1887

Abstract

The actinomycetes strains KRD168 and KRD185 were isolated from sediments collected from the deep Southern Ocean and, in this work, they are described as representing two novel species of the genus through a polyphasic approach. Despite sharing >99 % 16S rRNA gene sequence similarity with other members of the genus, comparative genomic analysis allowed species delimitation based on average nucleotide identity and digital DNA–DNA hybridization. The KRD168 genome is characterized by a size of 6.31 Mbp and a G+C content of 73.44 mol%, while the KRD185 genome has a size of 6.82 Mbp and a G+C content of 73.98 mol%. Both strains contain -diaminopimelic acid as the diagnostic diamino acid, glucose as the major whole-cell sugar, MK-8(H) as a major menaquinone and -branched hexadecanoic acid as a major fatty acid. Biochemical and fatty acid analyses also revealed differences between these strains and their phylogenetic neighbours, supporting their status as distinct species. The names sp. nov. (type strain KRD168=DSM 111918=NCIMB 15270) and (type strain KRD185=DSM 111919=NCIMB 15269) are proposed.

Funding
This study was supported by the:
  • Programa de Innovación y Capital Humano para la Competitividad (PINN) of The Ministry of Science, Technology and Telecommunications of Costa Rica (MICITT) (Award 2-1-4-17-1-037.)
    • Principle Award Recipient: JonathanParra
  • This is an open-access article distributed under the terms of the Creative Commons Attribution NonCommercial 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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2021-09-28
2021-10-24
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References

  1. Henssen A. Beiträge zur Morphologie und Systematik der thermophilen Actinomyceten [Contributions to the morphology and systematics of the thermophilic actinomycetes]. Archiv Mikrobiol 1957; 26:373–414 [View Article]
    [Google Scholar]
  2. Reichert K, Lipski A, Pradella S, Stackebrandt E, Altendorf K. Pseudonocardia asaccharolytica sp. nov. and Pseudonocardia sulfidoxydans sp. nov., two new dimethyl disulfide-degrading actinomycetes and emended description of the genus Pseudonocardia. Int J Syst Bacteriol 1998; 48 Pt 2:441–449 [View Article] [PubMed]
    [Google Scholar]
  3. Warwick S, Bowen T, McVeigh H, Embley TM. A phylogenetic analysis of the family Pseudonocardiaceae and the genera Actinokineospora and Saccharothrix with 16S rRNA sequences and a proposal to combine the genera Amycolata and Pseudonocardia in an emended genus Pseudonocardia. Int J Syst Bacteriol 1994; 44:293–299 [View Article] [PubMed]
    [Google Scholar]
  4. Huang Y, Wang L, Lu Z, Hong L, Liu Z et al. Proposal to combine the genera Actinobispora and Pseudonocardia in an emended genus Pseudonocardia, and description of Pseudonocardia zijingensis sp. nov. Int J Syst Evol Microbiol 2002; 52:977–982 [View Article] [PubMed]
    [Google Scholar]
  5. Park SW, Park ST, Lee JE, Kim YM. Pseudonocardia carboxydivorans sp. nov., a carbon monoxide-oxidizing actinomycete, and an emended description of the genus Pseudonocardia. Int J Syst Evol Microbiol 2008; 58:2475–2478 [View Article] [PubMed]
    [Google Scholar]
  6. Huang Y, Goodfellow M. Pseudonocardia. Trujillo ME, Dedysh S, DeVos P, Hedlund B, Kämpfer P. eds In Bergey’s Manual of Systematics of archaea and bacteria Wiley; 2015 pp 1–32
    [Google Scholar]
  7. 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]
  8. LPSN - List of Prokaryotic names with Standing in Nomenclature Genus Pseudonocardia. https://lpsn.dsmz.de/genus/pseudonocardia
  9. Gontang EA, Fenical W, Jensen PR. Phylogenetic diversity of gram-positive bacteria cultured from marine sediments. Appl Environ Microbiol 2007; 73:3272–3282 [View Article] [PubMed]
    [Google Scholar]
  10. Maldonado LA, Stach JEM, Pathom-aree W, Ward AC, Bull AT et al. Diversity of cultivable actinobacteria in geographically widespread marine sediments. Antonie van Leeuwenhoek 2005; 87:11–18 [View Article]
