1887

Abstract

Strain ARgP5, an actinobacterium isolated from a root nodule present on an Alnus incana subspecies rugosa shrub growing in Quebec City, Canada, was the subject of polyphasic taxonomic studies to clarify its status within the genus Frankia . 16S rRNA gene sequence similarities and ANI values between ARgP5 and type strains of species of the genus Frankia with validly published names were 98.8 and 82 % or less, respectively. The in silico DNA G+C content was 72.4 mol%. ARgP5 is characterised by the presence of meso-A2pm, galactose, glucose, mannose, rhamnose (trace), ribose and xylose as whole-organism hydrolysates; MK-9(H8) as predominant menaquinone; diphosphatidylglycerol, phosphatidylinositol and phosphatidylglycerol as polar lipids and iso-C16 : 0 and C17 : 1ω8c as major fatty acids. The proteomic results confirmed the distinct position of ARgP5 from its closest neighbours in Frankia cluster 1. ARgP5 was found to be infective on two alder (Alnus glutinosa and Alnusalnobetula subsp. crispa) and on one bayberry (Morella pensylvanica) species and to fix nitrogen in symbiosis and in pure culture. On the basis of phylogenetic (16S rRNA gene sequence), genomic, proteomic and phenotypic results, strain ARgP5 (=DSM 45898=CECT 9033) is considered to represent a novel species within the genus Frankia for which the name Frankia canadensis sp. nov., is proposed.

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2018-07-30
2024-12-14
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References

  1. Benson DR, Silvester WB. Biology of Frankia strains, actinomycete symbionts of actinorhizal plants. Microbiol Rev 1993; 57:293–319[PubMed]
    [Google Scholar]
  2. Smolander A, Sundman V. Frankia in acid soils of forests devoid of actinorhizal plants. Physiol Plant 1987; 70:297–303 [View Article]
    [Google Scholar]
  3. Tisa L, McBride M, Ensign JC. Studies on growth and morphology of Frankia strains EAN1pec, EuI1c, CpI1 and ACN1AG. Can J Bot 1983; 61:2768–2773
    [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. 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]
  6. 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]
  7. 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]
  8. 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]
  9. 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]
  10. 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]
  11. 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]
  12. 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]
  13. Rodriguez-Barrueco C, Bond G. A discussion of the results of cross-inoculation trials between Alnus glutinosa and Myrica gale. In Nutman P. (editor) Symbiotic Nitrogen Fixation in Plants London: Cambridge Univ. Press; 1976 pp. 561–566
    [Google Scholar]
  14. Anne-Emmanuelle H, Hasna B, Antoine B, Marjolaine R, Guillaume M et al. Control of endophytic Frankia sporulation by Alnus nodule metabolites. Mol Plant Microbe Interact 2017; 30:205–214 [View Article][PubMed]
    [Google Scholar]
  15. Carro L, Pujic P, Alloisio N, Fournier P, Boubakri H et al. Alnus peptides modify membrane porosity and induce the release of nitrogen-rich metabolites from nitrogen-fixing Frankia. ISME J 2015; 9:1723–1733 [View Article][PubMed]
    [Google Scholar]
  16. Oshone R, Hurst SG, Abebe-Akele F, Simpson S, Morris K et al. Permanent draft genome sequences for two variants of Frankia sp. strain CpI1, the first Frankia strain isolated from root nodules of Comptonia peregrina. Genome Announc 2016; 4:e01588-15 [View Article][PubMed]
    [Google Scholar]
  17. Lalonde M. Immunological and ultrastructural demonstration of nodulation of the European Alnus glutinosa (L.) Gaertn. host plant by an actinomycetal isolate from the North American Comptonia peregrina (L.) Coult. root nodule. Bot Gaz 1979; 140:S35–S43 [View Article]
    [Google Scholar]
