1887

Abstract

A red pigmented actinobacterium designated G2, forming extremely branched vegetative hyphae, vesicles and mutilocular sporangia, was isolated from Casuarina equisetifolia nodules. The strain failed to nodulate its original host plant but effectively nodulated members of actinorhizal Rhamnales. The taxonomic position of G2 was determined using a polyphasic approach. The peptidoglycan of the strain contained meso-diaminopimelic acid as diagnostic diamino acid, galactose, glucose, mannose, rhamnose, ribose and xylose. The polar lipid pattern consisted of phosphatidylinositol (PI), diphosphatidylglycerol (DPG), glycophospholipids (GPL1–2), phosphatidylglycerol (PG), aminophospholipid (APL) and unknown lipids (L). The predominant menaquinones were MK-9 (H4) and MK-9 (H6) while the major fatty acids were iso-C16 : 0, C17 : 1ω8c and C15 : 0. The size of the genome of G2 was 9.5 Mb and digital DNA G+C content was 70.9 %. The 16S rRNA gene showed 97.4–99.5 % sequence identity with the type strains of species of the genus Frankia . Digital DNA –DNA hybridisation (dDDH) values between G2 and its nearest phylogenetic neighbours Frankia elaeagni and Frankia discariae were below the threshold of 70 %. On the basis of these results, strain G2 (=DSM 45899=CECT 9038) is proposed to represent the type strain of a novel species Frankia irregularis sp. nov.

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2018-07-16
2024-03-29
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References

  1. Brunchorst J. Über einige Wurzelanschwellungen, besonders diejenigen von Alnus und den Elaegnaceen. Botanische Institut Tubingen 1886; 2:151–177
    [Google Scholar]
  2. Becking JH. Frankiaceae fam. nov. (Actinomycetales) with one new combination and six new species of the genus Frankia Brunchorst 1886, 174. Int J Syst Bacteriol 1970; 20:201–220 [View Article]
    [Google Scholar]
  3. Zhi XY, Li WJ, Stackebrandt E. An update of the structure and 16S rRNA gene sequence-based definition of higher ranks of the class Actinobacteria, with the proposal of two new suborders and four new families and emended descriptions of the existing higher taxa. Int J Syst Evol Microbiol 2009; 59:589–608 [View Article][PubMed]
    [Google Scholar]
  4. Sen A, Daubin V, Abrouk D, Gifford I, Berry AM et al. Phylogeny of the class Actinobacteria revisited in the light of complete genomes. The orders 'Frankiales' and Micrococcales should be split into coherent entities: proposal of Frankiales ord. nov., Geodermatophilales ord. nov., Acidothermales ord. nov. and Nakamurellales ord. nov. Int J Syst Evol Microbiol 2014; 64:3821–3832 [View Article][PubMed]
    [Google Scholar]
  5. Chaia EE, Wall LG, Huss-Danell K. Life in soil by the actinorhizal root nodule endophyte Frankia. A review. Symbiosis 2010; 51:201–226 [View Article]
    [Google Scholar]
  6. Normand P, Orso S, Cournoyer B, Jeannin P, Chapelon C et al. Molecular phylogeny of the genus Frankia and related genera and emendation of the family Frankiaceae. Int J Syst Bacteriol 1996; 46:1–9 [View Article][PubMed]
    [Google Scholar]
  7. Nouioui I, Ghodhbane-Gtari F, Beauchemin NJ, Tisa LS, Gtari M. Phylogeny of members of the Frankia genus based on gyrB, nifH and glnII sequences. Antonie van Leeuwenhoek 2011; 100:579–587 [View Article][PubMed]
    [Google Scholar]
  8. Ghodhbane-Gtari F, Nouioui I, Chair M, Boudabous A, Gtari M. 16S–23S rRNA intergenic spacer region variability in the genus Frankia. Microb Ecol 2010; 60:487–495 [View Article][PubMed]
    [Google Scholar]
