1887

Abstract

The taxonomic position of three actinobacterial strains, BCCO 10_0061, BCCO 10_0798, and BCCO 10_0856, recovered from bare soil in the Sokolov Coal Basin, Czech Republic, was established using a polyphasic approach. The multilocus sequence analysis based on 100 single-copy genes positioned BCCO 10_0061 in the same cluster as , strain BCCO 10_0798 in the same cluster as , , , and , and strain BCCO 10_0856 clustered together with and . Morphological and chemotaxonomic characteristics of these strains support their assignment to the genus . In all three strains, MK-9(H) accounted for more than 80 % of the isoprenoid quinone. The diagnostic diamino acid in the cell-wall peptidoglycan was -diaminopimelic acid. The whole-cell sugars were rhamnose, ribose, mannose, glucose, and galactose. The major fatty acids (>10 %) were iso-C, anteiso-C, iso-C, and C. The polar lipids were diphosphatidylglycerol, methyl-phosphatidylethanolamine, phosphatidylethanolamine, hydroxy-phosphatidylethanolamine, phosphatidylglycerol, and phosphatidylinositol. The genomic DNA G+C content of strains (mol%) was 68.8 for BCCO 10_0061, 69.2 for BCCO 10_0798, and 68.5 for BCCO 10_0856. The combination of digital DNA–DNA hybridization results, average nucleotide identity values and phenotypic characteristics of BCCO 10_0061, BCCO 10_0798, and BCCO 10_0856 distinguishes them from their closely related strains. Bioinformatic analysis of the genome sequences of the strains revealed several biosynthetic gene clusters (BGCs) with identities >50 % to already known clusters, including BGCs for geosmin, coelichelin, ε-poly--lysine, and erythromycin-like BGCs. Most of the identified BGCs showed low similarity to known BGCs (<50 %) suggesting their genetic potential for the biosynthesis of novel secondary metabolites. Based on the above results, each strain represents a novel species of the genus , for which we propose the name sp. nov. for BCCO 10_0061 (=DSM 116175), sp. nov. for BCCO 10_0798 (=DSM 116176), and sp. nov. for BCCO 10_0856 (=DSM 116177).

Funding
This study was supported by the:
  • Leibniz Association through the Collaborative Excellence (Award K445/2022)
    • Principle Award Recipient: YvonneMast
  • Deutsches Zentrum für Infektionsforschung (Award TTU 09.819)
    • Principle Award Recipient: YvonneMast
  • Ministerstvo školství, mládeže a tělovýchovy České republiky (Award OP VVV CZ.02.2.69/0.0/0.0/18_054/0014649, ABERA - Anchoring the Biological Centre AV ČR, v. v. i. in the European Research Area)
    • Principle Award Recipient: ApplicableNot
  • Ministerstvo školství, mládeže a tělovýchovy České republiky (Award OP VVV CZ.02.1.01/0.0/0.0/18_046/0016045 and Czech-BioImaging LM2023050)
    • Principle Award Recipient: ApplicableNot
  • Akademie věd České republiky (Award Strategie AV21)
    • Principle Award Recipient: ChroňákováAlica
  • Ministerstvo Zdravotnictví České Republiky (Award No. 17-30091A)
    • Principle Award Recipient: ChroňákováAlica
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License. This article was made open access via a Publish and Read agreement between the Microbiology Society and the corresponding author’s institution.