    [Google Scholar]
  11. Chanama S, Janphen S, Suriyachadkun C, Chanama M. Pseudonocardia mangrovi sp. nov., isolated from soil. Int J Syst Evol Microbiol 2018; 68:2949–2955 [View Article] [PubMed]
    [Google Scholar]
  12. Liu Z-P, Wu J-F, Liu Z-H, Liu S-J. Pseudonocardia ammonioxydans sp. nov., isolated from coastal sediment. Int J Syst Evol Microbiol 2006; 56:555–558 [View Article] [PubMed]
    [Google Scholar]
  13. Zhang D-F, Jiang Z, Li L, Liu B-B, Zhang X-M et al. Pseudonocardia sediminis sp. nov., isolated from marine sediment. Int J Syst Evol Microbiol 2014; 64:745–750 [View Article] [PubMed]
    [Google Scholar]
  14. Tian X-P, Long L-J, Li S-M, Zhang J, Xu Y et al. Pseudonocardia antitumoralis sp. nov., a deoxynyboquinone-producing actinomycete isolated from a deep-sea sediment. Int J Syst Evol Microbiol 2013; 63:893–899 [View Article] [PubMed]
    [Google Scholar]
  15. Zhang G, Wang L, Li J, Zhou Y. Pseudonocardia profundimaris sp. nov., isolated from marine sediment. Int J Syst Evol Microbiol 2017; 67:1693–1697 [View Article] [PubMed]
    [Google Scholar]
  16. Millán-Aguiñaga N, Soldatou S, Brozio S, Munnoch JT, Howe J et al. Awakening ancient polar Actinobacteria: diversity, evolution and specialized metabolite potential. Microbiol 2019; 165:1169–1180 [View Article]
    [Google Scholar]
  17. Soldatou S, Eldjárn GH, Ramsay A, van der Hooft JJJ, Hughes AH et al. Comparative metabologenomics analysis of polar actinomycetes. Mar Drugs 2021; 19:103 [View Article] [PubMed]
    [Google Scholar]
  18. Howe JA, Shimmield TM, Diaz R. Deep-water sedimentary environments of the Northwestern Weddell Sea and South Sandwich Islands, Antarctica. Deep Res Part II Top Stud Oceanogr 2004; 51:1489–1514
    [Google Scholar]
  19. Mincer TJ, Jensen PR, Kauffman CA, Fenical W. Widespread and persistent populations of a major new marine actinomycete taxon in ocean sediments. Appl Environ Microbiol 2002; 68:5005–5011 [View Article] [PubMed]
    [Google Scholar]
  20. Shirling ET, Gottlieb D. Methods for characterization of Streptomyces species. Int J Syst Bacteriol 1966; 16:313–340 [View Article]
    [Google Scholar]
  21. Weisburg WG, Barns SM, Pelletier DA, Lane DJ. 16S ribosomal DNA amplification for phylogenetic study. J Bacteriol 1991; 173:697–703 [View Article] [PubMed]
    [Google Scholar]
  22. 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]
  23. 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]
  24. 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] [PubMed]
    [Google Scholar]
  25. 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]
  26. Tamura K, Nei M. Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol 1993; 10:512–526 [View Article] [PubMed]
    [Google Scholar]
  27. 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 [View Article] [PubMed]
    [Google Scholar]
  28. Felsenstein J. Confidence limits on phylogenies: an approach using the bootstrap. Evolution 1985; 39:783–791 [View Article]
    [Google Scholar]
  29. Marmur J. A procedure for the isolation of deoxyribonucleic acid from micro-organisms. J Mol Biol 1961; 3:208–218
    [Google Scholar]
  30. Kolmogorov M, Yuan J, Lin Y, Pevzner PA. Assembly of long, error-prone reads using repeat graphs. Nat Biotechnol 2019; 37:540–546 [View Article] [PubMed]
    [Google Scholar]
  31. Langmead B, Salzberg SL. Fast gapped-read alignment with Bowtie 2. Nat Methods 2012; 9:357–359 [View Article] [PubMed]
    [Google Scholar]
  32. Walker BJ, Abeel T, Shea T, Priest M, Abouelliel A et al. Pilon: an integrated tool for comprehensive microbial variant detection and genome assembly improvement. PLoS One 2014; 9:e112963 [View Article] [PubMed]
    [Google Scholar]
  33. Chin C-S, Alexander DH, Marks P, Klammer AA, Drake J et al. Nonhybrid, finished microbial genome assemblies from long-read SMRT sequencing data. Nat Methods 2013; 10:563–569 [View Article] [PubMed]
    [Google Scholar]
