Pinus flexilis and Picea engelmannii share a simple and consistent needle endophyte microbiota with a potential role in nitrogen fixation

Frontiers in Microbiology

Volumn 5, Issue JULY, 2014, Pages

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

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

16S rRNA; Acetobacteraceae; Bacterial endophytes; Conifers; Nitrogen; Picea; Pinus; Subalpine

Indexed keywords

ABIOTIC STRESS; ACETOBACTERACEAE; ARTICLE; CONTROLLED STUDY; DNA EXTRACTION; ENDOPHYTE; MICROFLORA; NITROGEN FIXATION; NONHUMAN; PHYLOGENY; PICEA ENGELMANNII; PINE; PINUS FLEXILIS; PLANT GROWTH; PLANT TAXONOMY; POLYMERASE CHAIN REACTION; PYROSEQUENCING; QUALITY CONTROL; SEQUENCE ANALYSIS; SIGNAL TRANSDUCTION;

EID: 84905394606     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2014.00333     Document Type: Article

References (98)

1. 2-fixation and growth promotion in cedar colonized by an endophytic strain of Paenibacillus polymyxa. Biol. Fertil. Soils 49, 235-239. doi: 10.1007/s00374-012-0735-9
2. 2-fixation and seedling growth promotion of lodgepole pine by endophytic Paenibacillus polymyxa. Microb. Ecol. 66, 369-374. doi: 10.1007/s00248-013-0196-1
3. Ando, S., Goto, M., Meunchang, S., Thongra-ar, P., Fujiwara, T., Hayashi, H.,et al. (2005). Detection of nifH squences in sugarcane (Saccharurnomcinarurn L.) and Pineapple (Ananas cornosus [L.] Merr.). Soil Sci. Plant Nutr. 51, 303-308. doi: 10.1111/j.1747-0765.2005.tb00034.x
4. Arnold, A. E., Mejia, L. C., Kyllo, D., Rojas, E. I., Maynard, Z., Robbins, N.,et al. (2003). Fungal endophytes limit pathogen damage in a tropical tree. Proc. Natl. Acad. Sci. U.S.A. 100, 15649-15654. doi: 10.1073/pnas.2533483100
5. Arshad, M., and Frankenberger, W. T. (1991). Microbial production of plant hormones. Plant Soil 133, 1-8. doi: 10.1007/BF00011893
6. Bal, A., Anand, R., Berge, O., and Chanway, C. P. (2012). Isolation and identification of diazotrophic bacteria from internal tissues of Pinus contorta and Thuja plicata. Can. J. For. Res. 42, 807-813. doi: 10.1139/x2012-023
7. Bal, A., and Chanway, C. P. (2012). Evidence of nitrogen fixation in lodgepole pine inoculated with diazotrophic Paenibacillus polymyxa. Botany 90, 891-896. doi: 10.1139/b2012-044
8. Berry, D., Ben Mahfoudh, K., Wagner, M., and Loy, A. (2011). Barcoded primers used in multiplex amplicon pyrosequencing bias amplification. Appl. Environ. Microbiol. 77, 7846-7849. doi: 10.1128/AEM.05220-11
9. Binkley, D., Yowhan, S., and Valentine, D. W. (2000). Do forests receive occult inputs of nitrogen? Ecosystems 3, 321-331. doi: 10.1007/s100210000029
10. Blanco, Y., Blanch, M., Pinon, D., Legaz, M. E., and Vicente, C. (2005). Antagonism of Gluconacetobacter diazotrophicus (a sugarcane endosymbiont) against Xanthomonas albilineans (pathogen) studied in alginate-immobilized sugarcane stalk tissues. J. Biosci. Bioeng. 99, 366-371. doi: 10.1263/jbb.99.366
11. Boddey, R. M. (1995). Biological nitrogen fixation in sugar cane: a key to energetically viable biofuel production. Crit. Rev. Plant Sci. 14, 263-279. doi: 10.1080/07352689509701929
12. Boddey, R. M., Urquiaga, S., and Reis, V. M. (2003). Endophytic nitrogen fixation in sugarcane: present knowledge and future applications. Plant Soil 252, 139-149. doi: 10.1023/A:1024152126541
13. Bodenhausen, N., Horton, M. W., and Bergelson, J. (2013). Bacterial communities associated with the leaves and the roots of Arabidopsis thaliana. PLoS ONE 8:e56329. doi: 10.1371/journal.pone.0056329
14. 2 fixation in pines, alder, and locust: evidence from the Sandbox Ecosystems study. Ecosystems 74, 583-598.
15. Bormann, B. T., Keller, C. K., Wang, D., and Bormann, H. (2002). Lessons from the Sandbox: is unexplained nitrogen real? Ecosystems 5, 727-733. doi: 10.1007/s10021-002-0189-2
