Bacterial endophyte communities in the foliage of coast redwood and giant sequoia

Frontiers in Microbiology

Volumn 6, Issue SEP, 2015, Pages

  Carrell, Alyssa A ^a,b,c   Frank, Anna C ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b DUKE UNIVERSITY   (United States)

^c OAK RIDGE NATIONAL LABORATORY   (United States)

Author keywords

16S rRNA; Bacterial endophytes; Foliage; Giant sequoia; Microbiome; Redwood; Sequoia sempervirens; Sequoiadendron giganteum

Indexed keywords

ACETIC ACID; RNA 16S;

ARTICLE; BACTERIAL ENDOPHYTE; COMMUNITY DYNAMICS; DNA EXTRACTION; DNA SEQUENCE; GENE; GENE AMPLIFICATION; GENE EXPRESSION; METABOLIC REGULATION; MICROBIAL COMMUNITY; MICROBIOLOGY; MUTAGENESIS; NONHUMAN; ORGANISMAL INTERACTION; PHYLOGENY; QUANTITATIVE ANALYSIS; SEQUENCE ANALYSIS; SEQUOIA;

EID: 84949650982     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2015.01008     Document Type: Article

References (71)

1. Adams, A. S., Six, D. L., Adams, S. M., and Holben, W. E. (2008). In vitro interactions between yeasts and bacteria and the fungal symbionts of the mountain pine beetle (Dendroctonus ponderosae). Microb. Ecol. 56, 460-466. doi: 10.1007/s00248-008-9364-0
2. Aleklett, K., Leff, J. W., Fierer, N., and Hart, M. (2015). Wild plant species growing closely connected in a subalpine meadow host distinct root-associated bacterial communities. Peer J. 3:e804. doi: 10.7717/peerj.804
3. Anand, R., Grayston, S., and Chanway, C. (2013). N2-Fixation and seedling growth promotion of lodgepole pine by endophytic Paenibacillus polymyxa. Microb. Ecol. 66, 369-374. doi: 10.1007/s00248-013-0196-1
4. Arnold, A. E., Henk, D. A., Eells, R. L., Lutzoni, F., and Vilgalys, R. (2007). Diversity and phylogenetic affinities of foliar fungal endophytes in loblolly pine inferred by culturing and environmental PCR. Mycologia 99, 185-206. doi: 10.3852/mycologia.99.2.185
5. Axelrood, P. E., Clarke, A. M., Radley, R., and Zemcov, S. J. (1996). Douglas-fir root-associated microorganisms with inhibitory activity towards fungal plant pathogens and human bacterial pathogens. Can. J. Microbiol. 42, 690-700. doi: 10.1139/m96-094
6. Bacon, C. W., and Hinton, D. M. (2011). In planta reduction of maize seedling stalk lesions by the bacterial endophyte Bacillus mojavensis. Can. J. Microbiol. 57, 485-492. doi: 10.1139/w11-031
7. Berg, G. (2014). The plant microbiome and its importance for plant and human health. Front. Microbiol. 5:491. doi: 10.3389/fmicb.2014.00491
8. Bordiec, S., Paquis, S., Lacroix, H., Dhondt, S., Ait Barka, E., Kauffmann, S., et al. (2011). Comparative analysis of defence responses induced by the endophytic plant growth-promoting rhizobacterium Burkholderia phytofirmans strain PsJN and the non-host bacterium Pseudomonas syringae pv. pisi in grapevine cell suspensions. J. Exp. Bot. 62, 595-603. doi: 10.1093/jxb/erq291
9. Bragina, A., Cardinale, M., Berg, C., and Berg, G. (2013). Vertical transmission explains the specific Burkholderia pattern in Sphagnum mosses at multi-geographic scale. Front. Microbiol. 4:394. doi: 10.3389/fmicb.2013.00394
10. Bulgarelli, D., Rott, M., Schlaeppi, K., Ver Loren van Themaat, E., Ahmadinejad, N., Assenza, F., et al. (2012). Revealing structure and assembly cues for Arabidopsis root-inhabiting bacterial microbiota. Nature 488, 91-95. doi: 10.1038/nature11336
