Plant genotype-specific archaeal and bacterial endophytes but similar Bacillus antagonists colonize Mediterranean olive trees

Frontiers in Microbiology

Volumn 6, Issue MAR, 2015, Pages

  Müller, Henry ^a   Berg, Christian ^b   Landa, Blanca B ^c   Auerbach, Anna ^d   Moissl Eichinger, Christine ^d,e,f   Berg, Gabriele ^a  

^a GRAZ UNIVERSITY OF TECHNOLOGY   (Austria)

^b UNIVERSITY OF GRAZ   (Austria)

^c INSTITUTO DE AGRICULTURA SOSTENIBLE   (Spain)

^d UNIVERSITY OF REGENSBURG   (Germany)

^e MEDICAL UNIVERSITY OF GRAZ   (Austria)

^f BIOTECHMED GRAZ   (Austria)

Author keywords

Antagonistic bacteria; Archaea; Endophytes; Olea europaea; Verticillium dahliae

Indexed keywords

ACTINOBACTERIA; ARTICLE; BACTERIAL COLONIZATION; BACTERIAL STRAIN; BACTERIUM ISOLATION; BACTEROIDETES; CRENARCHAEOTA; ENDOPHYTE; EURYARCHAEOTA; FIRMICUTES; GENE SEQUENCE; GENETIC VARIABILITY; GENOTYPE ENVIRONMENT INTERACTION; GEOGRAPHIC DISTRIBUTION; MICROBIAL COMMUNITY; MICROBIOME; NONHUMAN; OLIVE TREE; ORGANISMAL INTERACTION; POLYMERASE CHAIN REACTION; PROTEOBACTERIA; REAL TIME POLYMERASE CHAIN REACTION; THAUMARCHAEOTA; VERTICILLIUM DAHLIAE;

ACTINOBACTERIA; ARCHAEA; BACILLUS (BACTERIUM); BACILLUS AMYLOLIQUEFACIENS; BACTERIA (MICROORGANISMS); BACTEROIDETES; CRENARCHAEOTA; EURYARCHAEOTA; FIRMICUTES; FUNGI; OLEA EUROPAEA; OLEA EUROPAEA VAR. SYLVESTRIS; OLEACEAE; PROTEOBACTERIA; VERTICILLIUM DAHLIAE;

EID: 84927167679     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2015.00138     Document Type: Article

References (52)

