1887

Abstract

Strains CN4, CN6, CN7 and CNm7 were isolated from root nodules of from Murree in Pakistan. They do not form root nodules on nor on although they deformed root hairs of . The colonies are bright red-pigmented, the strains form hyphae and sporangia but no N-fixing vesicles and do not fix nitrogen . The peptidoglycan of strain CN4 contains -diaminopimelic acid; whole cell sugars consist of ribose, mannose, glucose, galactose and rhamnose. Diphosphatidylglycerol, phosphatidylglycerol, phosphatidylinositol and two unknown lipids represent the major polar lipids; MK-9(H) and MK-9(H) are the predominant menaquinones (>15 %), and iso-C and Cω8 are the major fatty acids (>15 %). The results of comparative 16S rRNA gene sequence analyses indicated that strain CN4 is most closely related to CN 3. An MLSA phylogeny using amino acids sequences of AtpD, DnaA, FtsZ, Pgk and RpoB, assigned the strain to cluster 4 non-nodulating species, close to CN 3 M16386 and EuI1c with 0.04 substitutions per site, while that value was 0.075 with other strains. Digital DNA–DNA hybridization (dDDH) and average nucleotide identity (ANI) values between CN4 and all species of the genus with validly published names were below the defined threshold for prokaryotic species demarcation, with dDDH and ANI values at or below 27.8 and 83.7 %, respectively. The four strains CN4, CN6, CN7 and CNm7 had dDDH (98.6–99.6 %) and ANI values that grouped them as representing a single species. CN4 has a 10.76 Mb genome. CN4 was different from its close phylogenetic neighbours with validly published names in being red-pigmented, in having several lantibiotic-coding clusters, a carbon monoxide dehydrogenase cluster and a clustered regularly interspaced short palindromic repeats (CRISPR) cluster. The results of phenotypic, physiological and phylogenomic analyses confirmed the assignment of strain CN4 (=DSM 114740 = LMG 32595) to a novel species, with CN4 as type strain, for which the name sp. nov. is proposed.

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2023-12-14
2024-04-27
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References

  1. Brunchorst J. Über Einige Wurzelanschwellungen, Besonders die Jenigen von Alnus, und den Elaeagnaceen. Unters Bot Inst Tübingen 1886; 2:151–177
    [Google Scholar]
  2. Benson DR, Silvester WB. Biology of Frankia strains, actinomycete symbionts of actinorhizal plants. Microbiol Rev 1993; 57:293–319 [View Article] [PubMed]
    [Google Scholar]
  3. 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]
  4. Callaham D, Deltredici P, Torrey JG. Isolation and cultivation in vitro of the actinomycete causing root nodulation in Comptonia. Science 1978; 199:899–902 [View Article] [PubMed]
    [Google Scholar]
  5. Diem H, Gauthier D, Dommergues Y. Isolation of Frankia from nodules of Casuarina equisetifolia. Can J Microbiol 1982; 28:526–530 [View Article]
    [Google Scholar]
  6. Caru M. Characterization of native Frankia strains isolated from Chilean shrubs (Rhamnaceae). Plant Soil 1993; 157:137–145 [View Article]
    [Google Scholar]
  7. Nouioui I, Ghodhbane-Gtari F, Montero-Calasanz MDC, 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]
  8. Nouioui I, Ghodhbane-Gtari F, Jando M, Tisa LS, Klenk H-P et al. Frankia torreyi sp. nov., the first actinobacterium of the genus Frankia Brunchorst 1886, 174AL isolated in axenic culture. Antonie van Leeuwenhoek 2018; 112:57–65 [View Article] [PubMed]
    [Google Scholar]
  9. Normand P, Nouioui I, Pujic P, Fournier P, Dubost A et al. Frankia canadensis sp. nov., isolated from root nodules of Alnus incana subspecies rugosa. Int J Syst Evol Microbiol 2018; 68:3001–3011 [View Article] [PubMed]
    [Google Scholar]
  10. Nouioui I, Ghodhbane-Gtari F, Pötter G, Klenk H-P, Goodfellow M. Novel species of Frankia, Frankia gtarii sp. nov. and Frankia tisai sp. nov., isolated from a root nodule of Alnus glutinosa. Syst Appl Microbiol 2023; 46:126377 [View Article] [PubMed]
    [Google Scholar]
  11. Normand P, Nouioui I, Wolf J, Neumann-Schaal M, Herrera-Belaroussi A et al. Frankia umida sp. nov., isolated from root nodules of Alnus glutinosa L. Int J Syst Evol Microbiol 2023; 73:005939 [View Article]
    [Google Scholar]
  12. 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]