11. Caporaso, J. G., Bittinger, K., Bushman, F. D., DeSantis, T. Z., Andersen, G. L., and Knight, R. (2010a). PyNAST: a flexible tool for aligning sequences to a template alignment. Bioinformatics 26, 266-267. doi: 10.1093/bioinformatics/btp636
12. Caporaso, J. G., Kuczynski, J., Stombaugh, J., Bittinger, K., Bushman, F. D., Costello, E. K., et al. (2010b). QIIME allows analysis of high-throughput community sequencing data. Nat. Methods 7, 335-336. doi: 10.1038/nmeth.f.303
13. Carrell, A. A., and Frank, A. C. (2014). Pinus flexilis and Picea engelmannii share a simple and consistent needle endophyte microbiota with a potential role in nitrogen fixation. Front. Microbiol. 5:333. doi: 10.3389/fmicb.2014.00333
14. Carroll, G. (1988). Fungal endophytes in stems and leaves: from latent pathogen to mutualistic symbiont. Ecology 69, 2-9. doi: 10.2307/1943154
15. Carroll, G. C., and Carroll, F. E. (1978). Studies on the incidence of coniferous needle endophytes in the Pacific Northwest. Can. J. Bot. 56, 3034-3043. doi: 10.1139/b78-367
16. Chelius, M. K., and Triplett, E. W. (2001). The diversity of archaea and bacteria in association with the roots of Zea mays L. Microb. Ecol. 41, 252-263. doi: 10.1007/s002480000087
17. Cocking, E. C., Stone, J. T., and Davey, M. R. (2006). Intracellular colonization of roots of arabidopsis and crop plants by Gluconacetobacter diazotrophicus. In Vitro Cell. Dev. Biol. 42, 74-82. doi: 10.1079/IVP2005716
18. Davidson, J. M., Patterson, H. A., and Rizzo, D. M. (2008). Sources of inoculum for Phytophthora ramorum in a redwood forest. Phytopathology 98, 860-866. doi: 10.1094/PHYTO-98-8-0860
19. DeSantis, T. Z., Hugenholtz, P., Larsen, N., Rojas, M., Brodie, E. L., Keller, K., et al. (2006). Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl. Environ. Microbiol. 72, 5069-72. doi: 10.1128/AEM.03006-05
20. Dutta, D., and Gachhui, R. (2007). Nitrogen-fixing and cellulose-producing Gluconacetobacter kombuchae sp. nov., isolated from Kombucha tea. Int. J. Syst. Evol. Microbiol. 57, 353-7. doi: 10.1099/ijs.0.64638-0
21. Edgar, R. C., Haas, B. J., Clemente, J. C., Quince, C., and Knight, R. (2011). UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27, 2194-2200. doi: 10.1093/bioinformatics/btr381
22. Edwards, J., Johnson, C., Santos-Medellín, C., Lurie, E., Podishetty, N. K., Bhatnagar, S., et al. (2015). Structure, variation, and assembly of the root-associated microbiomes of rice. Proc. Natl. Acad. Sci. U.S.A. 112, E911-E920. doi: 10.1073/pnas.1414592112
23. Elbeltagy, A., Nishioka, K., Sato, T., Suzuki, H., Ye, B., Hamada, T., et al. (2001). Endophytic colonization and in planta nitrogen fixation by a Herbaspirillum sp. isolated from wild rice species. Appl. Environ. Microbiol. 67, 5285-5293. doi: 10.1128/AEM.67.11.5285-5293.2001
24. Espinosa-Garcia, F. J., and Langenheim, J. H. (1990). The endophytic fungal community in leaves of a coastal redwood population diversity and spatial patterns. New Phytol. 116, 89-97. doi: 10.1111/j.1469-8137.1990.tb00513.x
25. Ewing, H. A., Weathers, K. C., Templer, P. H., Dawson, T. E., Firestone, M. K., Elliott, A. M., et al. (2009). Fog water and ecosystem function: heterogeneity in a california redwood forest. Ecosystems 12, 417-433. doi: 10.1007/s10021-009-9232-x
26. Friesen, M. L., Porter, S. S., Stark, S. C., von Wettberg, E. J., Sachs, J. L., and Martinez-Romero, E. (2011). Microbially mediated plant functional traits. Annu. Rev. Ecol. Evol. Syst. 42, 23-46. doi: 10.1146/annurev-ecolsys-102710-145039