16. 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
17. Cankar, K., Kraigher, H., Ravnikar, M., and Rupnik, M. (2005). Bacterial endophytes from seeds of Norway spruce (Picea abies L. Karst). FEMS Microbiol. Lett. 244, 341-345. doi: 10.1016/j.femsle.2005.02.008
18. 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
19. 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
20. Carroll, G. (1988). Fungal endophytes in stems and leaves: from latent pathogen to mutualistic symbiont. Ecology 69, 2-9. doi: 10.2307/1943154
21. Chanway, C., and Holl, F. B. (1991). Biomass increase and associative nitrogen fixation of mycorrhizal Pinus contorta seedlings inoculated with a plant growth promoting Bacillus strain. Can. J. Bot. 69, 507-511. doi: 10.1139/b91-069
22. Chapman, W. K., and Paul, L. (2012). Evidence that northern pioneering pines with tuberculate mycorrhizae are unaffected by varying soil nitrogen levels. Microb. Ecol. 64, 964-972. doi: 10.1007/s00248-012-0076-0
23. 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.
24. 2-fixing communities in agricultural soils. Environ. Microbiol. doi: 10.1111/1462-2920.12423 [Epub ahead of print].
25. Conn, V. M., Walker, A. R., and Franco, C. M. (2008). Endophytic actinobacteria induce defense pathways in Arabidopsis thaliana. Mol. Plant Microbe Interact. 21, 208-218. doi: 10.1094/MPMI-21-2-0208
26. Crotti, E., Rizzi, A., Chouaia, B., Ricci, I., Favia, G., Alma, A.,et al. (2010). Acetic acid bacteria, newly emerging symbionts of insects. Appl. Environ. Microbiol. 76, 6963-6970. doi: 10.1128/AEM.01336-10
27. DeLuca, T. H., Zackrisson, O., Nilsson, M. C., and Sellstedt, A. (2002). Quantifying nitrogen-fixation in feather moss carpets of boreal forests. Nature 419, 917-920. doi: 10.1038/nature01051
28. Delwiche, C., Zinke, P. J., Johnson, C. M., and Virginia, R. A. (1979). Nitrogen isotope distribution as a presumptive indicator of nitrogen fixation. Bot. Gaz. 140, 65-69. doi: 10.1086/337037
29. 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, 5069-5072. doi: 10.1128/AEM.03006-05
30. Dong, Z., Canny, M. J., McCully, M. E., Roboredo, M. R., Cabadilla, C. F., Ortega, E.,et al. (1994). A nitrogen-fixing endophyte of sugarcane stems (a new role for the apoplast). Plant Physiol. 105, 1139-1147.
31. Dutta, D., and Gachhui, R. (2006). Novel nitrogen-fixing Acetobacter nitrogenifigens sp. nov., isolated from Kombucha tea. Int. J. Syst. Evol. Microbiol. 56, 1899-1903. doi: 10.1099/ijs.0.64101-64100
32. 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, 353-357. doi: 10.1099/ijs.0.64638-0
33. Edgar, R. C. (2010). Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26, 2460-2461. doi: 10.1093/bioinformatics/btq461
34. 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
35. Engel, P., and Moran, N. A. (2013). The gut microbiota of insects-diversity in structure and function. FEMS Microbiol. Rev. 37, 699-735. doi: 10.1111/1574-6976.12025
36. Farnelid, H., Bentzon-Tilia, M., Andersson, A. F., Bertilsson, S., Jost, G., Labrenz, M.,et al. (2013). Active nitrogen-fixing heterotrophic bacteria at and below the chemocline of the central Baltic Sea. ISME J. 7, 1413-1423. doi: 10.1038/ismej.2013.26
37. Favilli, F., and Messini, A. (1990). Nitrogen fixation at phyllospheric level in coniferous plants in Italy. Plant Soil 128, 91-95. doi: 10.1007/BF00009400
38. 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.
39. Gillis, M., Kersters, K., Hoste, B., Janssens, D., Kroppenstedt, R. M., Stephan, M. P.,et al. (1989). Acetobacter diazotrophicus sp. nov., a nitrogen-fixing acetic acid bacterium associated with sugarcane. Int. J. Syst. Bacteriol. 39, 361-364. doi: 10.1099/00207713-39-3-361
