Abstract
Actinorhizal plants have been found in eight genera belonging to three orders (Fagales, Rosales and Cucurbitales). These all bear root nodules inhabited by bacteria identified as the nitrogen-fixing actinobacterium Frankia. These nodules all have a peripheral cortex with enlarged cells filled with Frankia hyphae and vesicles. Isolation in pure culture has been notoriously difficult, due in a large part to the growth of fast-growing contaminants where, it was later found, Frankia was slow-growing. Many of these contaminants, which were later found to be Micromonospora, were obtained from Casuarina and Coriaria. Our study was aimed at determining if Micromonospora were also present in other actinorhizal plants. Nodules from Alnus glutinosa, Alnus viridis, Coriaria myrtifolia, Elaeagnus x ebbingei, Hippophae rhamnoides, Myrica gale and Morella pensylvanica were tested and were all found to contain Micromonospora isolates. These were found to belong to mainly three species: Micromonospora lupini, Micromonospora coriariae and Micromonospora saelicesensis. Micromonospora isolates were found to inhibit some Frankia strains and to be innocuous to other strains.
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References
Atlas RM 1993 Handbook of microbiological media (Boca Raton, FL: CRC Press)
Baker D and Torrey J 1979 The isolation and cultivation of actinomycetous root nodule endophytes; in Symbiotic nitrogen fixation in the management of temperate forests (eds) JC Gordon, CT Wheeler, DA Perry and OR Corvallis (Oregon State University, Forest Research Laboratory) pp 38–56
Benson DR and Silvester WB 1993 Biology of Frankia strains, actinomycete symbionts of actinorhizal plants. Microbiol. Rev. 57 293–319
Berdy J 2005 Bioactive microbial metabolites. J. Antibiot. 58 1–26
Callaham D, Del Tredici P and Torrey J 1978 Isolation and cultivation in vitro of the actinomycete causing root nodulation in Comptonia. Science 199 899–902
Carro L, Sproer C, Alonso P and Trujillo ME 2012a Diversity of Micromonospora strains isolated from nitrogen fixing nodules and rhizosphere of Pisum sativum analyzed by multilocus sequence analysis. Syst. Appl. Microbiol. 35 73–80
Carro L, Pukall R, Spröer C, Kroppenstedt RM and Trujillo ME 2012b Micromonospora cremea sp. nov. and Micromonospora zamorensis sp. nov., isolated from the rhizosphere of Pisum sativum. Int. J. Syst. Evol. Microbiol. 62 2971–2977
Carro L, Pukall R, Spröer C, Kroppenstedt RM and Trujillo ME 2013 Micromonospora halotolerans sp. nov., isolated from the rhizosphere of a Pisum sativum plant. Antonie Van Leeuwenhoek 103 1245–1254
Ceremonie H, Debelle F and Fernandez MP 1999 Structural and functional comparison of Frankia root hair deforming factor and rhizobia Nod factor. Can. J. Bot. 77 1293–1301
Coombs JT and Franco CM 2003 Isolation and identification of actinobacteria from surface-sterilized wheat roots. Appl. Environ. Microbiol. 69 5603–5608
Felsenstein J 1985 Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39 783–791
Fernandez M, Meugnier H, Grimont P and Bardin R 1989 Deoxyribonucleic acid relatedness among members of the genus Frankia. Int. J. Syst. Bacteriol. 39 424–429
