Diverse bacteria inhabit living hyphae of phylogenetically diverse fungal endophytes

Applied and Environmental Microbiology

Volumn 76, Issue 12, 2010, Pages 4063-4075

  Hoffman, Michele T ^a   Arnold, A Elizabeth ^a  

^a UNIVERSITY OF ARIZONA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ABIOTIC FACTORS; ENDOPHYTIC FUNGI; HOST PLANTS; MOLECULAR TECHNIQUES; PHOTOSYNTHETIC TISSUES; PHYLOGENETIC RELATIONSHIPS; PLANT GENOTYPE; PROTEOBACTERIA; SYMBIOTA; TREE SPECIES;

BACTERIOLOGY; FUNGI;

BACTERIA;

BACTERIAL DNA; BACTERIAL RNA; FUNGAL DNA; FUNGAL RNA; RIBOSOMAL SPACER DNA; RIBOSOME DNA; RIBOSOME RNA; RNA 16S; RNA, RIBOSOMAL, 26S;

BACTERIUM; BIOGEOGRAPHY; ENDOPHYTE; ENDOSYMBIONT; GENOTYPE; HOST PLANT; HOST-SYMBIONT INTERACTION; MICROSCOPY; MOLECULAR ANALYSIS; PHYLOGENETICS; PHYLOGENY; SOIL MICROORGANISM; SPECIES DIVERSITY; SPECIES OCCURRENCE; SPECIES RICHNESS; TAXONOMY;

ARTICLE; BACTERIAL PHENOMENA AND FUNCTIONS; BACTERIUM; BIODIVERSITY; CHEMISTRY; CLASSIFICATION; CLUSTER ANALYSIS; DNA SEQUENCE; FUNGUS; GENETICS; ISOLATION AND PURIFICATION; MICROBIOLOGY; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PHYLOGENY; PHYSIOLOGY; PLANT; RNA GENE; SYMBIOSIS; BACTERIA;

BACTERIA; BACTERIAL PHYSIOLOGICAL PHENOMENA; BIODIVERSITY; CLUSTER ANALYSIS; DNA, BACTERIAL; DNA, FUNGAL; DNA, RIBOSOMAL; DNA, RIBOSOMAL SPACER; FUNGI; GENES, RRNA; MOLECULAR SEQUENCE DATA; PHYLOGENY; PLANTS; RNA, BACTERIAL; RNA, FUNGAL; RNA, RIBOSOMAL; RNA, RIBOSOMAL, 16S; SEQUENCE ANALYSIS, DNA; SYMBIOSIS;

ASCOMYCOTA; BACILLACEAE; BACTERIA (MICROORGANISMS); BASIDIOMYCOTA; DOTHIDEOMYCETES; EUROTIOMYCETES; FUNGI; GLOMEROMYCOTA; MYCELIUM (GENUS); PEZIZOMYCETES; PROTEOBACTERIA; SORDARIOMYCETES;

EID: 77953624125     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.02928-09     Document Type: Article

References (72)