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2024-04-17
2024-04-30
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References

  1. Yassin AF, Rainey FA, Brzezinka H, Jahnke KD, Weissbrodt H et al. Lentzea gen. nov., a new genus of the order Actinomycetales. Int J Syst Bacteriol 1995; 45:357–363 [View Article] [PubMed]
    [Google Scholar]
  2. 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]
  3. Goodfellow M, Nouioui I, Sanderson R, Xie F, Bull AT. Rare taxa and dark microbial matter: novel bioactive actinobacteria abound in Atacama Desert soils. Antonie Van Leeuwenhoek 2018; 111:1315–1332 [View Article] [PubMed]
    [Google Scholar]
  4. González-Salazar LA, Quezada M, Rodríguez-Orduña L, Ramos-Aboites H, Capon RJ et al. Biosynthetic novelty index reveals the metabolic potential of rare actinobacteria isolated from highly oligotrophic sediments. Microb Genom 2023; 9:mgen000921 [View Article] [PubMed]
    [Google Scholar]
  5. Maiti PK, Mandal S. Comprehensive genome analysis of Lentzea reveals repertoire of polymer-degrading enzymes and bioactive compounds with clinical relevance. Sci Rep 2022; 12:8409 [View Article] [PubMed]
    [Google Scholar]
  6. Wichner D, Idris H, Houssen WE, McEwan AR, Bull AT et al. Isolation and anti-HIV-1 integrase activity of lentzeosides A–F from extremotolerant lentzea sp. H45, a strain isolated from a high-altitude Atacama Desert soil. J Antibiot 2017; 70:448–453 [View Article]
    [Google Scholar]
  7. Li C, Hu Y, Wu X, Stumpf SD, Qi Y et al. Discovery of unusual dimeric piperazyl cyclopeptides encoded by a Lentzea flaviverrucosa DSM 44664 biosynthetic supercluster. Proc Natl Acad Sci USA 2022; 119:e2117941119 [View Article] [PubMed]
    [Google Scholar]
  8. Ping M, Yun-Lin Z, Jun L, Jian G, Zheng-Gang X. Proposal of Lentzea deserti (Okoro et al. 2010) Nouioui et al. 2018 as a later heterotypic synonym of Lentzea atacamensis (Okoro et al. 2010) Nouioui et al. 2018 and an emended description of Lentzea atacamensis. PLoS One 2010; 16:e0246533 [View Article]
    [Google Scholar]
  9. Křı́bek B, Strnad M, Boháček Z, Sýkorová I, Čejka J et al. Geochemistry of Miocene lacustrine sediments from the Sokolov Coal Basin (Czech Republic). Int J Coal Geol 1998; 37:207–233 [View Article]
    [Google Scholar]
  10. Petříčková K, Chroňáková A, Zelenka T, Chrudimský T, Pospíšil S et al. Evolution of cyclizing 5-aminolevulinate synthases in the biosynthesis of actinomycete secondary metabolites: outcomes for genetic screening techniques. Front Microbiol 2015; 6:814 [View Article] [PubMed]
    [Google Scholar]
  11. Chronáková A, Kristůfek V, Tichý M, Elhottová D. Biodiversity of Streptomycetes isolated from a succession sequence at a post-mining site and their evidence in Miocene lacustrine sediment. Microbiol Res 2010; 165:594–608 [View Article] [PubMed]
    [Google Scholar]
  12. Shirling EB, Gottlieb D. Methods for characterization of Streptomyces species. Int J Syst Bacteriol 1966; 16:313–340 [View Article]
    [Google Scholar]
  13. Bertani G. Studies on lysogenesis I. J Bacteriol 1951; 62:293–300 [View Article]
    [Google Scholar]
  14. Edwards U, Rogall T, Blöcker H, Emde M, Böttger EC. Isolation and direct complete nucleotide determination of entire genes. Characterization of a gene coding for 16S ribosomal RNA. Nucl Acids Res 1989; 17:7843–7853 [View Article]
    [Google Scholar]
  15. 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]
  16. Edgar RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 2004; 32:1792–1797 [View Article] [PubMed]
    [Google Scholar]
  17. Kozlov AM, Darriba D, Flouri T, Morel B, Stamatakis A. RAxML-NG: a fast, scalable and user-friendly tool for maximum likelihood phylogenetic inference. Bioinformatics 2019; 35:4453–4455 [View Article] [PubMed]
    [Google Scholar]
  18. Miller MA, Pfeiffer W, Schwartz T. Creating the CIPRES Science Gateway for inference of large phylogenetic trees. In 2010 Gateway Computing Environments Workshop (GCE) 2010 pp 1–8
    [Google Scholar]
  19. Letunic I, Bork P. Interactive Tree Of Life (iTOL) v5: an online tool for phylogenetic tree display and annotation. Nucleic Acids Res 2021; 49:W293–W296 [View Article] [PubMed]
    [Google Scholar]
  20. Labeda DP, Donahue JM, Sells SF, Kroppenstedt RM. Lentzea kentuckyensis sp. nov., of equine origin. Int J Syst Evol Microbiol 2007; 57:1780–1783 [View Article] [PubMed]
    [Google Scholar]
  21. Li D, Zheng W, Zhao J, Han L, Zhao X et al. Lentzea soli sp. nov., an actinomycete isolated from soil. Int J Syst Evol Microbiol 2018; 68:1496–1501 [View Article] [PubMed]