Furumai T, Takagi K, Igarashi Y, Saito N and Oki T 2000 Arisostatins A and B, new members of tetrocarcin class of antibiotics from Micromonospora sp. TP-A0316. I. Taxonomy, fermentation, isolation and biological properties. J. Antibiot. 53 227–232
Furumai T, Igarashi Y, Higuchi H, Saito N and Oki T 2002 Kosinostatin, a quinocycline antibiotic with antitumor activity from Micromonospora sp. TP-A0468. J. Antibiot. 55 128–133
Garcia LC, Martínez-Molina E abd Trujillo ME 2010 Micromonospora pisi sp. nov., isolated from root nodules of Pisum sativum. Int. J. Syst. Evol. Microbiol. 60 331–337
Gauthier D, Diem H and Dommergues Y 1981 In vitro nitrogen fixation by two actinomycete strains isolated from Casuarina nodules. Appl. Environ. Microbiol. 41 306–308
Genilloud O 2012 Genus I. Micromonospora; in Bergey's manual of systematic bacteriology: The Actinobacteria 2nd edition (eds) M Goodfellow, P Kämpfer, H-J Busse, ME Trujillo, KI Suzuki, W Ludwig and WB Whitman (Athens, GA: Bergey's Manual Trust, Springer) pp 1039–1057
Gherbi H, Markmann K, Svistoonoff S, Estevan J, Autran D, Giczey G, Auguy F, Peret B, et al. 2008 SymRK defines a common genetic basis for plant root endosymbioses with arbuscular mycorrhiza fungi, rhizobia, and Frankia bacteria. Proc. Natl. Acad. Sci. USA 105 4928–4932
Hall TA 1999 BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp. Ser. 41 95–98
Hammad Y, Nalin R, Marechal J, Fiasson K, Pepin R, Berry AM, Normand P and Domenach A-M 2003 A possible role for phenylacetic acid (PAA) in Alnus glutinosa nodulation by Frankia. Plant Soil 254 193–205
Hocher V, Alloisio N, Auguy F, Fournier P, Doumas P, Pujic P Gherbi H, Queiroux C, et al. 2011 Transcriptomics of actinorhizal symbioses reveals homologs of the whole common symbiotic signaling cascade. Plant Physiol. 156 1–12
Igarashi Y, Higuchi H, Oki T and Furumai T 2002 NMR analysis of quinocycline antibiotics: structure determination of kosinostatin, an antitumor substance from Micromonospora sp. TP-A0468. J. Antibiot. 55 134–140
Igarashi Y, Miyanaga S, Onaka H, Takeshita M and Furumai T 2005 Revision of the structure assigned to the antibiotic BU-4664L from Micromonopora. J. Antibiot. 58 350–352
Igarashi Y, Takagi K, Kan Y, Fujii K, Harada K, Furumai T and Oki T 2000 Arisostatins A and B, new members of tetrocarcin class of antibiotics from Micromonospora sp. TP-A0316. II. Structure determination. J. Antibiot. 53 233–240
Igarashi Y, Ogura H, Furihata K, Oku N, Indananda C and Thamchaipenet A 2011a Maklamicin, an antibacterial polyketide from an endophytic Micromonospora sp. J. Nat. Prod. 74 670–674
Igarashi Y, Yanase S, Sugimoto K, Enomoto M, Miyanaga S, Trujillo ME Saiki I and Kuwahara S 2011b Lupinacidin C, an inhibitor of tumor cell invasion from Micromonospora lupini. J. Nat. Prod. 74 862–865
Igarashi Y, Trujillo ME, Martinez-Molina E, Yanase S, Miyanaga S, Obata T, Sakurai H, Saiki I, Fujita T and Furumai T 2007 Antitumor anthraquinones from an endophytic actinomycete Micromonospora lupini sp. nov. Bioorg. Med. Chem. Lett. 17 3702–3705
Kim TU, Cho SH, Han JH, Shin YM, Lee HB and Kim SB 2012a Diversity and physiological properties of root endophytic actinobacteria in native herbaceous plants of Korea. J. Microbiol. 50 50–57
Kim OS, Cho YJ, Lee K, Yoon SH, Kim M, Na H, Park SC, Jeon YS, Lee JH, Yi H, Won S and Chun J 2012b Introducing EzTaxon-e: a prokaryotic 16S rRNA Gene sequence database with phylotypes that represent uncultured species. Int. J. Syst. Evol. Microbiol. 62 716–721
