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Volume 71, Issue 10

sp. nov., novel actinobacteria isolated from pine forest soil in Poland No Access

Abstract

The taxonomic status of two filamentous actinobacteria, isolates NF23 and NL8, recovered from the litter layer of a pine forest soil in Poland was established in a genome-based polyphasic study. The isolates showed a combination of chemotaxonomic, morphological and physiological properties associated with their classification in the genus . They formed a well supported lineage within the 16S rRNA gene tree and were most closely related to the type strains of (99.1%), (99.9 %) and (99.1 %), and like them, were found to have large genomes (10.8 and 11.5 Mbp, respectively). A phylogenomic tree based on the draft genomes of isolates NF23 and NL8 and their phylogenetic neighbours showed that they formed a distinct branch in the clade that was most closely related to DSM 111109. The isolates shared a combination of genomic, genotypic and phenotypic features, and had high average nucleotide index (ANI) and digital DNA:DNA hybridization (dDDH) similarities consistent with their assignment to the same species. The isolates were distinguished from the and strains by a wealth of taxonomic data and by low ANI (84.9–93.9 %) and dDDH (29.6–54.7 %) values. It is proposed that the isolates be classified in the genus as sp. nov. with isolate NL8 (=DSM 111110=PCM 3045) as the type strain. The genomes of strains NF23 and NL8 are rich in natural product-biosynthetic gene clusters hence these strains have the potential to synthesize new specialised metabolites.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): Catenulispora pinistramenti , forest soil , genomics , phylogeny and polyphasic taxonomy
Funding
This study was supported by the:
  • narodowe centrum nauki (Award 2016/23/N/NZ9/00247)
    • Principle Award Recipient: MagdalenaWypij
  • narodowe centrum nauki (Award 2017/01/X/NZ8/00140)
    • Principle Award Recipient: PatrycjaGolinska
© 2021 The Authors
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2021-10-21
2024-04-19
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References

  1. Goodfellow M, Williams ST. Ecology of actinomycetes. Annu Rev Microbiol 1983; 37:189–216 [View Article]
     [Google Scholar]
  2. Williams ST, Lanning S, Wellington EMH. Ecology of actinomycetes. Goodfellow M, Mordarski M, Williams ST. eds In The Biology of the Actinomycetes London: Academic Press; 1984 pp 481–528
     [Google Scholar]
  3. Poomthongdee N, Duangmal K, Pathom-aree W. Acidophilic actinomycetes from rhizosphere soil: diversity and properties beneficial to plants. J Antibiot 2015; 68:106–114 [View Article]
     [Google Scholar]
  4. Tamreihao K, Nimaichand S, Ningthoujam DS. Use of acidophilic or acidotolerant actinobacteria for sustainable agricultural production in acidic soils. Egamberdieva D, Birkeland NK, Panosyan H, Li WJ. eds In Extremophiles in Eurasian Ecosystems Vol 8 Singapore: Springer; 2018 pp 453–464
     [Google Scholar]
  5. Donadio S, Cavaletti L, Monciardini P. Order IV. Catenulisporales ord. Nov. Goodfellow M, Kämpfer P, Busse H-. J, Trujillo ME. eds In Bergey’s Manual of systematic Bacteriology, 2nd. edn New York: Springer; 2012 p 225
     [Google Scholar]
  6. Busti E, Cavaletti L, Monciardini P, Schumann P, Rohde M et al. Catenulispora acidiphila gen. nov., sp. nov., a novel, mycelium-forming actinomycete, and proposal of Catenulisporaceae fam. nov. Int J Syst Evol Microbiol 2006; 56:1741–1746 [View Article] [PubMed]
     [Google Scholar]
  7. Cavaletti L, Monciardini P, Schumann P, Rohde M, Bamonte R et al. Actinospica robiniae gen. nov., sp. nov. and Actinospica acidiphila sp. nov.: proposal for Actinospicaceae fam. nov. and Catenulisporinae subord. nov. in the order Actinomycetales . Int J Syst Evol Microbiol 2006; 56:1747–1753 [View Article] [PubMed]