1. Alavi, P., Starcher, M. R., Zachow, C., Müller, H., and Berg, G. (2013). Root-microbe systems: the effect and mode of interaction of stress protecting agent (SPA) Stenotrophomonas rhizophila DSM14405T. Front. Plant Sci. 4:141. doi: 10.3389/fpls.2013.00141.
2. Amann, R. I., Ludwig, W., and Schleifer, K. H. (1995). Phylogenetic identification and in situ detection of individual microbial cells without cultivation. Microbiol. Rev. 59, 143-169.
3. Aranda, S., Montes-Borrego, M., Jiménez-Díaz, R. M., and Landa, B. B. (2011). Microbial communities associated with the root system of wild olives (Olea europaea L. subsp. europaea var. sylvestris) are good reservoirs of bacteria with antagonistic potential against Verticillium dahliae. Plant Soil 343, 329-345. doi: 10.1007/s11104-011-0721-2.
4. Backman, P. A., and Sikora, R. A. (2008). Endophytes: an emerging tool for biological control. Biol. Control 46, 1-3. doi: 10.1016/j.biocontrol.2008.03.009.
5. Berg, G. (2009). Plant-microbe interactions promoting plant growth and health: perspectives for controlled use of microorganisms in agriculture. Appl. Microbiol. Biotechnol. 84, 11-18. doi: 10.1007/s00253-009-2092-7.
6. Berg, G. (2014). Beyond borders: investigating microbiome interactivity and diversity for advanced biocontrol technologies. Microb. Biotechnol. doi: 10.1111/1751-7915.12235 [Epub ahead of print].
7. Berg, G., Krechel, A., Ditz, M., Sikora, R. A., Ulrich, A., and Hallmann, J. (2005). Endophytic and ectophytic potato-associated bacterial communities differ in structure and antagonistic function against plant pathogenic fungi. FEMS Microbiol. Ecol. 51, 215-229. doi: 10.1016/j.femsec.2004.08.006.
8. Berg, G., Zachow, C., Müller, H., Phillips, J., and Tilcher, R. (2013). Next-generation bio-products sowing the seeds of success for sustainable agriculture. Agronomy 3, 648-656. doi: 10.3390/agronomy3040648.
9. Besnard, G., Khadari, B., Navascués, M., Fernández-Mazuecos, M., El Bakkali, A., Arrigo, N., et al. (2013). The complex history of the olive tree: from late quaternary diversification of Mediterranean lineages to primary domestication in the northern Levant. Proc. R. Soc. B Biol. Sci. 280, 1471-2954. doi: 10.1098/rspb.2012.2833.
10. Breton, C., Pinatel, C., Médail, F., Bonhomme, F., and Bervillé, A. (2008). Comparison between classical and Bayesian methods to investigate the history of olive cultivars using SSR-polymorphisms. Plant Sci. 175, 524-532. doi: 10.1016/j.plantsci.2008.05.025.
11. Breton, C., Terral, J. F., Pinatel, C., Médail, F., Bonhomme, F., and Bervillé, A. (2009). The origins of the domestication of the olive tree. C. R. Biol. 332, 1059-1064. doi: 10.1016/j.crvi.2009.08.001.
12. Bulgarelli, D., Schlaeppi, K., Spaepen, S., van Themaat, E. V. L., and Schulze-Lefert, P. (2013). Structure and functions of the bacterial microbiota of plants. Annu. Rev. Plant Biol. 64, 807-838. doi: 10.1146/annurev-arplant-050312-120106.
13. Caporaso, J. G., Lauber, C. L., Walters, W. A., Berg-Lyons, D., Huntley, J., Fierer, N., et al. (2012). Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. ISME J. 6, 1621-1624. doi: 10.1038/ismej.2012.8.
14. 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.
15. Díaz, A., Rosa, R., Martín, A., and Rallo, P. (2006). Development, characterization and inheritance of new microsatellites in olive (Olea europaea L.) and evaluation of their usefulness in cultivar identification and genetic relationship studies. Tree Genet. Genomes 2, 165-175. doi: 10.1007/s11295-006-0041-5.
16. Díez, C. M., Trujillo, I., Barrio, E., Belaj, A., Barranco, D., and Rallo, L. (2011). Centennial olive trees as a reservoir of genetic diversity. Ann. Bot. 108, 797-807. doi: 10.1093/aob/mcr194.
17. Edgar, R. C. (2010). Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26, 2460-2461. doi: 10.1093/bioinformatics/btq461.
18. 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.
19. El Fantroussi, S., Verschuere, L., Verstraete, W., and Top, E. M. (1999). Effect of phenylurea herbicides on soil microbial communities estimated by analysis of 16S rRNA gene fingerprints and community level physiological profiles. Appl. Environ. Microbiol. 65, 982-988.
20. Emmert, E. A., and Handelsman, J. (1999). Biocontrol of plant disease: a (gram-) positive perspective. FEMS Microbiol. Lett. 171, 1-9. doi: 10.1111/j.1574-6968.1999.tb13405.x.
21. Finkel, O. M., Burch, A. Y., Lindow, S. E., Post, A. F., and Belkin, S. (2011). Geographical location determines the population structure in phyllosphere microbial communities of a salt-excreting desert tree. Appl. Environ. Microbiol. 77, 7647-7655. doi: 10.1128/AEM.05565-11.
22. FAOSTAT. (2014). Agricultural Production Database. Available at: http://faostat3.fao.org (accessed October 23, 2014).
23. Green, P. S. (2002). A revision of Olea L. (Oleaceae). Kew Bull. 57, 91-140. doi: 10.2307/4110824.
24. Hallmann, J., Quadt-Hallmann, A., Mahaffee, W., and Kloepper, J. (1997). Bacterial endophytes in agricultural crops. Can. J. Microbiol. 43, 895-914. doi: 10.1139/m97-131.
25. Haouane, H., El Bakkali, A., Moukhli, A., Tollon, C., Santoni, S., Oukabli, A., et al. (2011). Genetic structure and core collection of the World Olive Germplasm Bank of Marrakech: towards the optimized management and use of Mediterranean olive genetic resources. Genetica 139, 1083-1094. doi: 10.1007/s10709-011-9608-7.
26. Hardoim, P. R., van Overbeek, L. S., and van 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.