  13. 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]
  14. Gtari M, Ghodhbane-Gtari F, Nouioui I. Frankia soli sp. nov., an actinobacterium isolated from soil beneath Ceanothus jepsonii. Int J Syst Evol Microbiol 2019; 70:1203–1209 [View Article]
    [Google Scholar]
  15. Nouioui I, Ghodhbane-Gtari F, Rhode M, Sangal V, Klenk H-P et al. Frankia irregularis sp. nov., an actinobacterium unable to nodulate its original host, Casuarina equisetifolia, but effectively nodulates members of the actinorhizal Rhamnales. Int J Syst Evol Microbiol 2018; 68:2883–2914 [View Article] [PubMed]
    [Google Scholar]
  16. 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]
  17. Nouioui I, Ghodhbane-Gtari F, Klenk H-P, 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]
  18. Nouioui I, Ghodhbane-Gtari F, Jando M, Klenk HP, Gtari M. Frankia colletiae sp. nov., a nitrogen-fixing actinobacterium isolated from Colletia cruciata. Int J Syst Evol Microbiol 2022; 73: [View Article] [PubMed]
    [Google Scholar]
  19. Pozzi ACM, Herrera-Belaroussi A, Schwob G, Bautista-Guerrero HH, Bethencourt L et al. Proposal of 'Candidatus Frankia alpina', the uncultured symbiont of Alnus alnobetula and A. incana that forms spore-containing nitrogen-fixing root nodules. Int J Syst Evol Microbiol 2020; 70:5453–5459 [View Article]
    [Google Scholar]
  20. Herrera-Belaroussi A, Normand P, Pawlowski K, Fernandez MP, Wibberg D et al. Candidatus Frankia nodulisporulans sp. nov., an Alnus glutinosa-infective Frankia species unable to grow in pure culture and able to sporulate in-planta. Syst Appl Microbiol 2020; 43:126134 [View Article] [PubMed]
    [Google Scholar]
  21. 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]
  22. Persson T, Battenberg K, Demina IV, Vigil-Stenman T, Vanden Heuvel B et al. Candidatus Frankia datiscae Dg1, the actinobacterial microsymbiont of Datisca glomerata, expresses the canonical nod genes nodABC in symbiosis with its host plant. PLoS One 2015; 10:e0127630 [View Article] [PubMed]
    [Google Scholar]
  23. Nguyen TV, Wibberg D, Vigil-Stenman T, Berckx F, Battenberg K et al. Frankia-enriched metagenomes from the earliest diverging symbiotic Frankia cluster: they come in teams. Genome Biol Evol 2019; 11:2273–2291 [View Article] [PubMed]
    [Google Scholar]
  24. Mirza MS, Hahn D, Akkermans ADL. Isolation and characterization of Frankia strains from Coriaria nepalensis. Syst Appl Microbiol 1992; 15:289–295 [View Article]
    [Google Scholar]
  25. Hahn D, Starrenburg MJC, Akkermans ADL. Variable compatibility of cloned Alnus glutinosa ecotypes against ineffective Frankia strains. Plant Soil 1988; 107:233–243 [View Article]
    [Google Scholar]
  26. Lechevalier MP, Ruan JS. Physiology and chemical diversity of Frankia spp. isolated from nodules of Comptonia peregrina (L.) Coult. and Ceanothus americanus L. Plant Soil 1984; 78:15–22 [View Article]
    [Google Scholar]
  27. Mirza MS, Janse JD, Hahn D, Akkermans ADL. Identification of atypical Frankia strains by fatty acid analysis. FEMS Microbiol Lett 1991; 83:91–98 [View Article]
    [Google Scholar]
  28. Gtari M, Nouioui I, Sarkar I, Ghodhbane-Gtari F, Tisa LS et al. An update on the taxonomy of the genus Frankia Brunchorst, 1886, 174AL. Antonie van Leeuwenhoek 2019; 112:5–21 [View Article] [PubMed]
    [Google Scholar]
  29. 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]
  30. Ben Tekaya S, Guerra T, Rodriguez D, Dawson JO, Hahn D. Frankia diversity in host plant root nodules is independent of abundance or relative diversity of Frankia populations in corresponding rhizosphere soils. Appl Environ Microbiol 2018; 84:e02248-17 [View Article] [PubMed]
    [Google Scholar]
  31. Carlos-Shanley C, Guerra T, Hahn D. Draft genomes of non-nitrogen-fixing Frankia strains. J Genomics 2021; 9:68–75
    [Google Scholar]
  32. Goris J, Konstantinidis KT, Klappenbach JA, Coenye T, Vandamme P et al. DNA–DNA hybridization values and their relationship to whole-genome sequence similarities. Int J Syst Evol Microbiol 2007; 57:81–91 [View Article] [PubMed]
    [Google Scholar]
  33. Murry MA, Fontaine MS, Torrey JG. Growth kinetics and nitrogenase induction in Frankia sp. HFPArI 3 grown in batch culture. Plant Soil 1984; 78:61–78 [View Article]
