    [Google Scholar]
  18. Leathers TD, Nunnally MS, Côté GL. Modification of alternan by dextranase. Biotechnol Lett 2009; 31:289–293 [View Article] [PubMed]
    [Google Scholar]
  19. Park T-S, Jeong HJ, Ko J-A, Ryu YB, Park S-J et al. Biochemical characterization of thermophilic dextranase from a thermophilic bacterium, Thermoanaerobacter pseudethanolicus. J Microbiol Biotechnol 2012; 22:637–641 [View Article] [PubMed]
    [Google Scholar]
  20. Sandoval-Powers M, Králová S, Nguyen G-S, Fawwal DV, Degnes K et al. Streptomyces poriferorum sp. nov., a novel marine sponge-derived Actinobacteria species expressing anti-MRSA activity. Syst Appl Microbiol 2021; 44:126244 [View Article] [PubMed]
    [Google Scholar]
  21. Zucchi TD, Kim B-Y, Kshetrimayum JD, Weon H-Y, Kwon S-W et al. Streptomyces brevispora sp. nov. and Streptomyces laculatispora sp. nov., actinomycetes isolated from soil. Int J Syst Evol Microbiol 2012; 62:478–483 [View Article] [PubMed]
    [Google Scholar]
  22. Puanglek S, Kimura S, Enomoto-Rogers Y, Kabe T, Yoshida M et al. In vitro synthesis of linear α-1,3-glucan and chemical modification to ester derivatives exhibiting outstanding thermal properties. Sci Rep 2016; 6:30479 [View Article] [PubMed]
    [Google Scholar]
  23. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol 1990; 215:403–410 [View Article] [PubMed]
    [Google Scholar]
  24. De Coster W, D’Hert S, Schultz DT, Cruts M, Van Broeckhoven C. NanoPack: visualizing and processing long-read sequencing data. Bioinformatics 2018; 34:2666–2669 [View Article] [PubMed]
    [Google Scholar]
  25. Lin Y, Yuan J, Kolmogorov M, Shen MW, Chaisson M et al. Assembly of long error-prone reads using de Bruijn graphs. Proc Natl Acad Sci USA 2016; 113:E8396–E8405 [View Article] [PubMed]
    [Google Scholar]
  26. Wick RR, Schultz MB, Zobel J, Holt KE. Bandage: interactive visualization of de novo genome assemblies. Bioinformatics 2015; 31:3350–3352 [View Article] [PubMed]
    [Google Scholar]
  27. Parks DH, Imelfort M, Skennerton CT, Hugenholtz P, Tyson GW. CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes. Genome Res 2015; 25:1043–1055 [View Article] [PubMed]
    [Google Scholar]
  28. Chaumeil P-A, Mussig AJ, Hugenholtz P, Parks DH. GTDB-Tk: a toolkit to classify genomes with the Genome Taxonomy Database. Bioinformatics 2020; 36:1925–1927 [View Article]
    [Google Scholar]
  29. Parks DH, Chuvochina M, Chaumeil P-A, Rinke C, Mussig AJ et al. A complete domain-to-species taxonomy for bacteria and archaea. Nat Biotechnol 2020; 38:1079–1086 [View Article] [PubMed]
    [Google Scholar]
  30. Schwengers O, Jelonek L, Dieckmann M, Beyvers S, Blom J et al. Bakta: rapid & standardized annotation of bacterial genomes via alignment-free sequence identification. Bioinformatics 2021; 7685 [View Article]
    [Google Scholar]
  31. Lipun K, Chantavorakit T, Mingma R, Duangmal K. Streptomyces acidicola sp. nov., isolated from a peat swamp forest in Thailand. J Antibiot 2020; 73:435–440 [View Article] [PubMed]
    [Google Scholar]
  32. Caicedo-Montoya C, Manzo-Ruiz M, Ríos-Estepa R. Pan-genome of the genus Streptomyces and prioritization of biosynthetic gene clusters with potential to produce antibiotic compounds. Front Microbiol 2021; 12:677558 [View Article] [PubMed]
    [Google Scholar]
  33. Yoon S-H, Ha S-M, Kwon S, Lim J, Kim Y 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 [View Article] [PubMed]
    [Google Scholar]
  34. Saitou N, Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 1987; 4:406–425 [View Article] [PubMed]
    [Google Scholar]
  35. Tamura K, Stecher G, Kumar S. MEGA11: Molecular Evolutionary Genetics Analysis version 11. Mol Biol Evol 2021; 38:3022–3027 [View Article] [PubMed]
    [Google Scholar]
  36. Madhaiyan M, Saravanan VS, See-Too W-S, Volpiano CG, Sant’Anna FH et al. Genomic and phylogenomic insights into the family Streptomycetaceae lead to the proposal of six novel genera. Int J Syst Evol Microbiol 2022; 72:005570 [View Article] [PubMed]
    [Google Scholar]
  37. Felsenstein J. Confidence limits on phylogenies: an approach using the bootstrap. Evolution 1985; 39:783–791 [View Article] [PubMed]
    [Google Scholar]
  38. Tamura K, Nei M, Kumar S. Prospects for inferring very large phylogenies by using the neighbor-joining method. Proc Natl Acad Sci USA 2004; 101:11030–11035 [View Article] [PubMed]
    [Google Scholar]