  18. Hahn D, Lechevalier MP, Fischer A, Stackebrandt E. Evidence for a close phylogenetic relationship between members of the genera Frankia, Geodermatophilus, and “Blastococcus” and emdendation of the family Frankiaceae. Syst Appl Microbiol 1989; 11:236–242 [View Article]
    [Google Scholar]
  19. 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]
  20. Fernandez MP, Meugnier H, Grimont PAD, Bardin R. Deoxyribonucleic acid relatedness among members of the genus Frankia. Int J Syst Bacteriol 1989; 39:424–429 [View Article]
    [Google Scholar]
  21. Pozzi A, Bautista-Guerrero HH, Abby SS, Herrera-Belaroussi A, Abrouk D et al. Multi-locus sequence analysis and extensive sampling bring new insights on Frankia phylogeny and phylogeography. Syst Appl Microbiol 2018; 41:311–323
    [Google Scholar]
  22. Bell CD, Soltis DE, Soltis PS. The age and diversification of the angiosperms re-revisited. Am J Bot 2010; 97:1296–1303 [View Article][PubMed]
    [Google Scholar]
  23. Normand P, Lalonde M. Evaluation of Frankia strains isolated from provenances of two Alnus species. Can J Microbiol 1982; 28:1133–1142 [View Article]
    [Google Scholar]
  24. Dijk C. Spore formation and endophyte diversity in root nodules of Alnus glutinosa (L.) VILL. New Phytol 1978; 81:601–615 [View Article]
    [Google Scholar]
  25. Pozzi AC, Bautista-Guerrero HH, Nouioui I, Cotin-Galvan L, Pepin R et al. In-planta sporulation phenotype: a major life history trait to understand the evolution of Alnus-infective Frankia strains. Environ Microbiol 2015; 17:3125–3138 [View Article][PubMed]
    [Google Scholar]
  26. 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]
  27. 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]
  28. Staneck JL, Roberts GD. Simplified approach to identification of aerobic actinomycetes by thin-layer chromatography. Appl Microbiol 1974; 28:226–231[PubMed]
    [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. Collins MD. Analysis of isoprenoid quinones. In Gottschalk G. (editor) Methods in Microbiology vol. 18 London, NY: Academic Press; 1985 pp. 329–366
    [Google Scholar]
  31. Kroppenstedt RM. Fatty acid and menaquinone analysis of actinomycetes and related organisms. In Goodfellow M, Minnikin DE. (editors) Chemical Methods in Bacterial Systematics London: Academic Press; 1985 pp. 173–199
    [Google Scholar]
  32. 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]
  33. 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]
  34. Sasser M. Identification of bacteria by gas chromatography of cellular fatty acids. USFCC Newsl 1990; 20:16
    [Google Scholar]
  35. Mort A, Normand P, Lalonde M. 2-O-methyl-d-mannose, a key sugar in the taxonomy of Frankia. Can J Microbiol 1983; 29:993–1002
    [Google Scholar]
  36. Vaas LA, 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]
  37. Pujic P, Bolotin A, Fournier P, Sorokin A, Lapidus A et al. Genome sequence of the atypical symbiotic Frankia R43 strain, a nitrogen-fixing and hydrogen-producing actinobacterium. Genome Announc 2015; 3:e01387-15 [View Article][PubMed]
    [Google Scholar]
  38. Nurk S, Bankevich A, Antipov D, Gurevich AA, Korobeynikov A et al. Assembling single-cell genomes and mini-metagenomes from chimeric MDA products. J Comput Biol 2013; 20:714–737 [View Article][PubMed]
    [Google Scholar]
  39. Boetzer M, Henkel CV, Jansen HJ, Butler D, Pirovano W. Scaffolding pre-assembled contigs using SSPACE. Bioinformatics 2011; 27:578–579 [View Article][PubMed]
    [Google Scholar]
  40. Overbeek R, Olson R, Pusch GD, Olsen GJ, Davis JJ et al. The SEED and the Rapid Annotation of microbial genomes using Subsystems Technology (RAST). Nucleic Acids Res 2014; 42:D206–D214 [View Article][PubMed]
    [Google Scholar]
  41. Chun J, Rainey FA. Integrating genomics into the taxonomy and systematics of the Bacteria and Archaea. Int J Syst Evol Microbiol 2014; 64:316–324 [View Article][PubMed]
    [Google Scholar]
  42. Corpet F, Gouzy J, Kahn D. The ProDom database of protein domain families. Nucleic Acids Res 1998; 26:323–326 [View Article][PubMed]
    [Google Scholar]