27. Jiménez-Díaz, R. M., Olivares-García, C., Landa, B. B., del Mar Jiménez-Gasco, M., and Navas-Cortés, J. (2011). Region-wide analysis of genetic diversity in Verticillium dahliae populations infecting olive in southern Spain and agricultural factors influencing the distribution and prevalence of vegetative compatibility groups and pathotypes. Phytopathology 101, 304-315. doi: 10.1094/PHYTO-07-10-0176.
28. Kloepper, J. W., Ryu, C.-M., and Zhang, S. (2004). Induced systemic resistance and promotion of plant growth by Bacillus spp. Phytopathology 94, 1259-1266. doi: 10.1094/PHYTO.2004.94.11.1259.
29. Knief, C., Delmotte, N., Chaffron, S., Stark, M., Innerebner, G., Wassmann, R., et al. (2012). Metaproteogenomic analysis of microbial communities in the phyllosphere and rhizosphere of rice. ISME J. 6, 1378-1390. doi: 10.1038/ismej.2011.192.
30. López-Escudero, F. J., and Mercado-Blanco, J. (2011). Verticillium wilt of olive: a case study to implement an integrated strategy to control a soil-borne pathogen. Plant Soil 344, 1-50. doi: 10.1007/s11104-010-0629-2.
31. 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.
32. Lumaret, R., and Quazzani, N. (2001). Ancient wild olives in Mediterranean forests. Nature 413, 700. doi: 10.1038/35099680.
33. Ma, B., Lv, X., Warren, A., and Gong, J. (2013). Shifts in diversity and community structure of endophytic bacteria and archaea across root, stem and leaf tissues in the common reed, Phragmites australis, along a salinity gradient in a marine tidal wetland of northern China. Antonie Van Leeuwenhoek 104, 759-768. doi: 10.1007/s10482-013-9984-3.
34. Magoc, T., and Salzberg, S. (2011). FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27, 2957-2963. doi: 10.1093/bioinformatics/btr507.
35. Maldonado-González, M. M., Prieto, P., Ramos, C., and Mercado-Blanco, J. (2013). From the root to the stem: interaction between the biocontrol root endophyte Pseudomonas fluorescens PICF7 and the pathogen Pseudomonas savastanoi NCPPB 3335 in olive knots. Microb. Biotechnol. 6, 275-287. doi: 10.1111/1751-7915.12036.
36. Maldonado-González, M. M., Schilirò, E., Prieto, P., and Mercado-Blanco, J. (2015). Endophytic colonization and biocontrol performance of Pseudomonas fluorescens PICF7 in olive (Olea europaea L.) are determined neither by pyoverdine production nor swimming motility. Environ. Microbiol. doi: 10.1111/1462-2920.12725 [Epub ahead of print].
37. Marten, P., Smalla, K., and Berg, G. (2000). Genotypic and phenotypic differentiation of an antifungal biocontrol strain belonging to Bacillus subtilis. J. Appl. Microbiol. 89, 463-471. doi: 10.1046/j.1365-2672.2000.01136.x.
38. Mercado-Blanco, J., Rodríguez-Jurado, D., Hervás, A., and Jiménez-Díaz, R. M. (2004). Suppression of Verticillium wilt in olive planting stocks by root-associated fluorescent Pseudomonas spp. Biol. Control 30, 474-486. doi: 10.1016/j.biocontrol.2004.02.002.
39. Oliveira, M. N., Santos, T. M., Vale, H. M., Delvaux, J. C., Cordero, A. P., Ferreira, A. B., et al. (2013). Endophytic microbial diversity in coffee cherries of Coffea arabica from southeastern Brazil. Can. J. Microbiol. 59, 221-230. doi: 10.1139/cjm-2012-0674.
40. Palomares-Rius, J. E., Castillo, P., Montes-Borrego, M., Müller, H., and Landa, B. B. (2012). Nematode community populations in the rhizosphere of cultivated olive differs according to the plant genotype. Soil Biol. Biochem. 45, 168-171. doi: 10.1016/j.soilbio.2011.11.009.
41. Prieto, P., and Mercado-Blanco, J. (2008). Endophytic colonization of olive roots by the biocontrol strain Pseudomonas fluorescens PICF7. FEMS Microbiol. Ecol. 64, 297-306. doi: 10.1111/j.1574-6941.2008.00450.x.
42. Prieto, P., Navarro-Raya, C., Valverde-Corredor, A., Amyotte, S. G., Dobinson, K. F., and Mercado-Blanco, J. (2009). Colonization process of olive tissues by Verticillium dahliae and its in planta interaction with the biocontrol root endophyte Pseudomonas fluorescens PICF7. Microb. Biotechnol. 2, 499-511. doi: 10.1111/j.1751-7915.2009.00105.x.
43. Probst, A. J., Auerbach, A. K., and Moissl-Eichinger, C. (2013). Archaea on human skin. PLoS ONE 8:e65388. doi: 10.1371/journal.pone.0065388.
44. Pruesse, E., Peplies, J., and Glöckner, F. O. (2012). SINA: accurate high-throughput multiple sequence alignment of ribosomal RNA genes. Bioinformatics 28, 1823-1829. doi: 10.1093/bioinformatics/bts252.
45. Raskin, L., Stromley, J. M., Rittmann, B. E., and Stahl, D. A. (1994). Group-specific 16S rRNA hybridization probes to describe natural communities of methanogens. Appl. Environ. Microbiol. 60, 1232-1240.
46. 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.
47. 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.
48. Rosenblueth, M., and Martínez-Romero, E. (2006). Bacterial endophytes and their interactions with hosts. Mol. Plant Microbe Interact. 19, 827-837. doi: 10.1094/MPMI-19-0827.
49. Ryan, R. P., Germaine, K., Franks, A., Ryan, D. J., and Dowling, D. N. (2008). Bacterial endophytes: recent developments and applications. FEMS Microbiol. Lett. 278, 1-9. doi: 10.1111/j.1574-6968.2007.00918.x.
50. Sanchez-Azofeifa, A., Oki, Y., Fernandes, G., Ball, R. A., and Gamon, J. (2012). Relationships between endophyte diversity and leaf optical properties. Trees 26, 291-299. doi: 10.1007/s00468-011-0591-5.
51. Wang, Q., Garrity, G. M., Tiedje, J. M., and Cole, J. R. (2007). Naïve 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.
52. Zohary, D., and Spiegel-Roy, P. (1975). Beginnings of fruit growing in the old world. Science 31, 319-327. doi: 10.1126/science.187.4174.319.