40. Glick, B. R. (2004). Bacterial ACC deaminase and the alleviation of plant stress. Adv. Appl. Microbiol. 56, 291-312. doi: 10.1016/S0065-2164(04)56009-4
41. 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, 5934-5944. doi: 10.1128/AEM.05255-11
42. Greenberg, D. E., Ding, L., Zelazny, A. M., Stock, F., Wong, A., Anderson, V. L.,et al. (2006). A novel bacterium associated with lymphadenitis in a patient with chronic granulomatous disease. PLoS Pathog. 2:e28. doi: 10.1371/journal.ppat.0020028
43. Hallman, J., Quadt-Hallmann, A., Mahaffee, W. F., and Kloepper, J. W. (1997). Bacterial endophytes in agricultural crops. Can. J. Microbiol. 43, 895-914. doi: 10.1139/m97-131
44. Hanshew, A. S., Mason, C. J., Raffa, K. F., and Currie, C. R. (2013). Minimization of chloroplast contamination in 16S rRNA gene pyrosequencing of insect herbivore bacterial communities. J. Microbiol. Methods 95, 149-155. doi: 10.1016/j.mimet.2013.08.007
45. 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
46. Higgins, K. L., Coley, P. D., Kursar, T. A., and Arnold, A. E. (2011). Culturing and direct PCR suggest prevalent host generalism among diverse fungal endophytes of tropical forest grasses. Mycologia 103, 247-260. doi: 10.3852/09-158
47. Hobbie, E. A., Macko, S. A., and Williams, M. (2000). Correlations between foliar d15N and nitrogen concentrations may indicate plant-mycorrhizal interactions. Oecologia 273-283. doi: 10.1007/PL00008856
48. Hurek, T., Handley, L. L., Reinhold-Hurek, B., and Piche, Y. (2002). Azoarcus grass endophytes contribute fixed nitrogen to the plant in an unculturable state. Mol. Plant Microbe Interact. 15, 233-242. doi: 10.1094/MPMI.2002.15.3.233
49. Idris, R., Trifonova, R., Puschenreiter, M., Wenzel, W. W., and Sessitsch, A. (2004). Bacterial communities associated with flowering plants of the Ni hyperaccumulator Thlaspi goes ingense. Appl. Environ. Microbiol. 70, 2667-2677. doi: 10.1128/AEM.70.5.2667-2677.2004
50. Izumi, H., Anderson, I. C., Killham, K., and Moore, E. R. (2008). Diversity of predominant endophytic bacteria in European deciduous and coniferous trees. Can. J. Microbiol. 54, 173-179. doi: 10.1139/W07-134
51. 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
52. Jojima, Y., Mihara, Y., Suzuki, S., Yokozeki, K., Yamanaka, S., and Fudou, R. (2004). Saccharibacter floricola gen. nov., sp. nov., a novel osmophilic acetic acid bacterium isolated from pollen. Int. J. Syst. Evol. Microbiol. 54, 2263-2267. doi: 10.1099/ijs.0.02911-0
53. Jones, K., King, E., and Eastlick, M. (1974). Nitrogen fixation by free-living bacteria in the soil and in the canopy of Douglas fir. Ann. Bot. Lond. 38, 765-762.
54. 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.
55. Knoth, J. L., Kim, S. H., Ettl, G. J., and Doty, S. L. (2013). Biological nitrogen fixation and biomass accumulation within poplar clones as a result of inoculations with diazotrophic endophyte consortia. New Phytol. doi: 10.1111/nph.12536 [Epub ahead of print].
56. Lee, S., Flores-Encarnación, M., Contreras-Zentella, M., Garcia-Flores, L., Escamilla, J. E., and Kennedy, C. (2004). Indole-3-acetic acid biosynthesis is deficient in Gluconacetobacter diazotrophicus strains with mutations in cytochrome c biogenesis genes. J. Bacteriol. 186, 5384-5391. doi: 10.1128/JB.186.16.5384-5391.2004
57. Lin, C.-P., Huang, J.-P., Wu, C.-S., Hsu, C.-Y., and Chaw, S.-M. (2010). Comparative chloroplast genomics reveals the evolution of Pinaceae genera and subfamilies. Genome Biol. Evol. 2, 504-517. doi: 10.1093/gbe/evq036
58. Lipson, D. A., and Schmidt, S. K. (2004). Seasonal changes in an alpine soil bacterial community in the colorado rocky mountains. Appl. Environ. Microbiol. 70, 2867-2879. doi: 10.1128/AEM.70.5.2867-2879.2004