Kimura M 1980 A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J. Mol. Evol. 16 111–120
Kirby BM and Meyers PR 2010 Micromonospora tulbaghiae sp. nov., isolated from the leaves of wild garlic, Tulbaghia violacea. Int. J. Syst. Evol. Microbiol. 60 1328–1333
Li L, Tang YL, Wei B, Xie QY, Deng Z and Hong K 2012 Micromonospora sonneratiae sp. nov., isolated from a root of Sonneratia apetala. Int. J. Syst. Evol. Microbiol. 63 2383
Mirza M, Janse J, Hahn D and Akkermans A 1991 Identification of atypical Frankia strains by fatty acid analysis. FEMS Microbiol. Lett. 83 91–98
Mort A, Normand P and Lalonde M 1983 2-O-methyl-D-mannose, a key sugar in the taxonomy of Frankia. Can. J. Microbiol. 29 993–1002
Murry M, Fontaine M and Torrey J 1984 Growth kinetics and nitrogenase induction in Frankia sp. HFPArI3 grown in batch culture. Plant Soil 78 61–78
Normand P and Lalonde M 1982 Evaluation of Frankia strains isolated from provenances of two Alnus species. Can. J. Microbiol. 28 1133–1142
Normand P and Benson DR 2012 Genus I Frankia Brunchorst 1886, 174AL; in Bergey's manual of systematic bacteriology, The actinobacteria (eds) M Goodfellow, P Kämpfer, H-J Busse, ME Trujillo, W Ludwig, and Suzuki KI (New York: Bergey's Manual Trust, Springer) pp 512–520
Normand P, Orso S, Cournoyer B, Jeannin P, Chapelon C, Dawson J, Evtushenko L, Misra AK 1996 Molecular phylogeny of the genus Frankia and related genera and emendation of the family Frankiaceae. Int. J. Syst. Bacteriol. 46 1–9
Normand P, Lapierre P, Tisa LS, Gogarten JP, Alloisio N, Bagnarol E, Bassi CA, Berry AM, et al. 2007 Genome characteristics of facultatively symbiotic Frankia sp. strains reflect host range and host plant biogeography. Genome Res. 17 7–15
Orskov J 1923 Investigations into the morphology of the ray fungi (Copenhagen: Denmark: Levin and Munksgaard)
Persson T, Benson DR, Normand P, Vanden Heuvel B, Pujic P, Chertkov O, Teshima H, Bruce DC, et al. 2011 Genome sequence of "Candidatus Frankia datiscae" Dg1, the uncultured microsymbiont from nitrogen-fixing root nodules of the dicot Datisca glomerata. J. Bacteriol. 193 7017–7018
Pommer E 1959 Uber die Isolierung des Endophyten aus den Wurzelknöllchen Alnus glutinosa Gaertn. und uber erfolgreiche Re-Infektionsversuche. Ber. Deutsch. Botan. Gesell. 72 138–150
Pujic P, Fournier P, Alloisio N, Hay AE, Marechal J, Anchisi S and Normand P 2012 Lectin genes in the Frankia alni genome. Arch. Microbiol. 194 47–56
Rivas R, Sanchez M, Trujillo ME, Zurdo-Pineiro JL, Mateos PF, Martinez-Molina E and Velazquez E 2003 Xylanimonas cellulosilytica gen. nov., sp. nov., a xylanolytic bacterium isolated from a decayed tree (Ulmus nigra). Int. J. Syst. Evol. Microbiol. 53 99–103
Saitou N and Nei M 1987 The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4 406–425
Simonet P, Navarro E, Rouvier C, Reddell P, Zimpfer J, Dawson J, Dommergues Y, Bardin R, Combarro P, Hamelin J, Domenach A-M, Gourbière F, Prin Y and Normand P 1999 Co-evolution between Frankia populations and host plants in the family Casuarinaceae and consequent patterns of global dispersal. Environ. Microbiol. 1 525-535
Solans M 2007 Discaria trinervis – Frankia symbiosis promotion by saprophytic actinomycetes. J. Basic Microbiol. 47 243–250