     [Google Scholar]
  8. Kim JJ, Marjerrison CE, Cornish Shartau SL, Brady AL, Sharp CE et al. Actinocrinis puniceicyclus gen. nov., sp. nov., an actinobacterium isolated from an acidic spring. Int J Syst Evol Microbiol 2017; 67:602–609 [View Article] [PubMed]
     [Google Scholar]
  9. Baltz RH. Gifted microbes for genome mining and natural product discovery. J Ind Microbiol Biotechnol 2017; 44:573–588 [View Article] [PubMed]
     [Google Scholar]
  10. Baltz RH. Natural product drug discovery in the genomic era: realities, conjectures, misconceptions, and opportunities. J Ind Microbiol Biotechnol 2019; 46:281–299 [View Article] [PubMed]
     [Google Scholar]
  11. Kusuma AB. Microbiology of Indonesian Extremobiospheres: from Unexplored Actinobacterial Diversity to Novel Antimicrobial Discovery. Ph.D. Thesis Newcastle University; Newcastle upon Tyne. UK: 2020
     [Google Scholar]
  12. Świecimska M, Golińska P, Wypij M, Goodfellow M. Genomic-based classification of Catenulispora pinisilvae sp. nov., novel actinobacteria isolated from a pine forest soil in Poland and emended description of Catenulispora rubra . Syst Appl Microbiol 2021; 44:S0723-2020(20)30119-3 [View Article] [PubMed]
     [Google Scholar]
  13. Wang H, van der Donk WA. Biosynthesis of the class III lantipeptide catenulipeptin. ACS Chem Biol 2012; 7:1529–1535 [View Article] [PubMed]
     [Google Scholar]
  14. Zettler J, Xia H, Burkard N, Kulik A, Grond S et al. New aminocoumarins from the rare actinomycete Catenulispora acidiphila DSM 44928T: identification, structure elucidation, and heterologous production. Chem Bio Chem 2014; 15:612–621 [View Article] [PubMed]
     [Google Scholar]
  15. Nouioui I, Carro L, García-López M, Meier-Kolthoff JP, Woyke T et al. Genome-based taxonomic classification of the phylum Actinobacteria. Front Microbiol 2018; 9:2007 [View Article]
     [Google Scholar]
  16. Lee HJ, Whang KS. Catenulispora fulva sp. nov., isolated from forest soil. Int J Syst Evol Microbiol 2016; 66:271–275 [View Article] [PubMed]
     [Google Scholar]
  17. Tamura T, Ishida Y, Sakane T, Suzuki K. Catenulispora rubra sp. nov., an acidophilic actinomycete isolated from forest soil. Int J Syst Evol Microbiol 2007; 57:2272–2274 [View Article] [PubMed]
     [Google Scholar]
  18. Lee HJ, Han SI, Whang KS. Catenulispora graminis sp. nov., a rhizobacterium from bamboo (Phyllostachys nigro var. Int J Syst Evol Microbiol 2012; 62:2589–2592 [View Article] [PubMed]
     [Google Scholar]
  19. Tamura T, Ishida Y, Otoguro M, Suzuki K. Catenulispora subtropica sp. nov. and Catenulispora yoronensis sp. nov. Int J Syst Evol Microbiol 2008; 58:1552–1555 [View Article] [PubMed]
     [Google Scholar]
  20. Goodfellow M, Hill IR, Gray TRG. Bacteria in a pine forest soil. Gray TRG, Parkinson D. eds In The Ecology of Soil Bacteria Liverpool: University Press; 1967 pp 500–515
     [Google Scholar]
  21. Küster E, Williams S. Selection of media for isolation of streptomycetes. Nature 1964; 202:928–929 [View Article] [PubMed]
     [Google Scholar]
  22. Golińska P, Dahm H, Goodfellow M. Streptacidophilus toruniensis sp. nov., isolated from a pine forest soil. Antonie van Leeuwenhoek 2016; 109:1583–1591 [View Article] [PubMed]
     [Google Scholar]
  23. Shirling EB, Gottlieb D. Methods for characterization of Streptomyces species. Int J Syst Bacteriol 1966; 16:313–340 [View Article]
     [Google Scholar]
  24. Jones KI. Fresh isolates of actinomycetes in which the presence of sporogenous aerial mycelia is a fluctuating characteristic. J Bacteriol 1949; 57:141–145 [View Article] [PubMed]
     [Google Scholar]
  25. Harris JL. Modified method for fungal slide culture. J Clin Microbiol 1986; 9:460–461 [View Article]