59. Loganathan, P., and Nair, S. (2004). Swaminathania salitolerans gen. nov., sp. nov., a salt-tolerant, nitrogen-fixing and phosphate-solubilizing bacterium from wild rice (Porteresia coarctata Tateoka). Int. J. Syst. Evol. Microbiol. 54, 1185-1190. doi: 10.1099/ijs.0.028170
60. 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
61. Martinson, V. G., Danforth, B. N., Minckley, R. L., Rueppell, O., Tingek, S., and Moran, N. A. (2011). A simple and distinctive microbiota associated with honey bees and bumble bees. Mol. Ecol. 20, 619-628. doi: 10.1111/j.1365-294X.2010.04959.x
62. Mayak, S., Tirosh, T., and Glick, B. R. (2004). Plant growth-promoting bacteria confer resistance in tomato plants to salt stress. Plant Physiol. Biochem. 42, 565-572. doi: 10.1016/j.plaphy.2004.05.009
63. Morford, S. L., Houlton, B. Z., and Dahlgren, R. A. (2011). Increased forest ecosystem carbon and nitrogen storage from nitrogen rich bedrock. Nature 477, 78-81. doi: 10.1038/nature10415
64. Muthukumarasamy, R., Cleenwerck, I., Revathi, G., Vadivelu, M., Janssens, D., Hoste, B.,et al. (2005). Natural association of Gluconacetobacter diazotrophicus and diazotrophic Acetobacter peroxydans with wetland rice. Syst. Appl. Microbiol. 28, 277-286. doi: 10.1016/j.syapm.2005.01.006
65. Näsholm, T., Kielland, K., and Ganeteg, U. (2009). Uptake of organic nitrogen by plants. New Phytol. 182, 31-48. doi: 10.1111/j.1469-8137.2008.02751.x
66. Oksanen, J., Kindt, P., Legendre, B., O'Hara, B., Simpson, G. L., and Stevenson, M. H. H. (2008). vegan: Community Ecology Package, R Package Version 1.11-4. Available at: http://cran.r-project.org/
67. Ping, L., and Boland, W. (2004). Signals from the underground: bacterial volatiles promote growth in Arabidopsis. Trends Plant Sci. 9, 263-266. doi: 10.1016/j.tplants.2004.04.008
68. Pirttilä, A., and Frank, A. C. (2011). Endophytes of Forest Trees: Biology and Application. Dordrecht: Springer. doi: 10.1007/978-94-007-1599-8
69. Pirttilä, A. M., Joensuu, P., Pospiech, H., Jalonen, J., and Hohtola, A. (2004). Bud endophytes of Scots pine produce adenine derivatives and other compounds that affect morphology and mitigate browning of callus cultures. Physiol. Plant. 121, 305-312. doi: 10.1111/j.0031-9317.2004.00330.x
70. Pirttilä, A. M., Laukkanen, H., Pospiech, H., Myllyla, R., and Hohtola, A. (2000). Detection of intracellular bacteria in the buds of Scotch pine (Pinus sylvestris L.) by in situ hybridization. Appl. Environ. Microbiol. 66, 3073-3077. doi: 10.1128/AEM.66.7.3073-3077.2000
71. Pirttilä, A. M., Pospiech, H., Laukkanen, H., Myllyla, R., and Hohtola, A. (2005). Seasonal variations in location and population structure of endophytes in buds of Scots pine. Tree Physiol. 25, 289-297. doi: 10.1093/treephys/25.3.289
72. Poole, A. M., Stouffer, D. B., and Tylianakis, J. M. (2012). "Ecosystomics": ecology by sequencer. Trends Ecol. Evol. 27, 309-310. doi: 10.1016/j.tree.2012.03.008
73. 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
74. Qin, J., Li, R., Raes, J., Arumugam, M., Burgdorf, K. S., Manichanh, C.,et al. (2010). A human gut microbial gene catalogue established by metagenomic sequencing. Nature 464, 59-65. doi: 10.1038/nature08821
75. Rastogi, G., Sbodio, A., Tech, J. J., Suslow, T. V., Coaker, G. L., and Leveau, J. H. (2012). Leaf microbiota in an agroecosystem: spatiotemporal variation in bacterial community composition on field-grown lettuce. ISME J. 6, 1812-1822. doi: 10.1038/ismej.2012.32
76. 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
77. Reed, S. C., Townsend, A. R., Cleveland, C. C., and Nemergut, D. (2010). Microbial community shifts influence patterns in tropical forest nitrogen fixation. Oecologia 264, 521-531. doi: 10.1007/s00442-010-1649-6