1. Arnold, A. E., J. Miadlikowska, K. L. Higgins, S. D. Sarvate, P. Gugger, A. Way, V. Hofstetter, F. Kauff, and F. Lutzoni. 2009. A phylogenetic estimation of trophic transition networks for ascomycetous fungi: are lichens cradles of symbiotrophic fungal diversification? Syst. Biol. 58:283-297.
2. Arnold, A. E., D. A. Henk, R. Eells, F. Lutzoni, and R. Vilgalys. 2007. Diversity and phylogenetic affinities of foliar fungal endophytes in loblolly pine inferred by culturing and environmental PCR. Mycologia 99:185-206.
3. Arnold, A. E., L. Mejfa, D. Kyllo, E. Rojas, Z. Maynard, N. A. Robbins, and E. A. Herre. 2003. Fungal endophytes limit pathogen damage in a tropical tree. Proc. Natl. Acad. Sci. U. S. A. 100:15649-15654.
4. Artursson, V., R. D. Finlay, and J. K. Jansson. 2005. Combined bromodeoxyuridine immunocapture and terminal-restriction fragment length polymorphism analysis highlights differences in the active soil bacterial metage- nome due to Glomus mosseae inoculation or plant species. Environ. Microbiol. 7:1952-1966. (Pubitemid 41752384)
5. Barbieri, E., L. Potenza, I. Rossi, D. Sisti, G. Giomaro, S. Rossetti, C. Beimfohr, and V. Stocchi. 2000. Phylogenetic characterization and in situ detection of a Cytophaga-Flexibacter-Bacteroides phylogroup bacterium in Tuber borchii Vittad. ectomycorrhizal mycelium. Appl. Environ. Microbiol. 66:5035-5042.
6. Barbieri, E., C. Guidi, J. Bertaux, P. Frey-Klett, J. Garbaye, P. Ceccaroli, R. Saltarelli, A. Zambonelli, and V. Stocchi. 2007. Occurrence and diversity of bacterial communities in Tuber magnátům during truffle maturation. Environ. Microbiol. 9:2234-2246.
7. Bertaux, J., M. Schmid, N. C. Prevost-Boure, J. L. Churin, A. Hartmann, J. Garbaye, and P. Frey-Klett. 2003. In situ identification of intracellular bacteria related to Paenibacillus spp. in the mycelium of the ectomycorrhizal fungus Laccarria bicolor S238N. Appl. Environ. Microbiol. 69:4243-4248. (Pubitemid 36870089)
8. Bertaux, J., M. Schmid, P. Hutzler, A. Hartmann, J. Garbaye, and P. FreyKlett. 2005. Occurrence and distribution of endobacteria in the plant-associated mycelium of the ectomycorrhizal fungus Lacearía bicolor S238N. Environ. Microbiol. 7:1786-1795. (Pubitemid 41532388)
9. Bianciotto, V., C. Bandi, D. Minerdi, M. Sironi, H. V. Tichy, and P. Bonfante. 1996. An obligately endosymbiotic mycorrhizal fungus itself harbors obligately intracellular bacteria. Appl. Environ. Microbiol. 62:3005-3010.
10. Bianciotto, V., E. Lumini, L. Lanfranco, D. Minerdi, P. Bonfante, and S. Perotto. 2000. Detection and identification of bacterial endosymbionts in arbuscular mycorrhizal fungi belonging to the family Gigasporaceae. Appl. Environ. Microbiol. 66:4503-4509.
11. Bianciotto, V., E. Lumini, P. Bonfante, and P. Vandamme. 2003. 'Candidatus Glomeribacter gigasporarum' gen. nov., sp. nov., an endosymbiont of arbuscular mycorrhizal fungi. Int. J. Syst. Evol. Microbiol. 53:121-124.
12. Bonfante, P., and I.-A. Anca. 2009. Plants, mycorrhizal fungi, and bacteria: a network of interactions. Annu. Rev. Microbiol. 63:363-383.
13. Cannone, J. J., S. Subramanian, M. N. Schnare, J. R. Collet, L. M. D'Souza, Y. Du, B. Feng, N. Lin, L. V. Madabusi, K. M. Muller, N. Pande, Z. Shang, N. Yu, and R. R. Gutell. 2002. The comparative RNA website (CRW): an online database of comparative sequence and structure information for ribosomal, intron, and other RNAs. BioMed. Cent. Bioinform. 3:15.
14. Carpenter-Boggs, L., T. E. Loynachan, and P. D. Stahl. 1995. Spore germination of Gigaspora margarita stimulated by volatiles of soil-isolated actinomycetes. Soil Biol. Biochem. 27:1445-1451.
15. Cole, J. R., B. Chai, R. J. Farris, Q. Wang, A. S. Kulam-Syed-Mohideen, D. M. McGarrell, A. M. Bandela, E. Cardenas, G. M. Garrity, and J. M. Tiedje. 2007. The Ribosomal Database Project (RDP-II): introducing myRDP space and quality controlled public data. Nucleic Acids Res. 35: D169-D172.