  43. Hotelling H. Analysis of a complex of statistical variables into principal components. J Educ Psychol 1933; 24:417–441 [View Article]
    [Google Scholar]
  44. 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]
  45. Galtier N, Gouy M, Gautier C. SEAVIEW and PHYLO_WIN: two graphic tools for sequence alignment and molecular phylogeny. Comput Appl Biosci 1996; 12:543–548 [View Article][PubMed]
    [Google Scholar]
  46. 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]
  47. Felsenstein J. Confidence limits on phylogenies: an approach using the bootstrap. Evolution 1985; 39:783–791 [View Article][PubMed]
    [Google Scholar]
  48. Hahn D, Mirza B, Benagli C, Vogel G, Tonolla M. Typing of nitrogen-fixing Frankia strains by matrix-assisted laser desorption ionization-time-of-flight (MALDI-TOF) mass spectrometry. Syst Appl Microbiol 2011; 34:63–68 [View Article][PubMed]
    [Google Scholar]
  49. Vandroemme J, Cottyn B, Pothier JF, Pflüger V, Duffy B et al. Xanthomonas arboricola pv. fragariae : what's in a name?. Plant Pathol 2013; 62:1123–1131 [View Article]
    [Google Scholar]
  50. Benzécri JP. L'Analyse des Données. Volume II. L'Analyse des Correspondances Paris, France: Dunod; 1973
    [Google Scholar]
  51. Lurthy T, Alloisio N, Fournier P, Anchisi S, Ponsero A et al. Molecular response to nitrogen starvation by Frankia alni ACN14a revealed by transcriptomics and functional analysis with a fosmid library in Escherichia coli. Res Microbiol 2018; 169:90–100 [View Article][PubMed]
    [Google Scholar]
  52. Vergnaud L, Chaboud A, Prin Y, Rougier M. Preinfection events in the establishment of Alnus–Frankia symbiosis: development of a spot inoculation technique. Plant Soil 1985; 87:67–78 [View Article]
    [Google Scholar]
  53. Swanson E, Oshone R, Simpson S, Morris K, Abebe-Akele F et al. Permanent draft genome sequence of Frankia sp. strain ACN1ag, a nitrogen-fixing actinobacterium isolated from the root nodules of Alnus glutinosa. Genome Announc 2015; 3:e01483-15 [View Article][PubMed]
    [Google Scholar]
  54. Normand P, Lapierre P, Tisa LS, Gogarten JP, Alloisio N et al. Genome characteristics of facultatively symbiotic Frankia sp. strains reflect host range and host plant biogeography. Genome Res 2007; 17:7–15 [View Article][PubMed]
    [Google Scholar]
  55. Swanson E, Oshone R, Simpson S, Morris K, Abebe-Akele F et al. Permanent draft genome sequence of Frankia sp. strain AvcI1, a nitrogen-fixing actinobacterium isolated from the root nodules of Alnus viridis subsp. crispa grown in Canada. Genome Announc 2015; 3:e01511-15 [View Article][PubMed]
    [Google Scholar]
  56. Oshone R, Hurst SG, Abebe-Akele F, Simpson S, Morris K et al. Permanent draft genome sequences for two variants of Frankia sp. strain CpI1, the first Frankia strain isolated from root nodules of Comptonia peregrina. Genome Announc 2016; 4:e01588-15 [View Article][PubMed]
    [Google Scholar]
  57. Sen A, Beauchemin N, Bruce D, Chain P, Chen A et al. Draft genome sequence of Frankia sp. strain QA3, a nitrogen-fixing actinobacterium isolated from the root nodule of Alnus nitida. Genome Announc 2013; 1:e00103-13 [View Article][PubMed]
    [Google Scholar]
  58. Mansour SR, Oshone R, Hurst SG, Morris K, Thomas WK et al. Draft genome sequence of Frankia sp. strain CcI6, a Salt-tolerant nitrogen-fixing actinobacterium isolated from the root nodule of Casuarina cunninghamiana. Genome Announc 2014; 2:e01205-13 [View Article][PubMed]
    [Google Scholar]
  59. Ghodhbane-Gtari F, Hurst SG, Oshone R, Morris K, Abebe-Akele F et al. Draft genome sequence of Frankia sp. strain BMG5.23, a salt-tolerant nitrogen-fixing actinobacterium isolated from the root nodules of Casuarina glauca grown in Tunisia. Genome Announc 2014; 2:e00520-14 [View Article][PubMed]
    [Google Scholar]
  60. Hurst SG, Oshone R, Ghodhbane-Gtari F, Morris K, Abebe-Akele F et al. Draft genome sequence of Frankia sp. strain Thr, a nitrogen-fixing actinobacterium isolated from the root nodules of Casuarina cunninghamiana grown in Egypt. Genome Announc 2014; 2:e00493-14 [View Article][PubMed]