78. Reiter, B., Bürgmann, H., Burg, K., and Sessitsch, A. (2003). Endophytic nifH gene diversity in African sweet potato. Can. J. Microbiol. 49, 549-555. doi: 10.1139/w03-070
79. Richards, B. N. (1964). Fixation of atmospheric nitrogen in coniferous forests. Aust. For. 28, 68-74. doi: 10.1080/00049158.1964.10675356
80. Roh, S. W., Nam, Y. D., Chang, H. W., Kim, K. H., Kim, M. S., Ryu, J. H.,et al. (2008). Phylogenetic characterization of two novel commensal bacteria involved with innate immune homeostasis in Drosophila melanogaster. Appl. Environ. Microbiol. 74, 6171-6177. doi: 10.1128/AEM.00301-08
81. 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
82. Rueth, H. M., and Baron, J. S. (2002). Differences in Englemann Spruce forest biogeochemistry East and West of the continental divide in Colorado, USA. Ecosystems 5, 45-57. doi: 10.1007/s10021-001-0054-8
83. 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
84. Schoettle, A. W., and Rochelle, S. G. (2000). Morphological variation of Pinus flexilis (Pinaceae), a bird-dispersed pine, across a range of elevations. Am. J. Bot. 87, 1797-1806. doi: 10.2307/2656832
85. Shade, A., and Handelsman, J. (2012). Beyond the Venn diagram: the hunt for a core microbiome. Environ. Microbiol. 14, 4-12. doi: 10.1111/j.1462-2920.2011.02585.x
86. Sharp, K. H., Distel, D., and Paul, V. J. (2012). Diversity and dynamics of bacterial communities in early life stages of the Caribbean coral Porites astreoides. ISME J. 6, 790-801. doi: 10.1038/ismej.2011.144
87. Smith, S., and Read, D. (2008). Mycorrhizal Symbiosis. London: Academic Press.
88. 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
89. 2-fixing bacterial diversity detected in rice roots by molecular evolutionary analysis of nifH gene sequences. J. Bacteriol. 177, 1414-1417.
90. Verma, S. C., Ladha, J. K., and Tripathi, A. K. (2001). Evaluation of plant growth promoting and colonization ability of endophytic diazotrophs from deep water rice. J. Biotechnol. 91, 127-141. doi: 10.1016/S0168-1656(01)00333-9
91. 2-fixing plants from selected ecosystems. Oecologia 54, 317-325. doi: 10.1007/BF00380000
92. Vitousek, P. M., Menge, D. N., Reed, S. C., and Cleveland, C. C. (2013). Biological nitrogen fixation: rates, patterns and ecological controls in terrestrial ecosystems. Philos. Trans. R. Soc. Lond. B Biol. Sci. 368, 20130119. doi: 10.1098/rstb.2013.0119
93. Wakelin, S. A., Warren, R. A., Harvey, P. R., and Ryder, M. H. (2004). Phosphate solubilization by Penicillium spp. closely associated with wheat roots. Biol. Fertil. Soils 40, 36-43. doi: 10.1007/s00374-004-0750-6
94. 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
95. Woebken, D., Prufert-Bebout, L., Burow, L., Bebout, B., Hoehler, T., Pett-Ridge, J.,et al. (2012). Identification of a previously unknown cyanobacterial group as active diazotrophs in coastal microbial mats using NanoSIMS. ISME J. 6, 1427-1439. doi: 10.1038/ismej.2011.200
96. Yukphan, P., Malimas, T., Muramatsu, Y., Takahashi, M., Kaneyasu, M., Potacharoen, W.,et al. (2009). Ameyamaea chiangmaiensis gen. nov., sp. nov., an acetic acid bacterium in the alpha-Proteobacteria. Biosci. Biotechnol. Biochem. 73, 2156-2162. doi: 10.1271/bbb.90070
97. Yukphan, P., Malimas, T., Muramatsu, Y., Takahashi, M., Kaneyasu, M., Tanasupawat, S.,et al. (2008). Tanticharoenia sakaeratensis gen. nov., sp. nov., a new osmotolerant acetic acid bacterium in the alpha-Proteobacteria. Biosci. Biotechnol. Biochem. 72, 672-676. doi: 10.1271/bbb.70319
98. Yukphan, P., Malimas, T., Potacharoen, W., Tanasupawat, S., Tanticharoen, M., and Yamada, Y. (2005). Neoasaia chiangmaiensis gen. nov., sp. nov., a novel osmotolerant acetic acid bacterium in the alpha-Proteobacteria. J. Gen. Appl. Microbiol. 51, 301-311. doi: 10.2323/jgam.51.301