    [Google Scholar]
  34. Guindon S, Gascuel O. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 2003; 52:696–704 [View Article] [PubMed]
    [Google Scholar]
  35. Felsenstein J. Confidence limits on phylogenies: an approach using the bootstrap. Evolution 1985; 39:783–791 [View Article] [PubMed]
    [Google Scholar]
  36. Guindon S, Dufayard J-F, Lefort V, Anisimova M, Hordijk W et al. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 2010; 59:307–321 [View Article] [PubMed]
    [Google Scholar]
  37. Parte AC, Carbasse JS, 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]
  38. 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]
  39. Pozzi AC, Bautista-Guerrero HH, Abby SS, Herrera-Belaroussi A, Abrouk D et al. Robust Frankia phylogeny, species delineation and intraspecies diversity based on Multi-Locus Sequence Analysis (MLSA) and Single-Locus Strain Typing (SLST) adapted to a large sample size. Syst Appl Microbiol 2018; 41:311–323 [View Article] [PubMed]
    [Google Scholar]
  40. Vallenet D, Calteau A, Cruveiller S, Gachet M, Lajus A et al. MicroScope in 2017: an expanding and evolving integrated resource for community expertise of microbial genomes. Nucleic Acids Res 2017; 45:D517–D528 [View Article] [PubMed]
    [Google Scholar]
  41. Medema MH, Blin K, Cimermancic P, de Jager V, Zakrzewski P et al. antiSMASH: rapid identification, annotation and analysis of secondary metabolite biosynthesis gene clusters in bacterial and fungal genome sequences. Nucleic Acids Res 2011; 39:W339–W346 [View Article] [PubMed]
    [Google Scholar]
  42. Vaas LAI, Sikorski J, Hofner B, Fiebig A, Buddruhs N et al. opm: an R package for analysing OmniLog® phenotype microarray data. Bioinformatics 2013; 29:1823–1824 [View Article] [PubMed]
    [Google Scholar]
  43. Schleifer KH, Kandler O. Peptidoglycan types of bacterial cell walls and their taxonomic implications. Bacteriol Rev 1972; 36:407–477 [View Article] [PubMed]
    [Google Scholar]
  44. Lechevalier MP, Lechevalier HA. Chemical composition as a criterion in the classification of aerobic actinomycetes. Int J Syst Bacteriol 1970; 20:435–443 [View Article]
    [Google Scholar]
  45. Staneck JL, Roberts GD. Simplified approach to identification of aerobic actinomycetes by thin-layer chromatography. Appl Microbiol 1974; 28:226–231 [View Article]
    [Google Scholar]
  46. 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 Meth 1984; 2:233–241 [View Article]
    [Google Scholar]
  47. Kroppenstedt RM, Goodfellow M. The family Thermomonosporaceae: Actinocorallia, Actinomadura, Spirillispora and Thermomonospora. In Dworkin F. eds The Prokaryotes: A Handbook on the Biology of BacteriaArchae, Bacteria Firmicutes, Actinomycetes, 3rd. edn vol 3 New York, NY, USA: Springer; 2006 pp 682–724 [View Article]
    [Google Scholar]
  48. 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: [View Article] [PubMed]
    [Google Scholar]
  49. Sasser M. Identification of bacteria by gas chromatography of cellular fatty acids. USFCC News 1990; 20:16
    [Google Scholar]
  50. Vieira S, Huber KJ, Neumann-Schaal M, Geppert A, Luckner M et al. Usitatibacter rugosus gen. 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]
  51. Cissoko M, Hocher V, Gherbi H, Gully D, Carré-Mlouka A et al. Actinorhizal signaling molecules: Frankia root hair deforming factor shares properties with NIN inducing factor. Front Plant Sci 2018; 9:1494 [View Article] [PubMed]
    [Google Scholar]
  52. Hameed S, Hafeez FY, Mirza MS, Malik KA, Akkermans ADL. Confirmation of an isolate from Datisca cannabina as atypical Frankia strain using PCR amplified 16S rRNA sequence analysis. Pak J Bot 1994; 26:247–251
    [Google Scholar]
  53. Ogasawara Y, Yackley BJ, Greenberg JA, Rogelj S, Melançon CE. Expanding our understanding of sequence–function relationships of type II polyketide biosynthetic gene clusters: bioinformatics-guided identification of frankiamicin A from Frankia sp. EAN1pec. PLoS One 2015; 10:e0121505 [View Article] [PubMed]
    [Google Scholar]
  54. Gerber NN, Lechevalier MP. Novel benzo[a]naphthacene quinones from an actinomycete, Frankia G-2 (ORS 020604). Can J Chem 1984; 62:2818–2821 [View Article]
    [Google Scholar]
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