     [Google Scholar]
  26. Kelly KL. Centroid notations for the revised ISCC-NBS color name blocks. J RES NATL BUR STAN 1958; 61:427–431 [View Article]
     [Google Scholar]
  27. Staneck JL, Roberts GD. Simplified approach to identification of aerobic actinomycetes by thin-layer chromatography. Appl Microbiol 1974; 28:226–231 [View Article] [PubMed]
     [Google Scholar]
  28. Hasegawa T, Takizawa M, Tanida S. A rapid analysis for chemical grouping of aerobic actinomycetes. J Gen Appl Microbiol 1983; 29:319–322 [View Article]
     [Google Scholar]
  29. Minnikin DE, O’Donnell AG, Goodfellow M, Alderson G, Athalye M et al. An integrated procedure for the extraction of bacterial isoprenoid quinones and polar lipids. J Microbiol Methods 1984; 2:233–241 [View Article]
     [Google Scholar]
  30. Kroppenstedt RM. Fatty acids and menaquinones of actinomycetes and related organisms. Goodfellow M, Minnikin DE. eds In Chemical Methods in Bacterial Systematics London: Academic Press; 1985 pp 173–200
     [Google Scholar]
  31. Sasser M. Identification of Bacteria by Gas Chromatography of Cellular Fatty Acids, MIDI Technical Note 101. Newark: MIDI Inc; 1990
     [Google Scholar]
  32. Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 2014; 30:2114–2120 [View Article] [PubMed]
     [Google Scholar]
  33. Nurk S, Bankevich A, Antipov D, Gurevich A, Korobeynikov A et al. Assembling genomes and mini-metagenomes from highly chimeric reads. In Deng M, Jiang R, Sun F, Zhang X. eds Research in Computational Molecular Biology. RECOMB 2013. Lecture Notes in Computer Science vol. 7821 Berlin, Heidelberg: Springer; 2013 pp 158–170
     [Google Scholar]
  34. Aziz RK, Bartels D, Best AA, DeJongh M, Disz T. The RAST Server: rapid annotations using subsystems technology. BMC Genomics 2008; 9:75 [View Article]
     [Google Scholar]
  35. Seemann T. Prokka: rapid prokaryotic genome annotation. Bioinformatics 2014; 30:2068–2069 [View Article] [PubMed]
     [Google Scholar]
  36. Aziz RK, Devoid S, Disz T, Edwards RA, Henry CS et al. SEED servers: high-performance access to the SEED genomes, annotations, and metabolic models. PLoS One 2012; 7:e48053 [View Article] [PubMed]
     [Google Scholar]
  37. Yoon SH, Ha SM, Kwon S, Lim J, Kim Y et al. Introducing EzBioCloud: a taxonomically united database of 16S rRNA and whole genome assemblies. Int J Syst Evol Microbiol 2017; 67:1613–1617 [View Article] [PubMed]
     [Google Scholar]
  38. Meier-Kolthoff JP, Göker M, Spröer C, Klenk H-P. When should a DDH experiment be mandatory in microbial taxonomy. Arch Microbiol 2013; 195:413–418 [View Article] [PubMed]
     [Google Scholar]
  39. Edgar RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 2004; 32:1792–1797 [View Article] [PubMed]
     [Google Scholar]
  40. Stamatakis A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 2014; 30:1312–1313 [View Article] [PubMed]
     [Google Scholar]
  41. Pattengale ND, Alipour M, Bininda-Emonds OR, Moret BM, Stamatakis A. How many bootstrap replicates are necessary. J Comput Biol 2010; 17:337–354 [View Article] [PubMed]
     [Google Scholar]
  42. Goloboff PA, Farris JS, Nixon KC. TNT, a free program for phylogenetic analysis. Cladistics 2008; 24:774–786 [View Article]
     [Google Scholar]
  43. PAUP SD. Phylogenetic Analysis Using Parsimony (* and other methods), version 4 Sunderland, MA: Sinauer Associates; 2002
     [Google Scholar]
  44. Kumar S, Stecher G, Tamura K. MEGA7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets. Mol Biol Evol 2016; 33:1870–1874 [View Article] [PubMed]
     [Google Scholar]
  45. Saitou N, Nei M. The neighbour-joining method: A new method for constructing phylogenetic trees. Mol Biol Evol 1987; 4:406–425 [View Article] [PubMed]
     [Google Scholar]