27. Fuentes-Ramirez, L. E., Bustillos-Cristales, R., Tapia-Hernandez, A., Jimenez-Salgado, T., Wang, E. T., Martinez-Romero, E., et al. (2001). Novel nitrogen-fixing acetic acid bacteria, Gluconacetobacter johannae sp. nov. and Gluconacetobacter azotocaptans sp. nov., associated with coffee plants. Int. J. Syst. Evol. Microbiol. 51, 1305-1314
28. Ganley, R. J., Brunsfeld, S. J., and Newcombe, G. (2004). A community of unknown, endophytic fungi in western white pine. Proc. Natl. Acad. Sci. U.S.A. 101, 10107-10112. doi: 10.1073/pnas.0401513101
29. Gottel, N. R., Castro, H. F., Kerley, M., Yang, Z., Pelletier, D. A., Podar, M., et al. (2011). Distinct microbial communities within the endosphere and rhizosphere of Populus deltoides roots across contrasting soil types. Appl. Environ. Microbiol. 77, 5934-44. doi: 10.1128/AEM.05255-11
30. Grube, M., Cardinale, M., de Castro, J. V., Müller, H., and Berg, G. (2009). Species-specific structural and functional diversity of bacterial communities in lichen symbioses. ISME J. 3, 1105-1115. doi: 10.1038/ismej.2009.63
31. Hardoim, P. R., van Overbeek, L. S., and Elsas, J. D. (2008). Properties of bacterial endophytes and their proposed role in plant growth. Trends Microbiol. 16, 463-471. doi: 10.1016/j.tim.2008.07.008
32. Hodkinson, B. P., Gottel, N. R., Schadt, C. W., and Lutzoni, F. (2012). Photoautotrophic symbiont and geography are major factors affecting highly structured and diverse bacterial communities in the lichen microbiome. Environ. Microbiol. 14, 147-161. doi: 10.1111/j.1462-2920.2011.02560.x
33. Hodkinson, B. P., and Lutzoni, F. (2009). A microbiotic survey of lichen-associated bacteria reveals a new lineage from the Rhizobiales. Symbiosis 49, 163-180. doi: 10.1007/s13199-009-0049-3
34. Jiao, J. Y., Wang, H. X., Zeng, Y., and Shen, Y. M. (2006). Enrichment for microbes living in association with plant tissues. J. Appl. Microbiol. 100, 830-837. doi: 10.1111/j.1365-2672.2006.02830.x
35. Kaewkla, O., and Franco, C. M. (2013). Rational approaches to improving the isolation of endophytic actinobacteria from Australian native trees. Microb. Ecol. 65, 384-393. doi: 10.1007/s00248-012-0113-z
36. Kersters, K., Lisdiyanti, P., Komagata, K., and Swings, J. (2006). "The family acetobacteraceae: the genera acetobacter, acidomonas, asaia, gluconacetobacter, gluconobacter, and kozakia," in The prokaryotes, eds M. Dworkin, S. Falkow, E. Rosenberg, K. H. Schleifer, and E. Stackebrandt (New York, NY: Springer), 163-200.
37. Knoth, J. L., Kim, S.-H., Ettl, G. J., and Doty, S. L. (2014). Biological nitrogen fixation and biomass accumulation within poplar clones as a result of inoculations with diazotrophic endophyte consortia. New Phytol. 201, 599-609. doi: 10.1111/nph.12536
38. Kwak, M. -J., Song, J. Y., Kim, S.-Y., Jeong, H., Kang, S. G., Kim, B. K., et al. (2012). Complete genome sequence of the endophytic bacterium Burkholderia sp. strain KJ006. J. Bacteriol. 194, 4432-4433. doi: 10.1128/JB.00821-12
39. Letunic, I., and Bork, P. (2011). Interactive Tree Of Life v2: online annotation and display of phylogenetic trees made easy. Nucleic Acids Res. 39, W475-W478. doi: 10.1093/nar/gkr201
40. Lozupone, C., and Knight, R. (2005). UniFrac: a new phylogenetic method for comparing microbial communities. Appl. Environ. Microbiol. 71, 8228-8235. doi: 10.1128/AEM.71.12.8228-8235.2005