  34. Koren S, Walenz BP, Berlin K, Miller JR, Bergman NH et al. Canu: scalable and accurate long-read assembly via adaptive k-mer weighting and repeat separation. Genome Res 2017; 27:722–736 [View Article] [PubMed]
    [Google Scholar]
  35. Vaser R, Šikić M. Raven: A de novo genome assembler for long reads. bioRxiv 202008.07.242461 [View Article]
    [Google Scholar]
  36. Wick RR, Judd LM, Gorrie CL, Holt KE. Unicycler: Resolving bacterial genome assemblies from short and long sequencing reads. PLoS Comput Biol 2017; 13:1–22
    [Google Scholar]
  37. 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]
  38. Gurevich A, Saveliev V, Vyahhi N, Tesler G. QUAST: Quality assessment tool for genome assemblies. Bioinformatics 2013; 29:1072–1075 [View Article] [PubMed]
    [Google Scholar]
  39. Simão FA, Waterhouse RM, Ioannidis P, Kriventseva EV, Zdobnov EM. BUSCO: Assessing genome assembly and annotation completeness with single-copy orthologs. Bioinformatics 2015; 31:3210–3212 [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 Bioinformatics 2013; 14:60 [View Article] [PubMed]
    [Google Scholar]
  41. Jain C, Rodriguez-R LM, Phillippy AM, Konstantinidis KT, Aluru S. High throughput ANI analysis of 90K prokaryotic genomes reveals clear species boundaries. Nat Commun 2018; 9:1–8
    [Google Scholar]
  42. Richter M, Rosselló-Móra R. Shifting the genomic gold standard for the prokaryotic species definition. Proc Natl Acad Sci U S A 2009; 106:19126–19131 [View Article] [PubMed]
    [Google Scholar]
  43. Meier-Kolthoff JP, Klenk H-P, Göker M. Taxonomic use of DNA G+C content and DNA-DNA hybridization in the genomic age. Int J Syst Evol Microbiol 2014; 64:352–356 [View Article] [PubMed]
    [Google Scholar]
  44. Alanjary M, Steinke K, Ziemert N. AutoMLST: an automated web server for generating multi-locus species trees highlighting natural product potential. Nucleic Acids Res 2019; 47:276–282 [View Article]
    [Google Scholar]
  45. Nolof G, Hirsch P. Nocardia hydrocarbonoxydans n. spec., ein oligocarbophiler Actinomycet. Arch Mikrobiol 1962; 44:266–277
    [Google Scholar]
  46. Kuykendall LD, Roy MA, O’Neill JJ, Devine TE. Fatty acids, antibiotic resistance, and deoxyribonucleic acid homology groups of Bradyrhizobium japonicum. Int J Syst Bacteriol 1988; 38:358–361 [View Article]
    [Google Scholar]
  47. Miller LT. Single derivatization method for routine analysis of bacterial whole-cell fatty acid methyl esters, including hydroxy acids. J Clin Microbiol 1982; 16:584–586 [View Article] [PubMed]
    [Google Scholar]
  48. Tindall BJ, Sikorski J, Smibert RA, Krieg NR. Phenotypic characterization and the principles of comparative systematics. In Methods for General and Molecular Microbiology Washington, DC, USA: ASM Press; 2014 pp 330–393
    [Google Scholar]
  49. Rhuland LE, Work E, Denman RF, Hoare DS. The behavior of the isomers of α,ε-diaminopimelic acid on paper chromatograms. J Am Chem Soc 1955; 77:4844–4846 [View Article]
    [Google Scholar]
  50. 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]
  51. Schwedock J, McCormick JR, Angert ER, Nodwell JR, Losick R. Assembly of the cell division protein FtsZ into ladder-like structures in the aerial hyphae of Streptomyces coelicolor. Mol Microbiol 1997; 25:847–858 [View Article] [PubMed]
    [Google Scholar]
  52. Schindelin J, Arganda-Carreras I, Frise E, Kaynig V, Longair M et al. Fiji: An open-source platform for biological-image analysis. Nat Methods 2012; 9:676–682 [View Article] [PubMed]
    [Google Scholar]
  53. Zhao GZ, Zhu WY, Li J, Xie Q, Xu LH et al. Pseudonocardia serianimatus sp. nov., a novel actinomycete isolated from the surface-sterilized leaves of Artemisia annua L. Antonie van Leeuwenhoek 2011; 100:521–528
    [Google Scholar]
  54. Mo P, Zhao Y, Liu J, Xu Z, Gao J. Pseudonocardia broussonetiae sp. nov., an endophytic actinomycete isolated from the roots of Broussonetia papyrifera. Int J Syst Evol Microbiol 2021; 71:004680
    [Google Scholar]
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