16. De Boer, W., L. B. Folman, R. C. Summerbell, and L. Boddy. 2005. Living in a fungal world: impact of fungi on soil bacterial niche development. FEMS Microbiol. Rev. 29:795-811.
17. DeSantis, T. Z., P. Hugenholtz, K. Keller, E. L. Brodie, N. Larsen, Y. M. Piceno, R. Phan, and G. L. Andersen. 2006. NAST: a multiple sequence alignment server for comparative analysis of 16S rRNA genes. Nucleic Acids Res. 34:W394-W399.
18. Ewing, B., and P. Green. 1998. Base-calling of automated sequencer traces using Phred. II. Error probabilities. Genome Res. 8:186-194.
19. Ewing, B., L. Hillier, M. Wendl, and P. Green. 1998. Base-calling of automated sequencer traces using Phred. I. Accuracy assessment. Genome Res. 8:175-185.
20. Farjon, A., C. N. Page, and N. Schellevis. 1993. A preliminary world list of threatened conifer taxa. Biodivers. Conserv. 2:304-326.
21. Farjon, A. 2008. A natural history of conifers. Timber Press, Portland, OR.
22. Fralish, J. S., and S. B. Franklin. 2002. Taxonomy and ecology of woody plants in North American forests. John Wiley and Sons, Inc., New York, NY.
23. Frey-Klett, P., J. Garbaye, and M. Tarkka. 2007. The mycorrhiza helper bacteria revisited. New Phytol. 176:22-36.
24. Fröhlich, J., and K. D. Hyde. 1999. Biodiversity of palm fungi in the tropics: are global fungal diversity estimates realistic? Biodivers. Conserv. 8:977-1004. (Pubitemid 29404848)
25. Gadek, P. A., D. L. Alpers, M. M. Heslewood, and C. J. Quinn. 2000. Relationships within Cupressaceae sensu lato: a combined morphological and molecular approach. Am. J. Bot. 87:1044-1057.
26. Garbaye, J. 1994. Helper bacteria-a new dimension to the mycorrhizal symbiosis. New Phytol. 128:197-210.
27. Gardes, M., and T. D. Bruns. 1993. ITS primers with enhanced specificity for basidiomycetes: application to the identification of mycorrhizae and rusts. Mol. Ecol. 2:113-118.
28. Hoffman, M. T. 2010. Bacterial endosymbionts of endophytic fungi: diversity, phylogenetic structure, and biotic interactions. Ph.D. dissertation. The University of Arizona, Tucson, AZ.
29. Hoffman, M. T., and A. E. Arnold. 2008. Geographic locality and host identity shape fungal endophyte communities in cupressaceous trees. Mycol. Res. 112:331-344.
30. Huelsenbeck, J. P., and F. Ronquist. 2001. MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17:754-755.
31. James, T. Y., F. Kauff, C. Schoch, P. B. Matheny, V. Hofstetter, C. Cox, G. Celio, C. Gueidan, E. Fraker, J. Miadlikowska, H. T. Lumbsch, A. Rauhut, V. Reeb, A. E. Arnold, A. Amtoft, J. E. Stajich, K. Hosaka, G.-H. Sung, D. Johnson, B. O'Rourke, M. Crockett, M. Binder, J. M. Curtis, J. C. Slot, Z. Wang, A. W. Wilson, A. Schüßler, J. E. Longcore, K. O'Donnell, S. MozleyStandridge, D. Porter, P. M. Letcher, M. J. Powell, J. W. Taylor, M. M. White, G. W. Griffith, D. R. Davies, R. A. Humber, J. B. Morton, J. Sugiyama, A. Y. Rossman, J. D. Rogers, D. H. Pfister, D. Hewitt, K. Hansen, S. Hambleton, R. A. Shoemaker, J. Kohlmeyer, B. Volkmann- Kohlmeyer, R. A. Spotts, M. Serdani, P. W. Crous, K. W. Hughes, K. Matsuura, E. Langer, G. Langer, W. A. Untereiner, R. Lücking, B. Büdel, D. M. Geiser, A. Aptroot, P. Diederich, I. Schmitt, M. Schultz, R. Yahr, D. Hibbett, F Lutzoni, D. McLaughlin, J. Spatafora, and R. Vilgalys. 2006. Reconstructing the early evolution of the fungi using a six gene phylogeny. Nature 443:818-822.
32. Kobayashi, D. Y., and J. A. Crouch. 2009. Bacterial/fungal interactions: from pathogens to mutualistic endosymbionts. Annu. Rev. Phytopathol. 47:63-82.
33. Lackner, G., N. Möbius, K. Scherlach, L. P. Partida-Martinez, R. Winkler, I. Schmitt, and C. Hertweck. 2009. Global distribution and evolution of a toxinogenic Burkholderia-Rhizopus symbiosis. Appl. Environ. Microbiol. 75: 2982-2986.
34. Lane, D. J. 1991. 16S/23S rRNA sequencing. In E. Stackebrandt and M. Goodfellow (ed.), Nucleic acid techniques in bacterial systematics. John Wiley and Sons, Inc., New York, NY.