  46. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA et al. Clustal W and Clustal X version 2.0. Bioinformatics 2007; 23:2947–2948 [View Article]
     [Google Scholar]
  47. Felsenstein J. Confidence limits on phylogenies: an approach using the bootstrap. Evolution 1985; 39:383–391 [View Article]
     [Google Scholar]
  48. Kimura M. A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 1980; 16:111–120 [View Article] [PubMed]
     [Google Scholar]
  49. Stackebrandt E, Goebel BM. Taxonomic note: a place for DNA-DNA reassociation and 16S rRNA sequence analysis in the present species definition in bacteriology. Int J Syst Bacteriol 1994; 44:846–849
     [Google Scholar]
  50. Stackebrandt E, Ebers J. Taxonomic parameters revisited: tarnished gold standards. Microbiol Today 2006; 33:152–155
     [Google Scholar]
  51. Meier-Kolthoff JP, Auch AF, Klenk HP, Göker M. Genome sequence based species delimitations with constant intervals and improved distance functions. BMC Bioinformatics 2013; 14:60 [View Article] [PubMed]
     [Google Scholar]
  52. Kim M, Oh H-S, Park S-C, Chun J. Towards a taxonomic coherence between average nucleotide identity and 16S rRNA gene sequence similarity for species demarcation of prokaryotes. Int J Syst Evol Microbiol 2014; 64:346–351 [View Article] [PubMed]
     [Google Scholar]
  53. 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]
  54. Ondov BD, Treangen TJ, Melsted P, Mallonee AB, Bergman NH et al. Mash: fast genome and metagenome distance estimation using MinHash. Genome Biol 2016; 17:1–14 [View Article]
     [Google Scholar]
  55. 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]
  56. Farris JS. Estimating phylogenetic trees from distance matrices. Am Nat 1972; 106:645–667 [View Article]
     [Google Scholar]
  57. Versalovic J, Schneider M, De Bruijn FJ, Lupski JR. Genomic fingerprinting of bacteria using repetitive sequence-based polymerase chain reaction. Methods Mol Cell Biol 1994; 5:25–40
     [Google Scholar]
  58. Trujillo ME, Alonso-Vega P, Rodríguez R, Carro L, Cerda E et al. The genus Micromonospora is widespread in legume root nodules: the example of Lupinus angustifolius. ISME J 2010; 4:1265–1281 [View Article] [PubMed]
     [Google Scholar]
  59. Yoon SH, Ha SM, Lim J, Kwon S, Chun J. A large-scale evaluation of algorithms to calculate average nucleotide identity. Antonie van Leeuwenhoek 2017; 110:1281–1286 [View Article] [PubMed]
     [Google Scholar]
  60. Wayne LG, Brenner DJ, Colwell RR, Grimont PAD, Kandler O et al. Report of the ad hoc committee on reconciliation of approaches to bacterial systematics. Int J Syst Evol Microbiol 1987; 37:463–464 [View Article]
     [Google Scholar]
  61. Chun J, Oren A, Ventosa A, Christensen H, Arahal DR et al. Proposed minimal standards for the use of genome data for the taxonomy of prokaryotes. Int J Syst Microbiol 2018; 68:461–466 [View Article]
     [Google Scholar]
  62. Blin K, Shaw S, Steinke K, Villebro R, Ziemert N et al. antiSMASH 5.0: updates to the secondary metabolite genome mining pipeline. Nucleic Acids Res 2019; 47:W81–W87 [View Article] [PubMed]
     [Google Scholar]
  63. Williams ST, Goodfellow M, Alderson G, Wellington EMH, Sneath PHA et al. Numerical classification of Streptomyces and related genera. J Gen Microbiol 1983; 129:1743–1813 [View Article] [PubMed]
     [Google Scholar]
  64. Murray PR, Boron EJ, Pfaller MA, Tenover FC, Yolken RH. Manual of Clinical Microbiology, 7th edn. Washington, DC: ASM Press; 1999
     [Google Scholar]
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Catenulispora pinistramenti sp. nov., novel actinobacteria isolated from pine forest soil in Poland
Int J Syst Evol Microbiol 71, 005063 (2021); https://doi.org/10.1099/ijsem.0.005063
/content/journal/ijsem/10.1099/ijsem.0.005063
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