Stevens G and Berry A 1988 Cytokinin secretion by Frankia sp. HFPArI3 in defined medium. Plant Physiol. 87 15–16
Tamura K, Dudley J, Nei M and Kumar S 2007 MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol. Biol. Evol. 24 1596–1599
Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F and Higgins DG 1997 The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 25 4876–4882
Trujillo M, Kroppenstedt R, Schumann P, Carro L and Martínez-Molina E 2006 Micromonospora coriariae sp. nov., isolated from root nodules of Coriaria myrtifolia. Int. J. Syst. Evol. Microbiol. 56 2381–2385
Trujillo ME, Kroppenstedt RM, Fernandez-Molinero C, Schumann P and Martinez-Molina E 2007 Micromonospora lupini sp. nov. and Micromonospora saelicesensis sp. nov., isolated from root nodules of Lupinus angustifolius. Int. J. Syst. Evol. Microbiol. 57 2799–2804
Trujillo ME, Alonso-Vega P, Rodriguez R, Carro L, Cerda E, Alonso P and Martinez-Molina E 2010 The genus Micromonospora is widespread in legume root nodules: the example of Lupinus angustifolius. Isme J. 4 1265–12581
Valdes M, Perez NO, Estrada-de Los Santos P, Caballero-Mellado J, Pena-Cabriales JJ, Normand P and Hirsch AM 2005 Non-Frankia actinomycetes isolated from surface-sterilized roots of Casuarina equisetifolia fix nitrogen. Appl. Environ. Microbiol. 71 460–466
Van Ghelue M, Lovaas E, Ringo E and Solheim B 1997 Early interactions between Alnus glutinosa and Frankia strain ArI3. Production and specificity of root hair deformation factor(s). Physiol. Plant 99 579–587
Vincent JM 1970 The cultivation, isolation and maintenance of rhizobia; in A manual for the practical study of root nodule bacteria (ed) JM Vincent (Oxford: Blackwell Scientific) pp 1–13
Wang C, Xu XX, Qu Z, Wang HL, Lin HP, Xie QY, Ruan JS and Hong K 2011 Micromonospora rhizosphaerae sp. nov., isolated from mangrove rhizosphere soil. Int. J. Syst. Evol. Microbiol. 61 320–324
Zhang Z, Lopez MF and Torrey JG 1984 A comparison of cultural characteristics and infectivity of Frankia isolates from root nodules of Casuarina species. Plant Soil 78 79–90
Zhao K, Penttinen P, Guan T, Xiao J, Chen Q, Xu J, Lindstrom K, Zhang L, Zhang X and Strobel GA 2011 The diversity and anti-microbial activity of endophytic actinomycetes isolated from medicinal plants in Panxi plateau, China. Curr. Microbiol. 62 182–190
Acknowledgments
Thanks are expressed to ANR Grant Sesam and MEC of the Spanish government for the postdoctoral fellowship to LC. MT acknowledges the grant MEC CGL2009-07287 from the Spanish government. We also thank Hugo Miettaux (Université de Lyon), María Fernandez (Université de Lyon) and Jean-Claude Cleyet-Marel (INRA, Montpellier) for the gift of biological material.
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[Carro L, Pujic P, Trujillo ME and Normand P 2013 Micromonospora is a normal occupant of actinorhizal nodules. J. Biosci. 38 1–9] DOI 10.1007/s12038-013-9359-y
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Carro, L., Pujic, P., Trujillo, M.E. et al. Micromonospora is a normal occupant of actinorhizal nodules. J Biosci 38, 685–693 (2013). https://doi.org/10.1007/s12038-013-9359-y
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DOI: https://doi.org/10.1007/s12038-013-9359-y