  39. Meier-Kolthoff JP, Göker M. TYGS is an automated high-throughput platform for state-of-the-art genome-based taxonomy. Nat Commun 2019; 10:2182 [View Article] [PubMed]
    [Google Scholar]
  40. Meier-Kolthoff JP, Auch AF, Klenk H-P, Göker M. Genome sequence-based species delimitation with confidence intervals and improved distance functions. BMC Bioinform 2013; 14:60 [View Article] [PubMed]
    [Google Scholar]
  41. Riesco R, Trujillo ME. Update on the proposed minimal standards for the use of genome data for the taxonomy of prokaryotes. Int J Syst Evol Microbiol 2024; 74:006300 [View Article] [PubMed]
    [Google Scholar]
  42. Komaki H. Resolution of housekeeping gene sequences used in MLSA for the genus Streptomyces and reclassification of Streptomyces anthocyanicus and Streptomyces tricolor as heterotypic synonyms of Streptomyces violaceoruber. Int J Syst Evol Microbiol 2022; 72: [View Article]
    [Google Scholar]
  43. Labeda DP, Dunlap CA, Rong X, Huang Y, Doroghazi JR et al. Phylogenetic relationships in the family Streptomycetaceae using multi-locus sequence analysis. Antonie van Leeuwenhoek 2017; 110:563–583 [View Article] [PubMed]
    [Google Scholar]
  44. Meier-Kolthoff JP, Carbasse JS, Peinado-Olarte RL, Göker M. TYGS and LPSN: a database tandem for fast and reliable genome-based classification and nomenclature of prokaryotes. Nucleic Acids Res 2022; 50:D801–D807 [View Article]
    [Google Scholar]
  45. Richter M, Rosselló-Móra R, Oliver Glöckner F, Peplies J. JSpeciesWS: a web server for prokaryotic species circumscription based on pairwise genome comparison. Bioinformatics 2016; 32:929–931 [View Article] [PubMed]
    [Google Scholar]
  46. Hu S, Li K, Zhang Y, Wang Y, Fu L et al. New insights into the threshold values of multi-locus sequence analysis, average nucleotide identity and digital DNA-DNA hybridization in delineating Streptomyces species. Front Microbiol 2022; 13:910277 [View Article] [PubMed]
    [Google Scholar]
  47. Chevrette MG, Carlson CM, Ortega HE, Thomas C, Ananiev GE et al. The antimicrobial potential of Streptomyces from insect microbiomes. Nat Commun 2019; 10:516 [View Article] [PubMed]
    [Google Scholar]
  48. Andam CP, Doroghazi JR, Campbell AN, Kelly PJ, Choudoir MJ et al. A latitudinal diversity gradient in terrestrial bacteria of the genus Streptomyces. mBio 2016; 7:e02200-15 [View Article] [PubMed]
    [Google Scholar]
  49. Blin K, Shaw S, Augustijn HE, Reitz ZL, Biermann F et al. antiSMASH 7.0: new and improved predictions for detection, regulation, chemical structures and visualisation. Nucleic Acids Res 2023; 51:W46–W50 [View Article] [PubMed]
    [Google Scholar]
  50. Shirling EB, Gottlieb D. Methods for characterization of Streptomyces species. Int J Syst Bacteriol 1966; 16:313–340 [View Article]
    [Google Scholar]
  51. Kitts PA, Church DM, Thibaud-Nissen F, Choi J, Hem V et al. Assembly: a resource for assembled genomes at NCBI. Nucleic Acids Res 2016; 44:D73–80 [View Article] [PubMed]
    [Google Scholar]
  52. Lefort V, Desper R, Gascuel O. FastME 2.0: a comprehensive, accurate, and fast distance-based phylogeny inference program. Mol Biol Evol 2015; 32:2798–2800 [View Article] [PubMed]
    [Google Scholar]
  53. Semêdo LTAS, Gomes RC, Linhares AA, Duarte GF, Nascimento RP et al. Streptomyces drozdowiczii sp. nov., a novel cellulolytic streptomycete from soil in Brazil. Int J Syst Evol Microbiol 2004; 54:1323–1328 [View Article] [PubMed]
    [Google Scholar]
  54. Shirling EB, Gottlieb D. Cooperative description of type cultures of Streptomyces.: II. Species descriptions from first study. Int J Syst Bacteriol 1968; 18:69–189 [View Article]
    [Google Scholar]
  55. Reimer LC, Sarda Carbasse J, Koblitz J, Podstawka A, Overmann J. Streptomyces drozdowiczii (Semêdo et al. 2004).
  56. Reimer LC, Sarda Carbasse J, Koblitz J, Podstawka A, Overmann J. Streptomyces atroolivaceus (Preobrazhenskaya et al. 1957) Pridham et al. 1958 emend. Nouioui et al. 2018.
  57. Reimer LC, Sardà Carbasse J, Koblitz J, Ebeling C, Podstawka A et al. BacDive in 2022: the knowledge base for standardized bacterial and archaeal data. Nucleic Acids Res 2022; 50:D741–D746 [View Article] [PubMed]
    [Google Scholar]
/content/journal/ijsem/10.1099/ijsem.0.006514
Loading
/content/journal/ijsem/10.1099/ijsem.0.006514
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error