  9. Gtari M, Ghodhbane-Gtari F, Nouioui I, Ktari A, Hezbri K et al. Cultivating the uncultured: growing the recalcitrant cluster-2 Frankia strains. Sci Rep 2015; 5:13112 [View Article][PubMed]
    [Google Scholar]
  10. Louis ST, Oshone R, Sarkar I, Ktari A, Sen A et al. Genomic approaches toward understanding the actinorhizal symbiosis: an update on the status of the Frankia genomes. Symbiosis 2016; 70:5–16
    [Google Scholar]
  11. Baker DD. Relationships among pure cultured strains of Frankia based on host specificity. Physiol Plant 1987; 70:245–248 [View Article]
    [Google Scholar]
  12. Nouioui I, Ghodhbane-Gtari F, Montero-Calasanz MD, Göker M, Meier-Kolthoff JP et al. Proposal of a type strain for Frankia alni (Woronin 1866) Von Tubeuf 1895, emended description of Frankia alni, and recognition of Frankia casuarinae sp. nov. and Frankia elaeagni sp. nov. Int J Syst Evol Microbiol 2016; 66:5201–5210 [View Article][PubMed]
    [Google Scholar]
  13. Normand N, Nouioui I, Pujic P, Fournier P, Dubost A et al. Frankia canadensis sp. nov., isolated from root nodules of Alnus incana subspecies rugosa growing in Canada. Int J Evol Syst Microbiol 2018
    [Google Scholar]
  14. Nouioui I, Ghodhbane-Gtari F, Rohde M, Klenk HP, Gtari M. Frankia coriariae sp. nov., an infective and effective microsymbiont isolated from Coriaria japonica. Int J Syst Evol Microbiol 2017; 67:1266–1270 [View Article][PubMed]
    [Google Scholar]
  15. Persson T, Benson DR, Normand P, vanden Heuvel B, Pujic P et al. Genome sequence of "Candidatus Frankia datiscae" Dg1, the uncultured microsymbiont from nitrogen-fixing root nodules of the dicot Datisca glomerata. J Bacteriol 2011; 193:7017–7018 [View Article][PubMed]
    [Google Scholar]
  16. Normand P, Nguyen TV, Battenberg K, Berry AM, Heuvel BV et al. Proposal of 'Candidatus Frankia californiensis', the uncultured symbiont in nitrogen-fixing root nodules of a phylogenetically broad group of hosts endemic to western North America. Int J Syst Evol Microbiol 2017; 67:3706–3715 [View Article][PubMed]
    [Google Scholar]
  17. Nouioui I, del Carmen Montero-Calasanz M, Ghodhbane-Gtari F, Rohde M, Tisa LS et al. Frankia discariae sp. nov.: an infective and effective microsymbiont isolated from the root nodule of Discaria trinervis. Arch Microbiol 2017; 199:641–647 [View Article][PubMed]
    [Google Scholar]
  18. Nouioui I, Ghodhbane-Gtari F, del Carmen Montero-Calasanz M, Rohde M, Tisa LS et al. Frankia inefficax sp. nov., an actinobacterial endophyte inducing ineffective, non nitrogen-fixing, root nodules on its actinorhizal host plants. Antonie van Leeuwenhoek 2017; 110:313–320 [View Article][PubMed]
    [Google Scholar]
  19. Nouioui I, Gueddou A, Ghodhbane-Gtari F, Rhode M, Gtari M et al. Frankia asymbiotica sp. nov., a non-infective actinobacterium isolated from Morella californica root nodule. Int J Syst Evol Microbiol 2017; 67:4897–4901 [View Article][PubMed]
    [Google Scholar]
  20. Nouioui I, Ghodhbane-Gtari F, Klenk HP, Gtari M. Frankia saprophytica sp. nov., an atypical, non-infective (Nod-) and non-nitrogen fixing (Fix-) actinobacterium isolated from Coriaria nepalensis root nodules. Int J Syst Evol Microbiol 2018; 68:1090–1095 [View Article][PubMed]
    [Google Scholar]
  21. Diem HG, Gauthier D, Dommergues YR. Isolation of Frankia from nodules of Casuarina equisetifolia. Can J Microbiol 1982; 28:526–530 [View Article]
    [Google Scholar]
  22. Murry MA, Fontaine MS, Torrey JG. Growth kinetics and nitrogenase induction in Frankia sp. HFPArI3 grown in batch culture. Plant Soil 1984; 78:61–78 [View Article]
