1887

INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY logo

Volume 70, Issue 10

Proposal of ' Frankia alpina', the uncultured symbiont of and that forms spore-containing nitrogen-fixing root nodules Free

Abstract

The members of the genus are, with a few exceptions, a group of nitrogen-fixing symbiotic actinobacteria that nodulate mostly woody dicotyledonous plants belonging to three orders, eight families and 23 genera of pioneer dicots. These bacteria have been characterized phylogenetically and grouped into four molecular clusters. One of the clusters, cluster 1 contains strains that induce nodules on spp. (), spp., spp. and spp. () that have global distributions. Some of these strains produce not only hyphae and vesicles, as other cluster 1 strains do, but also numerous sporangia in their host symbiotic tissues, hence their phenotype being described as spore-positive (Sp+). While Sp+ strains have resisted repeated attempts at cultivation, their genomes have recently been characterized and found to be different from those of all described species, being markedly smaller than their phylogenetic neighbours. We thus hereby propose to create a ' Frankia alpina' species for some strains present in nodules of and that grow in alpine environments at high altitudes or in subarctic environments at high latitudes.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): alder , spores and Symbiotic
Funding
This study was supported by the:
  • Division of Emerging Frontiers (US)
    • Principle Award Recipient: Aude Herrera-Belaroussi
© 2020 The Authors
Loading

Article metrics loading...

/content/journal/ijsem/10.1099/ijsem.0.004433
2020-09-10
2024-04-24
Loading full text...

Full text loading...

/deliver/fulltext/ijsem/70/10/5453.html?itemId=/content/journal/ijsem/10.1099/ijsem.0.004433&mimeType=html&fmt=ahah

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. Soltis DE, Soltis PS, Morgan DR, Swensen SM, Mullin BC et al. Chloroplast gene sequence data suggest a single origin of the predisposition for symbiotic nitrogen fixation in angiosperms. Proc Natl Acad Sci U S A 1995; 92:2647–2651 [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. Pozzi AC, Roy M, Nagati M, Schwob G, Manzi S et al. Patterns of diversity, endemism and specialization in the root symbiont communities of alder species on the island of Corsica. New Phytol 2018; 219:336–349 [View Article][PubMed]
     [Google Scholar]
  5. Normand P, Fernandez MP, Brunchorst F. Frankia Brunchorst 1886, 174AL . In Whitman W, Goodfellow M, DeVos Paul, Dedysh Svetlana, Hedlund Brian. (editors) Bergey’s Manual of Systematics of Archaea and Bacteria, Online John Wiley & Sons, Inc., in association with Bergey’s Manual Trust; 2019 In press
    [Google Scholar]
  6. Pommer E. Über die Isolierung des Endophyten aus den Wurzelknöllchen Alnus glutinosa Gaertn. und uber erfolgreiche Re-Infektionsversuche. Ber Deutsch Botan Gesell 1959; 72:138–150
     [Google Scholar]
  7. 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]
  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 2019; 112:57-65 [View Article][PubMed]
     [Google Scholar]
  9. 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]
  10. 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]
  11. 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]
  12. 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]
  13. 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]
  14. 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]
  15. 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; 68:30013011 [View Article][PubMed]
     [Google Scholar]
  16. Nouioui I, Ghodhbane-Gtari F, Rohde M, Klenk H-P, 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]
  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
     [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, 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]
  20. 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]
  21. 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
     [Google Scholar]
  22. Normand P, Nguyen TV, Battenberg K, Berry AM, Heuvel BV, Vanden Heuvel B 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]
  23. 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]
  24. 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]
  25. 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]
  26. Peklo J. Die pflanzlichen Aktinomykosen. Centralbl Bakteriol Parasit II 1910; 27:451–579
     [Google Scholar]
  27. Dijk C, Simmer A, Weber A. Host range differentiation of spore-positive and spore-negative strain types of Frankia in stands of Alnus glutinosa and Alnus incana in Finland. Physiol Plant 1988; 72:349–358 [View Article]
     [Google Scholar]
  28. Schwintzer CR. Spore-positive and spore-negative nodules. In Schwintzer CR, Tjepkema JD. (editors) The Biology of Frankia and Actinorhizal Plants San Diego: Academic Press, Inc; 1990 pp 177–193
     [Google Scholar]
  29. Simonet P, Bosco M, Chapelon C, Moiroud A, Normand P. Molecular characterization of Frankia microsymbionts from spore-positive and spore-negative nodules in a natural alder stand. Appl Environ Microbiol 1994; 60:1335–1341 [View Article][PubMed]
     [Google Scholar]
  30. 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]
  31. Bautista GHH, 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]
  32. Kurdali F, Rinaudo G, Moiroud A, Domenach AM. Competition for nodulation and 15N2-fixation between a Sp+ and a Sp − Frankia strain in Alnus incana . Soil Biol Biochem 1990; 22:57–64 [View Article]
     [Google Scholar]
  33. Cotin-Galvan L, Pozzi AC, Schwob G, Fournier P, Fernandez MP et al. In-planta sporulation capacity enhances infectivity and rhizospheric competitiveness of Frankia strains. Microbes Environ 2016; 31:11–18 [View Article][PubMed]
     [Google Scholar]
  34. 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]
  35. Bethencourt L, Boubakri H, Taib N, Normand P, Armengaud J et al. Comparative genomics and proteogenomics of Frankia sporulation. Res Microbiol 2019; S0923-2508:30038–30035
     [Google Scholar]
  36. Tisa LS, Beauchemin N, Gtari M, Sen A, Wall LG. What stories can the Frankia genomes start to tell us?. J Biosci 2013; 38:719–726 [View Article][PubMed]
     [Google Scholar]
  37. Bethencourt L, Vautrin F, Taib N, Dubost A, Castro-Garcia L et al. Draft genome sequences for three unisolated Alnus-infective Frankia Sp+ strains, AgTrS, AiOr and AvVan, the first sequenced Frankia strains able to sporulate in-planta . J Genomics 2019; 7:50–55 [View Article][PubMed]
     [Google Scholar]
  38. 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]
  39. 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]
  40. 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]
  41. Felsenstein J. Confidence limits on phylogenies: an approach using the bootstrap. Evolution 1985; 39:783–791 [View Article][PubMed]
     [Google Scholar]
  42. 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]
  43. Schwob G, Roy M, Pozzi AC, Herrera-Belaroussi A, Fernandez MP. In planta sporulation of Frankia spp. as a determinant of alder-symbiont interactions. Appl Environ Microbiol 2018; 84:e01737–01718 [View Article][PubMed]
     [Google Scholar]
  44. Navarro E, Bousquet J, Moiroud A, Munive A, Piou D et al. Molecular phylogeny of Alnus (Betulaceae), inferred from nuclear ribosomal DNA ITS sequences. Plant Soil 2003; 254:207–217 [View Article]
     [Google Scholar]
  45. Schwob G, Roy M, Manzi S, Pommier T, Fernandez MP. Green alder (Alnus viridis) encroachment shapes microbial communities in subalpine soils and impacts its bacterial or fungal symbionts differently. Environ Microbiol 2017; 19:3235–3250 [View Article][PubMed]
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/ijsem/10.1099/ijsem.0.004433
Loading
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 70, 5453 (2020); https://doi.org/10.1099/ijsem.0.004433
/content/journal/ijsem/10.1099/ijsem.0.004433
/content/journal/ijsem/10.1099/ijsem.0.004433
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF

Most cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error