BMC Microbiology | |
The new species Enterobacter oryziphilus sp. nov. and Enterobacter oryzendophyticus sp. nov. are key inhabitants of the endosphere of rice | |
Jan Dirk van Elsas3  Leonard Simon van Overbeek5  Elisa Korenblum3  Dana Elhottová1  Angela Sessitsch4  Rashid Nazir3  Pablo Rodrigo Hardoim2  | |
[1] Institute of Soil Biology, Biology Centre, ASCR, v.v.i., Na Sádkách 7, České Budějovice CZ 370 05, Czech Republic;Current address: Centre of Marine Science, University of Algarve, Faro 8005-139, Portugal;Department of Microbial Ecology, University of Groningen, Centre for Ecological and Evolutionary Studies, Nijenborgh 7, Groningen 9747AG, The Netherlands;AIT Austrian Institute of Technology GmbH, Bioresources Unit, Tulln, Austria;Plant Research International, Droevendaalsesteeg 1, Wageningen 6708PB, The Netherlands | |
关键词: International Rice Research Institute; Production of indole-3-acetic acid; Phosphate-solubilizing bacteria; Methanotrophic bacteria; Diazotrophic bacteria; Endophytes; Plant growth-promoting bacteria; | |
Others : 1143420 DOI : 10.1186/1471-2180-13-164 |
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received in 2013-02-05, accepted in 2013-07-08, 发布年份 2013 | |
【 摘 要 】
Background
Six independent Gram-negative, facultatively anaerobic, non-spore-forming, nitrogen-fixing rod-shaped isolates were obtained from the root endosphere of rice grown at the International Rice Research Institute (IRRI) and investigated in a polyphasic taxonomic study.
Results
The strains produced fatty acid patterns typical for members of the family Enterobacteriaceae. Comparative sequence analyses of the 16S rRNA as well as rpoB genes allocated the strains to two well-defined groups within the genus Enterobacter, family Enterobacteriaceae. The analyses indicated Enterobacter radicincitans, Enterobacter arachidis and Enterobacter oryzae to be the closest related species. An RpoB (translated) protein comparison supported the placement in the genus Enterobacter and the relatedness of our isolates to the aforementioned species. Genomic DNA:DNA hybridization analyses and biochemical analyses provided further evidence that the novel strains belong to two new species within the genus Enterobacter. The two species can be differentiated from each other and from existing enteric species by acid production from L-rhamnose and D-melibiose, decarboxylation of ornithine and utilization of D-alanine, D-raffinose L-proline and L-aspartic acid, among other characteristics. Members of both species revealed capacities to colonise rice roots, including plant-growth-promoting capabilities such as an active supply of fixed nitrogen to the plant and solubilisation of inorganic phosphorus, next to traits allowing adaptation to the plant.
Conclusions
Two novel proposed enterobacterial species, denominated Enterobacter oryziphilus sp. nov. (type strain REICA_142T=LMG 26429T=NCCB 100393T) and Enterobacter oryzendophyticus sp. nov. (type strain REICA_082T=LMG 26432T =NCCB 100390T) were isolated from rice roots. Both species are capable of promoting rice growth by supplying nitrogen and phosphorus.
【 授权许可】
2013 Hardoim et al.; licensee BioMed Central Ltd.
【 预 览 】
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Figure 2. | 111KB | Image | download |
Figure 1. | 101KB | Image | download |
【 图 表 】
Figure 1.
Figure 2.
【 参考文献 】
- [1]Hayat R, Ali S, Amara U, Khalid R, Ahmed I: Soil beneficial bacteria and their role in plant growth promotion: a review. Ann Microbiol 2010, 60:579-598.
- [2]Dimkpa C, Weinand T, Asch F: Plant-rhizobacteria interactions alleviate abiotic stress conditions. Plant Cell Environ 2009, 32:1682-94.
- [3]Peng G, Zhang W, Luo H, Xie H, Lai W, Tan Z: Enterobacter oryzae sp. nov., a nitrogen-fixing bacterium isolated from the wild rice species Oryza latifolia. Int J Syst Evol Microbiol 2009, 59:1650-5.
- [4]Hardoim PR, Hardoim CCP, Van Overbeek LS, Van Elsas JD: Dynamics of seed-borne rice endophytes on early plant growth stages. PLoS One 2012, 7:e30438.
- [5]Kaga H, Mano H, Tanaka F, Watanabe A, Kaneko S, Morisaki H: Rice seeds as sources of endophytic bacteria. Microbes Environ 2009, 24:154-162.
- [6]Pedrosa FO, Monteiro RA, Wassem R, Cruz LM, Ayub RA, Colauto NB, Fernandez MA, Fungaro MHP, Grisard EC, Hungria M, Madeira HMF, Nodari RO, Osaku CA, Petzl-Erler ML, Terenzi H, Vieira LGE, Steffens MBR, Weiss VA, Pereira LFP, Almeida MIM, Alves LR, Marin A, Araujo LM, Balsanelli E, Baura VA, Chubatsu LS, Faoro H, Favetti A, Friedermann G, Glienke C, et al.: Genome of Herbaspirillum seropedicae strain SmR1, a specialized diazotrophic endophyte of tropical grasses. PLoS Genet 2011, 7:e1002064.