41. Lundberg, D. S., Lebeis, S. L., Paredes, S. H., Yourstone, S., Gehring, J., Malfatti, S., et al. (2012). Defining the core Arabidopsis thaliana root microbiome. Nature 488, 86-90. doi: 10.1038/nature11237
42. Mendes, R., Kruijt, M., de Bruijn, I., Dekkers, E., van der Voort, M., Schneider, J. H., et al. (2011). Deciphering the rhizosphere microbiome for disease-suppressive bacteria. Science 332, 1097-1100. doi: 10.1126/science.1203980
43. Müller, H., Berg, C., Landa, B. B., Auerbach, A., Moissl-Eichinger, C., and Berg, G. (2015). Plant genotype-specific archaeal and bacterial endophytes but similar Bacillus antagonists colonize Mediterranean olive trees. Front. Microbiol. 6:138. doi: 10.3389/fmicb.2015.00138
44. Nawrocki, E. P., Kolbe, D. L., and Eddy, S. R. (2009). Infernal 1.0: inference of RNA alignments. Bioinformatics 25, 1335-1337. doi: 10.1093/bioinformatics/btp157
45. Nissinen, R. M., Männistö, M. K., and van Elsas, J. D. (2012). Endophytic bacterial communities in three arctic plants from low arctic fell tundra are cold-adapted and host-plant specific. FEMS Microbiol. Ecol. 82, 510-522. doi: 10.1111/j.1574-6941.2012.01464.x
46. Ongena, M., and Jacques, P. (2008). Bacillus lipopeptides: versatile weapons for plant disease biocontrol. Trends Microbiol. 16, 115-125. doi: 10.1016/j.tim.2007.12.009
47. Oono, R., Lutzoni, F., Arnold, A. E., Kaye, L., U'Ren, J. M., May, G., et al. (2014). Genetic variation in horizontally transmitted fungal endophytes of pine needles reveals population structure in cryptic species. Am. J. Bot. 101, 1362-1374. doi: 10.3732/ajb.1400141
48. Peñuelas, J., and Terradas, J. (2014). The foliar microbiome. Trends Plant Sci. 19, 278-280. doi: 10.1016/j.tplants.2013.12.007
49. Porras-Alfaro, A., and Bayman, P. (2011). Hidden fungi, emergent properties: endophytes and microbiomes. Annu. Rev. Phytopathol. 49, 291-315. doi: 10.1146/annurev-phyto-080508-081831
50. Postma, J., Scheper, R. W. A., and Schilder, M. T. (2010). Effect of successive cauliflower plantings and Rhizoctonia solani AG 2-1 inoculations on disease suppressiveness of a suppressive and a conducive soil. Soil Biol. Biochem. 42, 804-812. doi: 10.1016/j.soilbio.2010.01.017
51. Price, M. N., Dehal, P. S., and Arkin, A. P. (2009). FastTree: computing large minimum evolution trees with profiles instead of a distance matrix. Mol. Biol. Evol. 26, 1641-1650. doi: 10.1093/molbev/msp077
52. Qadri, M., Rajput, R., Abdin, M. Z., Vishwakarma, R. A., and Riyaz-Ul-Hassan, S. (2014). Diversity, molecular phylogeny, and bioactive potential of fungal endophytes associated with the himalayan blue pine (Pinus wallichiana). Microb. Ecol. 67, 877-887. doi: 10.1007/s00248-014-0379-4
53. Qin, S., Xing, K., Jiang, J.-H., Xu, L.-H., and Li, W.-J. (2011). Biodiversity, bioactive natural products and biotechnological potential of plant-associated endophytic actinobacteria. Appl. Microbiol. Biotechnol. 89, 457-473. doi: 10.1007/s00253-010-2923-6
54. Raaijmakers, J. M., and Mazzola, M. (2012). Diversity and natural functions of antibiotics produced by beneficial and plant pathogenic bacteria. Annu. Rev. Phytopathol. 50, 403-424. doi: 10.1146/annurev-phyto-081211-172908
55. Redford, A. J., Bowers, R. M., Knight, R., Linhart, Y., and Fierer, N. (2010). The ecology of the phyllosphere: geographic and phylogenetic variability in the distribution of bacteria on tree leaves. Environ. Microbiol. 12, 2885-2893. doi: 10.1111/j.1462-2920.2010.02258.x