    [Google Scholar]
  22. Hassler HB, Probert B, Moore C, Lawson E, Jackson RW et al. Phylogenies of the 16S rRNA gene and its hypervariable regions lack concordance with core genome phylogenies. Microbiome 2022; 10: [View Article]
    [Google Scholar]
  23. Nakano Y, Domon Y, Yamagishi K. Phylogenetic trees of closely related bacterial species and subspecies based on frequencies of short nucleotide sequences. PLoS One 2023; 18:e0268847 [View Article] [PubMed]
    [Google Scholar]
  24. Andrews S, Krueger F, Segonds-Pichon A, Biggins L, Krueger C et al. FastQC Babraham, UK: Babraham Institute; 2012
    [Google Scholar]
  25. Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 2014; 30:2114–2120 [View Article]
    [Google Scholar]
  26. Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M et al. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 2012; 19:455–477 [View Article] [PubMed]
    [Google Scholar]
  27. Zerbino DR. Using the Velvet de novo assembler for short-read sequencing technologies. Curr Protoc Bioinformatics 2010; Chapter 11:Unit [View Article] [PubMed]
    [Google Scholar]
  28. Arkin AP, Cottingham RW, Henry CS, Harris NL, Stevens RL et al. KBase: the United States Department of Energy systems biology knowledgebase. Nat Biotechnol 2018; 36:566–569 [View Article] [PubMed]
    [Google Scholar]
  29. Sayers EW, Bolton EE, Brister JR, Canese K, Chan J et al. Database resources of the National Center for Biotechnology Information. Nucleic Acids Res 2022; 50:D20–D26 [View Article] [PubMed]
    [Google Scholar]
  30. 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]
  31. Seemann T. Prokka: rapid prokaryotic genome annotation. Bioinformatics 2014; 30:2068–2069 [View Article] [PubMed]
    [Google Scholar]
  32. Kanehisa M, Furumichi M, Sato Y, Kawashima M, Ishiguro-Watanabe M. KEGG for taxonomy-based analysis of pathways and genomes. Nucleic Acids Res 2023; 51:D587–D592 [View Article] [PubMed]
    [Google Scholar]
  33. Aziz RK, Bartels D, Best AA, DeJongh M, Disz T et al. The RAST server: rapid annotations using subsystems technology. BMC Genomics 2008; 9:75 [View Article] [PubMed]
    [Google Scholar]
  34. Lee I, Ouk Kim Y, Park SC, Chun J. OrthoANI: An improved algorithm and software for calculating average nucleotide identity. Int J Syst Evol Microbiol 2016; 66:1100–1103 [View Article] [PubMed]
    [Google Scholar]
  35. 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] [PubMed]
    [Google Scholar]
  36. 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 Evol Microbiol 1994; 44:846–849 [View Article]
    [Google Scholar]
  37. Moore WEC, Stackebrandt E, Kandler O, Colwell RR, Krichevsky MI 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]
  38. Jalil M, Quddos F, Anwer F, Nasir S, Rahman A et al. Comparative pan-genomic analysis revealed an improved multi-locus sequence typing scheme for Staphylococcus aureus. Genes (Basel) 2022; 13:2160 [View Article] [PubMed]
    [Google Scholar]
  39. Ruppitsch W, Pietzka A, Prior K, Bletz S, Fernandez HL et al. Defining and evaluating a core genome multilocus sequence typing scheme for whole-genome sequence-based typing of Listeria monocytogenes. J Clin Microbiol 2015; 53:2869–2876 [View Article] [PubMed]
    [Google Scholar]
  40. Kohl TA, Diel R, Harmsen D, Rothgänger J, Walter KM et al. Whole-genome-based Mycobacterium tuberculosis surveillance: a standardized, portable, and expandable approach. J Clin Microbiol 2014; 52:2479–2486 [View Article] [PubMed]
    [Google Scholar]
  41. Higgins PG, Prior K, Harmsen D, Seifert H. Development and evaluation of a core genome multilocus typing scheme for whole-genome sequence-based typing of Acinetobacter baumannii. PLoS One 2017; 12:e0179228 [View Article] [PubMed]
    [Google Scholar]
  42. Mellmann A, Harmsen D, Cummings CA, Zentz EB, Leopold SR et al. Prospective genomic characterization of the German enterohemorrhagic Escherichia coli O104:H4 outbreak by rapid next generation sequencing technology. PLoS One 2011; 6:e22751 [View Article]
    [Google Scholar]
  43. Gonzalez-Escalona N, Jolley KA, Reed E, Martinez-Urtaza J. Defining a core genome multilocus sequence typing scheme for the global epidemiology of Vibrio parahaemolyticus. J Clin Microbiol 2017; 55:1682–1697 [View Article] [PubMed]
    [Google Scholar]
  44. de Been M, Pinholt M, Top J, Bletz S, Mellmann A et al. Core genome multilocus sequence typing scheme for high-resolution typing of Enterococcus faecium. J Clin Microbiol 2015; 53:3788–3797 [View Article] [PubMed]