- [7]Elbeltagy A, Nishioka K, Sato T, Suzuki H, Ye B, Hamada T, Isawa T, Mitsui H, Minamisawa K: Endophytic colonization and in planta nitrogen fixation by a Herbaspirillum sp. isolated from wild rice species. App Environ microbiol 2001, 67:5285-93.
- [8]Brenner DJ, McWhorter AC, Kai A, Steigerwalt AG, Farmer JJ: Enterobacter asburiae sp. nov., a new species found in clinical specimens, and reassignment of Erwinia dissolvens and Erwinia nimipressuralis to the genus Enterobacter as Enterobacter dissolvens comb. nov. and Enterobacter nimipressuralis comb. nov. J Clin Microbiol 1986, 23:1114-20.
- [9]Prakamhang J, Minamisawa K, Teamtaisong K, Boonkerd N, Teaumroong N: The communities of endophytic diazotrophic bacteria in cultivated rice (Oryza sativa L.). Appl Soil Ecol 2009, 42:141-149.
- [10]Chung YR, Brenner DJ, Steigerwalt AG, Kim BS, Kim HT, Cho KY: Enterobacter pyrinus sp. nov., an organism associated with brown leaf spot disease of pear trees. Int J Syst Bacteriol 1993, 43:157-161.
- [11]Dickey RS, Zumoff CH: Emended description of Enterobacter cancerogenus comb. nov. (Formerly Erwinia cancerogena). Int J Syst Bacteriol 1988, 38:371-374.
- [12]Kämpfer P, Ruppel S, Remus R: Enterobacter radicincitans sp. nov., a plant growth promoting species of the family Enterobacteriaceae. Syst Appl Microbiol 2005, 28:213-21.
- [13]Madhaiyan M, Poonguzhali S, Lee JS, Saravanan VS, Lee KC, Santhanakrishnan P: Enterobacter arachidissp. nov., a plant-growth-promoting diazotrophic bacterium isolated from rhizosphere soil of groundnut. Int J Syst Evol Microbiol 2010, 60:1559-1564.
- [14]Hardoim PR: Bacterial endophytes of rice: diversity, characteristics and perspectives. Ridderkerk.. Ridderprint: NL; 2011.
- [15]Lee HS, Madhaiyan M, Kim CW, Choi SJ, Chung KY, Sa TM: Physiological enhancement of early growth of rice seedlings (Oryza sativaL.) by production of phytohormone of N2-fixing methylotrophic isolates. Biol Fert Soils 2006, 42:402-408.
- [16]Mollet C, Drancourt M, Raoult D: rpoB sequence analysis as a novel basis for bacterial identification. Mol Microbiol 1997, 26:1005-11.
- [17]Adékambi T, Drancourt M, Raoult D: The rpoB gene as a tool for clinical microbiologists. Trends Microbiol 2009, 17:37-45.
- [18]Drancourt M, Bollet C, Carta A, Rousselier P: Phylogenetic analyses of Klebsiella species delineate Klebsiella and Raoultella gen. nov., with description of Raoultella ornithinolytica comb. nov., Raoultella terrigena comb. nov. and Raoultella planticola comb. nov. Int J Syst Evol Microbiol 2001, 51:925-32.
- [19]Ruppel S, Rühlmann J, Merbach W: Quantification and localization of bacteria in plant tissues using quantitative real-time PCR and online emission fingerprinting. Plant Soil 2006, 286:21-35.
- [20]Mesbah M, Premachandran U, Whitman WB: Precise measurement of the G+C content of deoxyribonucleic acid by High-Performance Liquid Chromatography. Inte J Syst Bacteriol 1989, 39:159-167.
- [21]Grimont F, Grimont P: The genus Enterobacter. In The Prokaryotes. 3rd edition. Edited by Dworkin M, Falkow S, Rosenberg E, Schleifer K-H, Stackebrandt E. Singapore: Springer; 2006:197-214.
- [22]Grimont F, Grimont P: The Proteobacteria. vol 2. In Bergey’s Manual of Systematic Bacteriology. 2nd edition. Edited by Brenner D, Krieg N, Staley J, Garrity G. Singapore: Springer; 2005:587-850.
- [23]Hoffmann H, Stindl S, Ludwig W, Stumpf A, Mehlen A, Heesemann J, Monget D, Schleifer KH, Roggenkamp A: Reassignment of Enterobacter dissolvens to Enterobacter cloacae asE. cloacae subspecies dissolvens comb. nov. and emended description of Enterobacter asburiae and Enterobacter kobei. Syst Appl Microbiol 2005, 28:196-205.
- [24]Hormaeche E, Edwards PR: Observations on the genus Aerobacter with a description of two species. Int J Syst Evol Microbiol 1958, 8:111-116.
- [25]Bouvet OMM, Lenormand P, Grimont PAD: Taxonomic diversity of the D-glucose oxidation pathway in the Enterobacteriaceae. Int J Syst Evol Microbiol 1989, 39:61-67.