    [Google Scholar]
  61. Ngom M, Oshone R, Hurst SG, Abebe-Akele F, Simpson S et al. Permanent draft genome sequence for Frankia sp. strain CeD, a nitrogen-fixing actinobacterium isolated from the root nodules of Casuarina equistifolia grown in Senegal. Genome Announc 2016; 4:e00265-16 [View Article][PubMed]
    [Google Scholar]
  62. Oshone R, Ngom M, Abebe-Akele F, Simpson S, Morris K et al. Permanent draft genome sequence of Frankia sp. strain Allo2, a salt-tolerant nitrogen-fixing Actinobacterium isolated from the root nodules of Allocasuarina. Genome Announc 2016; 4:e00388-16 [View Article][PubMed]
    [Google Scholar]
  63. Simonet P, Capellano A, Navarro E, Bardin R, Moiroud A. An improved method for lysis of Frankia with acharomopeptidase allows detection of new plasmids. Can J Microbiol 1984; 30:1292–1295 [View Article]
    [Google Scholar]
  64. Burggraaf AJP, Valstar J. Heterogeneity within Frankia sp. LDAgpl studied among clones and reisolates. Plant Soil 1984; 78:29–43 [View Article]
    [Google Scholar]
  65. Simonet P, Thi Le N, Moiroud A, Bardin R. Diversity of Frankia strains isolated from a single alder stand. Plant Soil 1989; 118:13–22 [View Article]
    [Google Scholar]
  66. Berry AM, Torrey JG. Isolation and characterization in vivo and in vitro of an actinomycetous endophyte from Alnus rubra Bong. In Gordon JC, Wheeler CT, Perry DA. (editors) Symbiotic Nitrogen Fixation in the Management of Temperate Forests Corvallis, OR: Forest Research Laboratory, Oregon State University; 1979 pp. 69–83
    [Google Scholar]
  67. Baker D, Pengelly WL, Torrey JG. Immunochemical analysis of relationships among isolated Frankiae (Actinomycetales). Int J Syst Bacteriol 1981; 31:148–151 [View Article]
    [Google Scholar]
  68. Dillon JT, Baker D. Variations in nitrogenase activity among pure-cultured Frankia strains tested on actinorhizal plants as an indication of symbiotic compatibility. New Phytol 1982; 92:215–219 [View Article]
    [Google Scholar]
  69. Wall LG, Beauchemin N, Cantor MN, Chaia E, Chen A et al. Draft genome sequence of Frankia sp. strain BCU110501, a nitrogen-fixing actinobacterium isolated from nodules of Discaria trinevis. Genome Announc 2013; 1:e00503-13 [View Article][PubMed]
    [Google Scholar]
  70. 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]
  71. Puppo A, Dimitrijevic L, Diem HG, Dommergues YR. Homogeneity of superoxide dismutase patterns in Frankia strains from Casuarinaceae. FEMS Microbiol Lett 1985; 30:43–46 [View Article]
    [Google Scholar]
  72. Bautista GH, Cruz HA, Nesme X, Valdés M, Mendoza HA et al. Genomospecies identification and phylogenomic relevance of AFLP analysis of isolated and non-isolated strains of Frankia spp. Syst Appl Microbiol 2011; 34:200–206 [View Article][PubMed]
    [Google Scholar]
  73. Diem HG, Dommergues Y. The isolation of Frankia from nodules of Casuarina. Can J Bot 1983; 61:2822–2825 [View Article]
    [Google Scholar]
  74. 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]
  75. Nguyen TV, Wibberg D, Battenberg K, Blom J, vanden Heuvel B et al. An assemblage of Frankia cluster II strains from California contains the canonical nod genes and also the sulfotransferase gene nodH. BMC Genomics 2016; 17:796 [View Article][PubMed]
    [Google Scholar]
  76. Bloom RA, Lechevalier MP. Physiological, chemical, morphological, and plant infectivity characteristics of Frankia isolates from Myrica pensylvanica: correlation to DNA restriction patterns. Appl Env Microbiol 1989; 55:2161–2166
    [Google Scholar]
  77. Lechevalier MP, Lechevalier HA. The taxonomic position of the actinomycetic endophytes. In Gordon JC, Wheeler CT, Perry DA. (editors) Symbiotic Nitrogen Fixation in the Management of Temperate Forests Forest Research Laboratory, Oregon State University: Corvallis, OR; 1979 pp. 111–121
    [Google Scholar]
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