35. Levy, A., B. J. Chang, L. K. Abbott, J. Kuo, G. Harnett, and T. J. J. Inglis. 2003. Invasion of spores of the arbuscular mycorrhizal fungus Gigaspora decipiens by Burkholderia spp. Appl. Environ. Microbiol. 69:6250-6256. (Pubitemid 37280351)
36. Little, D. P. 2006. Evolution and circumscription of the true cypresses (Cupressaceae: Cupressus). Syst. Bot. 31:461-480.
37. Ludwig, W., O. Strunk, R. Westram, L. Richter, H. Meier, Yadhukumar, A. Buchner, T. Lai, S. Steppi, G. Jobb, W. Förster, I. Brettske, S. Gerber, A. W. Ginhart, O. Gross, S. Grumann, S. Hermann, R. Jost, A. König, T. Liss, R. Lüssmann, M. May, B. Nonhoff, B. Reichel, R. Strehlow, A. Stamatakis, N. Stuckmann, A. Vilbig, M. Lenke, T. Ludwig, A. Bode, and K.-H. Schleifer. 2004. ARB: a software environment for sequence data. Nucleic Acids Res. 32:1363-1371. (Pubitemid 38854737)
38. Lumini, E., V. Bianciotto, P. Jargeat, M. Novero, A. Salvioli, A. Faccio, G. Bécard, and P. Bonfante. 2007. Presymbiotic growth and sporal morphology are affected in the arbuscular mycorrhizal fungus Gigaspora margarita cured of its endobacteria. Cell. Microbiol. 9:1716-1729.
39. MacDonald, R. M., and M. R. Chandler. 1981. Bacterium-like organelles in the vesicular-arbuscular mycorrhizal fungus Glomus caledonius. New Phytol. 89:241-246.
40. Maddison, D. R., and W. P. Maddison. 2005. ChromaSeq module. Mesquite: a modular system for evolutionary analysis. Version 1.06. http: //mesquiteproject.org/.
41. Maddison, W. P., and D. R. Maddison. 2009. Mesquite: a modular system for evolutionary analysis. Version 2.6. http://mesquiteproject.org/.
42. Manz, W., R. Amann, W. Ludwig, M. Wagner, and K.-H. Schleifer. 1992. Phylogenetic oligodeoxynucleotide probes for the major subclass of proteobacteria: problems and solutions. Syst. Appl. Microbiol. 15:593-600.
43. Márquez, L. M., R. S. Redman, R. J. Rodriguez, and M. J. Roossinck. 2007. A virus in a fungus in a plant: three-way symbiosis required for thermal tolerance. Science 315:513-517.
44. Minerdi, D., M. Moretti, G. Gilardi, C. Barberio, M. L. Gullino, and A. Garibaldi. 2008. Bacterial ectosymbionts and virulence silencing in a Fusarium oxysporum strain. Environ. Microbiol. 10:1725-1741.
45. Mirabal-Alonso, L., and E. Ortega-Delgado. 2007. Phosphate solubilizing bacteria isolated from the inside of Glomus mosseae spores from Cuba. First International Meeting on Microbial Phosphate Solubilization. In E. Velazquez and C. Rodriguez-Barrueco (ed.), Developments in plant and soil sciences, vol. 102.
46. [Reprint of Plant Soil 287:1-84.]
47. Moran, N. A., C. Dale, H. Dunbar, W. A. Smith, and H. Ochman. 2003. Intracellular symbionts of sharpshooters (Insecta: Hemiptera: Cicadellinae) form a distinct clade with a small genome. Environ. Microbiol. 5:116-126.
48. Murphy, D. B. 2001. Fundamentals of light microscopy and electronic imaging. Wiley-Liss, New York, NY.
49. Nixon, K. C. 1999. The parsimony ratchet, a new method for rapid parsimony analysis. Cladistics 15:407-414. (Pubitemid 30203167)
50. O'Brien, H. E., J. Miadlikowska, and F. Lutzoni. 2005. Assessing host specialization in symbiotic cyanobacteria associated with four closely related species of the lichen fungus Peltigera. Eur. J. Phycol. 40:363-378.
51. Pan, J. J., A. M. Baumgarten, and G. May. 2008. Effects of host plant environment and Ustilago maydis infection on the fungal endophyte community of maize (Zea mays). New Phytol. 178:147-156.
52. Parrent, J. L., T. Y. James, R. Vasaitis, and A. F. S. Taylor. 2009. Friend or foe? Evolutionary history of glycoside hydrolase family 32 genes encoding for sucrolytic activity in fungi and its implications for plant-fungal symbioses. BMC Evol. Biol. 9:148.
53. Partida-Martinez, L. P., and C. Hertweck. 2005. Pathogenic fungus harbours endosymbiotic bacteria for toxin production. Nature 437:884-888.