- [26]Wang GF, Xie GL, Zhu B, Huang JS, Liu B, Kawicha P, Benyon L, Duan YP: Identification and characterization of the Enterobacter complex causing mulberry (Morus alba) wilt disease in China. Eur J Plant Pathol 2009, 126:465-478.
- [27]Kim KY, Hwangbo H, Park RD, Kim YW, Rim YS, Park KH, Kim TH, Suh JS: 2-Ketogluconic acid production and phosphate solubilization by Enterobacter intermedium. Curr Microbiol 2003, 47:87-92.
- [28]Reinhold-Hurek B, Hurek T: Living inside plants: bacterial endophytes. Curr Opin Plant Biol 2011, 14:435-43.
- [29]Sessitsch A, Hardoim P, Döring J, Weilharter A, Krause A, Woyke T, Mitter B, Hauberg-Lotte L, Friedrich F, Rahalkar M, Hurek T, Sarkar A, Bodrossy L, Van Overbeek L, Brar D, Van Elsas JD, Reinhold-Hurek B: Functional characteristics of an endophyte community colonizing rice roots as revealed by metagenomic analysis. Mol Plant Microbe In 2012, 25:28-36.
- [30]Stevens P, Van Elsas JD: Genetic and phenotypic diversity of Ralstonia solanacearum biovar 2 strains obtained from Dutch waterways. Antonie Van Leeuwenhoek 2010, 97:171-88.
- [31]Pruesse E, Quast C, Knittel K, Fuchs BM, Ludwig W, Peplies J, Glöckner FO: SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucleic Acids Res 2007, 35:7188-96.
- [32]Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S: MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 2011, 28:2731-9.
- [33]Wilson K: Preparation of genomic DNA from bacteria. In Current Protocols in Molecular Biology. Edited by Ausubel F, Brent R, Kingston R, Moore D, Seidman J, Smith J, Struhl K. New York, NY: Greene Publishing and Wiley-Interscience; 1987:2.4.1-2.4.5.
- [34]Ezaki T, Hashimoto Y, Yabuuchi E: Fluorometric deoxyribonucleic acid-deoxyribonucleic acid hybridization in microdilution wells as an alternative to membrane filter hybridization in which radioisotopes are used to determine genetic relatedness among bacterial strains. Int J Syst Bacteriol 1989, 39:224-229.
- [35]Gerhardt P, Gerhardt P, Murray R, Krieg NR, Wood WA, Wood WA: Methods for General and Molecular Bacteriology . Washington, DC: ASM Press; 1994.
- [36]Gordon SA, Weber RP: Colorimetric estimation of indoleacetic acid. Plant Physiol 1951, 26:192-5.
- [37]Schwyn B, Neilands JB: Universal chemical assay for the detection and determination of siderophores. Anal Biochem 1987, 160:47-56.
- [38]Nautiyal CS: An efficient microbiological growth medium for screening phosphate solubilizing microorganisms. FEMS Microbiol Lett 1999, 170:265-270.
- [39]Semenov AM, van Bruggen AHC, Zelenev VV: Moving waves of bacterial populations and total organic carbon along roots of wheat. Microb Ecol 1999, 37:116-128.
- [40]Penrose DM, Glick BR: Methods for isolating and characterizing ACC deaminase-containing plant growth-promoting rhizobacteria. Physiol Plant 2003, 118:10-15.
- [41]Corpe WA: A method for detecting methylotrophic bacteria on solid surfaces. J Microbiol Meth 1985, 3:215-221.
- [42]McDonald I, Murrell J: The methanol dehydrogenase structural gene mxaF and its use as a functional gene probe for methanotrophs and methylotrophs. Appl Envir Microbiol 1997, 63:3218-3224.
- [43]Poly F, Monrozier LJ, Bally R: Improvement in the RFLP procedure for studying the diversity of nifH genes in communities of nitrogen fixers in soil. Res Microbiol 2001, 152:95-103.
- [44]Andreote FD, de Araújo WL, de Azevedo JL, Van Elsas JD, da Rocha UN, Van Overbeek LS: Endophytic colonization of potato (Solanum tuberosum L.) by a novel competent bacterial endophyte, Pseudomonas putida strain P9, and its effect on associated bacterial communities. Appl Environ Microbiol 2009, 75:3396-406.
- [45]Inceoglu O, Hoogwout EF, Hill P, Van Elsas JD: Effect of DNA extraction method on the apparent microbial diversity of soil. Appl Environ Microbiol 2010, 76:3378-82.
- [46]Hurek T, Reinhold-Hurek B, Van Montagu M, Kellenberger E: Root colonization and systemic spreading ofAzoarcussp. strain BH72 in grasses. J Bacteriol 1994, 176:1913-23.
- [47]Rademaker J, Louws F, Versalovic J, de Bruijn F: Characterization of the diversity of ecologically important microbes by rep-PCR genomic fingerprinting. In Molecular Microbial Ecology Manual. Edited by Kowalchuk G, de Bruijn F, Head I, Akkermans A, van Elsas J. Dordrecht NL: Springer; 2004:611-644.