56. Reinhold-Hurek, B., and Hurek, T. (2011). Living inside plants: bacterial endophytes. Curr. Opin. Plant Biol. 14, 435-443. doi: 10.1016/j.pbi.2011.04.004
57. Rodriguez, R. J., Redman, R. S., and Henson, J. M. (2004). the role of fungal symbioses in the adaptation of plants to high stress environments. Mitig. Adapt. Strateg. Glob. Change 9, 1573-1596. doi: 10.1023/B:MITI.0000029922.31110.97
58. Rollinger, J. L., and Langenheim, J. H. (1993). Geographic survey of fungal endophyte community composition in leaves of coastal redwood. Mycologia 85, 149. doi: 10.2307/3760450
59. Rosenblueth, M., and Martinez-Romero, E. (2006). Bacterial endophytes and their interactions with hosts. Mol. Plant Microbe Interact. 19, 827-837. doi: 10.1094/MPMI-19-0827
60. Rout, M. E., Chrzanowski, T. H., Westlie, T. K., Deluca, T. H., Callaway, R. M., and Holben, W. E. (2013). Bacterial endophytes enhance competition by invasive plants. Am. J. Bot. 100, 1726-1737. doi: 10.3732/ajb.1200577
61. Schlaeppi, K., Dombrowski, N., Oter, R. G., Ver Loren van Themaat, E., and Schulze-Lefert, P. (2014). Quantitative divergence of the bacterial root microbiota in Arabidopsis thaliana relatives. Proc. Natl. Acad. Sci. U.S.A. 111, 585-592. doi: 10.1073/pnas.1321597111
62. Shakya, M., Gottel, N., Castro, H., Yang, Z. K., Gunter, L., Labbã, J., et al. (2013). A multifactor analysis of fungal and bacterial community structure in the root microbiome of mature populus deltoides trees. PLoS ONE 8:e76382 doi: 10.1371/journal.pone.0076382
63. Shen, S. Y., and Fulthorpe, R. (2015). Seasonal variation of bacterial endophytes in urban trees. Front. Microbiol. 6:427. doi: 10.3389/fmicb.2015.00427
64. Sillett, S. C., and Pelt, R. V. (2007). Trunk reiteration promotes epiphytes and water storage in an old-growth redwood forest canopy. Ecol. Monogr. 77, 335-359. doi: 10.1890/06-0994.1
65. Stamatakis, A., Ludwig, T., and Meier, H. (2005). RAxML-III: a fast program for maximum likelihood-based inference of large phylogenetic trees. Bioinformatics 21, 456-463. doi: 10.1093/bioinformatics/bti191
66. Suárez-Moreno, Z. R., Caballero-Mellado, J., Coutinho, B. G., Mendonça-Previato, L., James, E. K., and Venturi, V. (2012). Common features of environmental and potentially beneficial plant-associated burkholderia. Microb. Ecol. 63, 249-266. doi: 10.1007/s00248-011-9929-1
67. Theocharis, A., Bordiec, S., Fernandez, O., Paquis, S., Dhondt-Cordelier, S., Baillieul, F., et al. (2012). Burkholderia phytofirmans PsJN primes Vitis vinifera L. and confers a better tolerance to low nonfreezing temperatures. Mol. Plant Microbe Interact. 25, 241-249. doi: 10.1094/MPMI-05-11-0124
68. Tiwari, K., and Gupta, R. K. (2012). Rare actinomycetes: a potential storehouse for novel antibiotics. Crit. Rev. Biotechnol. 32, 108-132. doi: 10.3109/07388551.2011.562482
69. Turner, T. R., James, E. K., and Poole, P. S. (2013). The plant microbiome. Genome Biol. 14, 209. doi: 10.1186/gb-2013-14-6-209
70. Wang, Q., Garrity, G. M., Tiedje, J. M., and Cole, J. R. (2007). Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl. Environ. Microbiol. 73, 5261-5267. doi: 10.1128/AEM.00062-07
71. Williams, C. B., and Sillett, S. C. (2007). Epiphyte communities on redwood (Sequoia sempervirens) in northwestern California. Bryologist 110, 420-452. doi: 10.1639/0007-2745(2007)11