54. Partida-Martinez, L. P., S. Monajembashi, K. O. Greulich, and C. Hertweck. 2007. Endosymbiont-dependent host reproduction maintains bacterial-fungal mutualism. Curr. Biol. 17:773-777.
55. Posada, D., and K. A. Crandall. 1998. MODELTEST: testing the model of DNA substitution. Bioinformatics 14:817-818. (Pubitemid 28552116)
56. Ruiz-Lozano, J. M., and P. Bonfante. 1999. Identification of a putative P-transporter Operon in the genome of a Burkholderia strain living inside the arbuscular mycorrhizal fungus Gigaspora margarita. J. Bacteriol. 181:4106-4109.
57. Saiki, R. K., S. Scharf, F. Faloona, K. B. Mullis, G. T. Horn, H. A. Erlich, and N. Arnheim. 1985. Enzymatic amplification of beta-globin genomic sequences and restriction site analysis for diagnosis of sickle cell anemia. Science 230:1350-1354.
58. Saunders, M., and L. M. Kohn. 2009. Evidence for alteration of fungal endophyte community assembly by host defense compounds. New Phytol. 182:229-238.
59. Schrey, S. D., M. Schellhammer, M. Ecke, R. Hampp, and M. T. Tarkka. 2005. Mycorrhiza helper bacterium Streptomyces AcH 505 induces differential gene expression in the ectomycorrhizal fungus Amanita muscaria. New Phytol. 168:205-216. (Pubitemid 43919618)
60. Sharma, M., M. Schmid, M. Rothballer, G. Hause, A. Zuccaro, J. Imani, P. Kämpfer, E. Domann, P. Schäfer, A. Hartmann, and K.-H. Kogel. 2008. Detection and identification of bacteria intimately associated with fungi of the order Sebacinales. Cell. Microbiol. 10:2235-2246.
61. Shefferson, R. P., M. Weiss, T. Kull, and D. L. Taylor. 2005. High specificity generally characterizes mycorrhizal associations in rare lady's slipper orchids, genus Cypripedium. Mol. Ecol. 14:613-626.
62. Sikes, D. S., and P. O. Lewis. 2001. Beta software, version 1. PAUPRat: PAUP* implementation of the parsimony ratchet. University of Connecticut, Storrs, CT.
63. Stackebrandt, E., and B. M. Göbel. 1994. Taxonomie note: a place for DNA-DNA reassociation and t65 rRNA sequence analysis in the present species definition in bacteriology. Int. J. Syst. Bacteriol. 44:846-849.
64. Stanosz, G. R., J. T. Blodgett, D. R. Smith, and E. L. Kruger. 2001. Water stress and Sphaeropsis sapinea as a latent pathogen of red pine seedlings. New Phytol. 149:531-538.
65. Stewart, A., and J. W. Deacon. 1995. Vital fluorochromes as tracers for fungal growth studies. Biotech. Histochem. 70:57-65.
66. Swofford, D. L. 2002. PAUP*: phylogenetic analysis using parsimony (* and other methods). Version 4b10. Sinauer Associates, Sunderland, MA.
67. U'Ren, J. M., J. W. Dalling, R. E. Gallery, D. R. Maddison, E. C. Davis, C. M. Gibson, and A. E. Arnold. 2009. Diversity and evolutionary origins of fungi associated with seeds of a neotropical pioneer tree: a case study for analysing fungal environmental samples. Mycol. Res. 113:432-449.
68. Vilgalys, R., and M. Hester. 1990. Rapid genetic identification and mapping of enzymatically amplified ribosomal DNA from several Cryptococcus species. J. Bacteriol. 172:4238-4246. (Pubitemid 20236711)
69. Waller, F., B. Achatz, H. Baltruschat, J. Fodor, K. Becker, M. Fischer, T. Heier, R. Hückelhoven, C. Neumann, D. von Wettstein, P. Franken, and K.-H. Kogel. 2005. The endophytic fungus Piriformospora indica reprograms barley to salt-stress tolerance, disease resistance, and higher yield. Proc. Natl. Acad. Sci. U. S. A. 102:13386-13391.
70. Wang, Q., G. M. Garrity, J. M. Tiedje, and J. R. Cole. 2007. Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl. Environ. Microbiol. 73:5261-5267.
71. White, T. J., T. Bruns, S. Lee, and J. Taylor. 1990. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In M. A. Innis, D. H. Gelfand, J. J. Sninsky, and T. J. White (ed.), PCR protocols: a guide to methods and applications. Academic Press, San Diego, CA.
72. Xavier, L. J. C., and J. J. She Germida. 2003. Bacteria associated with Glomus clarum spores influence mycorrhizal activity. Soil Biol. Biochem. 35:471-1178