    [Google Scholar]
  45. Kim J, Na S-I, Kim D, Chun J. UBCG2: up-to-date bacterial core genes and pipeline for phylogenomic analysis. J Microbiol 2021; 59:609–615 [View Article]
    [Google Scholar]
  46. Paysan-Lafosse T, Blum M, Chuguransky S, Grego T, Pinto BL et al. InterPro in 2022. Nucleic Acids Res 2023; 51:D418–D427 [View Article] [PubMed]
    [Google Scholar]
  47. Blin K, Shaw S, Kloosterman AM, Charlop-Powers Z, van Wezel GP et al. antiSMASH 6.0: improving cluster detection and comparison capabilities. Nucleic Acids Res 2021; 49:W29–W35 [View Article]
    [Google Scholar]
  48. Garbeva P, Avalos M, Ulanova D, van Wezel GP, Dickschat JS. Volatile sensation: the chemical ecology of the earthy odorant geosmin. Environ Microbiol 2023; 25:1565–1574 [View Article] [PubMed]
    [Google Scholar]
  49. Gerber NN, Lechevalier HA. Geosmin, an earthly-smelling substance isolated from actinomycetes. Appl Microbiol 1965; 13:935–938 [View Article] [PubMed]
    [Google Scholar]
  50. Becher PG, Verschut V, Bibb MJ, Bush MJ, Molnár BP et al. Developmentally regulated volatiles geosmin and 2-methylisoborneol attract a soil arthropod to Streptomyces bacteria promoting spore dispersal. Nat Microbiol 2020; 5:821–829 [View Article] [PubMed]
    [Google Scholar]
  51. Traxler MF, Seyedsayamdost MR, Clardy J, Kolter R. Interspecies modulation of bacterial development through iron competition and siderophore piracy. Mol Microbiol 2012; 86:628–644 [View Article] [PubMed]
    [Google Scholar]
  52. Hyldgaard M, Mygind T, Vad BS, Stenvang M, Otzen DE et al. The antimicrobial mechanism of action of epsilon-poly-l-lysine. Appl Environ Microbiol 2014; 80:7758–7770 [View Article] [PubMed]
    [Google Scholar]
  53. Chen Y, Guo M, Yang J, Chen J, Xie B et al. Potential TSPO ligand and photooxidation quencher isorenieratene from Arctic Ocean Rhodococcus sp. B7740. Mar Drugs 2019; 17:316 [View Article] [PubMed]
    [Google Scholar]
  54. Woo EJ, Starks CM, Carney JR, Arslanian R, Cadapan L et al. Migrastatin and a new compound, isomigrastatin, from Streptomyces platensis. J Antibiot 2002; 55:141–146 [View Article]
    [Google Scholar]
  55. Khosravi Babadi Z, Ebrahimipour G, Wink J, Narmani A, Risdian C. Isolation and identification of Streptomyces sp. Act4Zk, a good producer of staurosporine and some derivatives. Lett Appl Microbiol 2021; 72:206–218 [View Article] [PubMed]
    [Google Scholar]
  56. Labeda DP, Hatano K, Kroppenstedt RM, Tamura T. Revival of the genus Lentzea and proposal for Lechevalieria gen. nov. Int J Syst Evol Microbiol 2001; 51:1045–1050 [View Article] [PubMed]
    [Google Scholar]
  57. Sun X, Zhao J, Luo X, Hou W, Xiang W et al. Lentzea alba sp. nov., a novel actinobacterium isolated from soil. Int J Syst Evol Microbiol 2021; 71:004661 [View Article] [PubMed]
    [Google Scholar]
  58. Pridham TG, Hesseltine CW, Benedict RG. A guide for the classification of streptomycetes according to selected groups; placement of strains in morphological sections. Appl Microbiol 1958; 6:52–79 [View Article] [PubMed]
    [Google Scholar]
  59. Lechevalier MP, Lechevalier H. Chemical composition as a criterion in the classification of aerobic actinomycetes. Int J Syst Bacteriol 1970; 20:435–443 [View Article]
    [Google Scholar]
  60. 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]
  61. 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]
  62. Vieira S, Huber KJ, Neumann-Schaal M, Geppert A, Luckner M et al. Usitatibacter rugosus gen. nov., sp. nov. and Usitatibacter palustris sp. nov., novel members of Usitatibacteraceae fam. nov. within the order Nitrosomonadales isolated from soil. Int J Syst Evol Microbiol 2021; 71:004631 [View Article]
    [Google Scholar]
  63. Schumann P, Kalensee F, Cao J, Criscuolo A, Clermont D. Reclassification of Haloactinobacterium glacieicola as Occultella glacieicola gen. nov., comb. nov., of Haloactinobacterium album as Ruania alba comb. nov, with an emended description of the genus Ruania, recognition that the genus names Haloactinobacterium and Ruania are heterotypic synonyms and description of Occultella aeris sp. nov., a halotolerant isolate from surface soil sampled at an ancient copper smelter. Int J Syst Evol Microbiol 2021; 71:004769 [View Article] [PubMed]
    [Google Scholar]
  64. Lechevalier MP, De Bievre C, Lechevalier H. Chemotaxonomy of aerobic Actinomycetes: phospholipid composition. Biochem Syst Ecol 1977; 5:249–260 [View Article]
    [Google Scholar]
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