1887

Abstract

strain Ag45/Mut15 was isolated from a root nodule of growing in a swamp at lake Grossensee, Germany. The strain forms root nodules on , in which it produces hyphae and clusters of N-fixing vesicles. N-fixing vesicles are also produced in nitrogen-free growth medium, in addition to hyphae and sporangia. The whole-cell hydrolysates of strain Ag45/Mut15 contained -diaminopimelic acid in the peptidoglycan and ribose, xylose, mannose, glucose, galactose and a trace of rhamnose as cell-wall sugars. The major polar lipids were phosphatidylglycerol, phosphatidylinositol, diphosphatidylglycerol and glyco-phospholipid. The predominant (>20 %) menaquinones were MK-9(H) and MK-9(H). The major fatty acid profile (>10 %) consisted of iso-C, C ω8 and C. Pairwise 16S rRNA gene distances showed that strain Ag45/Mut15 was most closely related to CpI1 and Frankia nodulisporulans with 16S rRNA gene similarity values of 0.001335 substitutions per site. An multilocus sequence analysis phylogeny based on , , , and amino acid sequences positioned the strain within cluster 1 of - and -nodulating species, close to F. nodulisporulans AgTrS and ARgP5. The digital DNA–DNA hybridization (dDDH) and average nucleotide identity (ANI) values between the studied strain Ag45/Mut15 and all validly named species were below the defined threshold for prokaryotic species demarcation. F. nodulisporulans AgTrS, which cannot be cultivated , was found to be the closest phylogenetic neighbour to strain strain Ag45/Mut15 with dDDH and ANI values of 61.8 and 97 %, respectively. Strain Ag45/Mut15 was not able to sporulate in nodule tissues like strain AgTrS.

Phenotypic, physiological and phylogenomic analyses confirmed the assignment of strain Ag45/Mut15 (=DSM 114737=LMG 326O1) to a novel species, with Ag45/Mut15 as type strain, for which the name sp. nov. is proposed.

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2023-06-23
2024-06-22
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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. Baker D, Torrey J. The isolation and cultivation of actinomycetous root nodule endophytes. In JC Gordon CW, Perry DA. eds Symbiotic Nitrogen Fixation in the Management of Temperate Forests Corvallis, OR: Forest Research Laboratory, Oregon State University; 1979 pp 38–56
    [Google Scholar]
  3. 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]
  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. 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. Botanical Gazette 1979; 140:S35–S43 [View Article]
    [Google Scholar]
  6. 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]
  7. 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]
  8. 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]
  9. Nouioui I, Ghodhbane-Gtari F, Montero-Calasanz M del C, 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]
    [Google Scholar]
  10. 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 2019; 112:57–65 [View Article]
    [Google Scholar]
  11. Nouioui I, Ghodhbane-Gtari F, Pötter G, Klenk HP, 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]
  12. 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]
  13. 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]
  14. 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]
  15. 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]
  16. Normand P, Pujic P, Abrouk D, Vemulapally S, Guerra T et al. Draft genomes of nitrogen-fixing Frankia strains Ag45/Mut15 and AgPM24 isolated from root nodules of Alnus Glutinosa. J Genomics 2022; 10:49–56 [View Article] [PubMed]
    [Google Scholar]
  17. 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]
  18. 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]
  19. 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]
  20. Felsenstein J. Confidence limits on phylogenies: an approach using the bootstrap. Evolution 1985; 39:783–791 [View Article] [PubMed]
    [Google Scholar]
  21. 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]
  22. Pritchard L, Glover RH, Humphris S, Elphinstone JG, Toth IK. Genomics and taxonomy in diagnostics for food security: soft-rotting enterobacterial plant pathogens. Anal Methods 2016; 8:12–24 [View Article]
    [Google Scholar]
  23. 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]
  24. 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]
  25. Huerta-Cepas J, Szklarczyk D, Forslund K, Cook H, Heller D et al. eggNOG 4.5: a hierarchical orthology framework with improved functional annotations for eukaryotic, prokaryotic and viral sequences. Nucleic Acids Res 2016; 44:D286–93 [View Article] [PubMed]
    [Google Scholar]
  26. 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:W339–46 [View Article] [PubMed]
    [Google Scholar]
  27. Vaas LAI, Sikorski J, Hofner B, Fiebig A, Buddruhs N et al. opm: an R package for analysing OmniLog(R) phenotype microarray data. Bioinformatics 2013; 29:1823–1824 [View Article] [PubMed]
    [Google Scholar]
  28. 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]
  29. 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]
  30. 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]
  31. 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]
  32. Kroppenstedt RM, Goodfellow M. The family Thermomonosporaceae: Actinocorallia, Actinomadura, Spirillispora and Thermomonospora. In Dworkin F, Schleifer KH. eds The Prokaryotes: A Handbook on the Biology of Bacteria. Rosenberg and Stackebrandt. (Editor)Archae, Bacteria Firmicutes, Actinomycetes, 3rd edn. vol 3 New York, NY, USA: Springer; 2006 pp 682–724 [View Article]
    [Google Scholar]
  33. Schumann P, Kalensee F, Cao J, Criscuolo A, Clermont D et al. 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; 71:71 [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. 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. without the order Nitrosomonadales isolated from soil. Int J Syst Evol Microbiol 2021; 71:004631
    [Google Scholar]
  36. Lechevalier MP. Taxonomy of the genus Frankia (Actinomycetales). Int J Syst Bacteriol 1994; 44:1–8 [View Article]
    [Google Scholar]
  37. Mirza BS, Welsh A, Hahn D. Saprophytic growth of inoculated Frankia sp. in soil microcosms. FEMS Microbiol Ecol 2007; 62:280–289 [View Article] [PubMed]
    [Google Scholar]
  38. Mirza BS, Welsh A, Hahn D. Growth of Frankia strains in leaf litter-amended soil and the rhizosphere of a nonactinorhizal plant. FEMS Microbiol Ecol 2009; 70:132–141 [View Article] [PubMed]
    [Google Scholar]
  39. Kim Tiam S, Boubakri H, Bethencourt L, Abrouk D, Fournier P et al. Genomic insights of Alnus-infective Frankia strains reveal unique genetic features and new evidence on their host-restricted lifestyle. Genes 2023; 14:530 [View Article] [PubMed]
    [Google Scholar]
  40. McCutcheon JP, McDonald BR, Moran NA. Origin of an alternative genetic code in the extremely small and GC-rich genome of a bacterial symbiont. PLoS Genet 2009; 5:e1000565 [View Article] [PubMed]
    [Google Scholar]
  41. Samant SS, Dawson JO, Hahn D. Growth responses of indigenous Frankia populations to edaphic factors in actinorhizal rhizospheres. Syst Appl Microbiol 2015; 38:501–505 [View Article] [PubMed]
    [Google Scholar]
  42. Samant SS, Dawson JO, Hahn D. Growth responses of introduced Frankia strains to edaphic factors. Plant Soil 2016; 400:123–132 [View Article]
    [Google Scholar]
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