    [Google Scholar]
  23. 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[PubMed]
    [Google Scholar]
  24. 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]
  25. Meier-Kolthoff JP, Auch AF, Klenk HP, Göker M. Genome sequence-based species delimitation with confidence intervals and improved distance functions. BMC Bioinformatics 2013; 14:60 [View Article][PubMed]
    [Google Scholar]
  26. Meier-Kolthoff JP, Göker M, Spröer C, Klenk HP. When should a DDH experiment be mandatory in microbial taxonomy?. Arch Microbiol 2013; 195:413–418 [View Article][PubMed]
    [Google Scholar]
  27. Meier-Kolthoff JP, Hahnke RL, Petersen J, Scheuner C, Michael V et al. Complete genome sequence of DSM 30083T, the type strain (U5/41T) of Escherichia coli, and a proposal for delineating subspecies in microbial taxonomy. Stand Genomic Sci 2014; 9:2 [View Article][PubMed]
    [Google Scholar]
  28. 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]
  29. Goloboff PA, Farris JS, Nixon KC. TNT, a free program for phylogenetic analysis. Cladistics 2008; 24:774–786 [View Article]
    [Google Scholar]
  30. 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]
  31. Edgar RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 2004; 32:1792–1797 [View Article][PubMed]
    [Google Scholar]
  32. Swofford DL. PAUP*: Phylogenetic Analysis Using Parsimony (*and Other Methods), Version 4.0 Sunderland: Sinauer Associates; 2002
    [Google Scholar]
  33. Gtari M, Brusetti L, Skander G, Mora D, Boudabous A et al. Isolation of Elaeagnus-compatible Frankia from soils collected in Tunisia. FEMS Microbiol Lett 2004; 234:349–355 [View Article][PubMed]
    [Google Scholar]
  34. Gtari M, Daffonchio D, Boudabous A. Assessment of the genetic diversity of Frankia microsymbionts of Elaeagnus angustifolia L. plants growing in a Tunisian date-palm oasis by analysis of PCR amplified nifD–K intergenic spacer. Can J Microbiol 2007; 53:440–445 [View Article][PubMed]
    [Google Scholar]
  35. Seemann T. Prokka: rapid prokaryotic genome annotation. Bioinformatics 2014; 30:2068–2069 [View Article][PubMed]
    [Google Scholar]
  36. Chaudhari NM, Gupta VK, Dutta C. BPGA- an ultra-fast pan-genome analysis pipeline. Sci Rep 2016; 6:24373 [View Article][PubMed]
    [Google Scholar]
  37. Castresana J. Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol 2000; 17:540–552 [View Article][PubMed]
    [Google Scholar]
  38. Minh BQ, Nguyen MA, von Haeseler A. Ultrafast approximation for phylogenetic bootstrap. Mol Biol Evol 2013; 30:1188–1195 [View Article][PubMed]
    [Google Scholar]
  39. Segata N, Börnigen D, Morgan XC, Huttenhower C. PhyloPhlAn is a new method for improved phylogenetic and taxonomic placement of microbes. Nat Commun 2013; 4:2304 [View Article][PubMed]
    [Google Scholar]
  40. Stamatakis A. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 2006; 22:2688–2690 [View Article][PubMed]
    [Google Scholar]
  41. Wayne LG, Moore WEC, Stackebrandt E, Kandler O, Colwell RR 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]
  42. Benson DR, Silvester WB. Biology of Frankia strains, actinomycete symbionts of actinorhizal plants. Microbiol Rev 1993; 57:293–319[PubMed]
    [Google Scholar]
  43. Schwencke J, Carú M. Advances in actinorhizal symbiosis: host plant- Frankia interactions, biology, and applications in arid land reclamation. A review. Arid Land Res Manag 2001; 15:285–327 [View Article]
    [Google Scholar]
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