Comparative transcriptomics of Bacillus mycoides root exudates reveals different genetic adaptation of endophytic and soil isolates

Frontiers in Microbiology

Volumn 8, Issue AUG, 2017, Pages

  Yi, Yanglei ^a   de Jong, Anne ^a   Frenzel, Elrike ^a   Kuipers, Oscar P ^a  

^a UNIVERSITY OF GRONINGEN   (Netherlands)

Author keywords

Bacillus mycoides; Endophyte; Root colonization; Root exudates; Transcriptome

Indexed keywords

AMINO ACID METABOLISM; ARTICLE; BACILLUS MYCOIDES; CONFOCAL LASER SCANNING MICROSCOPY; DNA EXTRACTION; DNA SEQUENCE; EVOLUTIONARY ADAPTATION; FLUORESCENCE MICROSCOPY; GENE EXPRESSION; GENETIC ANALYSIS; NONHUMAN; OVERLAPPING GENE; PHENOTYPE; ROOT EXUDATE; SOIL ANALYSIS; TRANSCRIPTOMICS;

EID: 85026818311     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2017.01487     Document Type: Article

References (64)

1. Ali, S., Duan, J., Charles, T. C., and Glick, B. R. (2014). A bioinformatics approach to the determination of genes involved in endophytic behavior in Burkholderia spp. J. Theor. Biol. 343, 193-198. doi: 10.1016/j.jtbi.2013.10.007
2. Altenhoff, A. M., Škunca, N., Glover, N., Train, C.-M., Sueki, A., Piližota, I., et al. (2014). The OMA orthology database in 2015: function predictions, better plant support, synteny view and other improvements. Nucleic Acids Res. 43, D240-D249. doi: 10.1093/nar/gku1158
3. Ambrosini, A., Stefanski, T., Lisboa, B. B., Beneduzi, A., Vargas, L. K., and Passaglia, L. M. P. (2016). Diazotrophic bacilli isolated from the sunflower rhizosphere and the potential of Bacillus mycoides B38V as biofertiliser. Ann. Appl. Biol. 168, 93-110. doi: 10.1111/aab.12245
4. Aziz, R. K., Bartels, D., Best, A. A., DeJongh, M., Disz, T., Edwards, R. A., et al. (2008). The RAST Server: rapid annotations using subsystems technology. BMC Genomics 9:75. doi: 10.1186/1471-2164-9-75
5. Bargabus, R., Zidack, N., Sherwood, J., and Jacobsen, B. (2002). Characterisation of systemic resistance in sugar beet elicited by a non-pathogenic, phyllosphere-colonizing Bacillus mycoides, biological control agent. Physiol. Mol. Plant Pathol. 61, 289-298. doi: 10.1006/pmpp.2003.0443
6. Brencic, A., and Winans, S. C. (2005). Detection of and response to signals involved in host-microbe interactions by plant-associated bacteria. Microbiol. Mol. Biol. Rev. 69, 155-194. doi: 10.1128/MMBR.69.1.155-194.2005
7. Compant, S., Clément, C., and Sessitsch, A. (2010). Plant growth-promoting bacteria in the rhizo-and endosphere of plants: their role, colonization, mechanisms involved and prospects for utilization. Soil Biol. Biochem. 42, 669-678. doi: 10.1016/j.soilbio.2009.11.024
8. de Jong, A., van der Meulen, S., Kuipers, O. P., and Kok, J. (2015). T-REx: transcriptome analysis webserver for RNA-seq expression data. BMC Genomics 16:663. doi: 10.1186/s12864-015-1834-4
9. Di Franco, C., Beccari, E., Santini, T., Pisaneschi, G., and Tecce, G. (2002). Colony shape as a genetic trait in the pattern-forming Bacillus mycoides. BMC Microbiol. 2:33. doi: 10.1186/1471-2180-2-33
10. Fan, B., Carvalhais, L. C., Becker, A., Fedoseyenko, D., von Wirén, N., and Borriss, R. (2012). Transcriptomic profiling of Bacillus amyloliquefaciens FZB42 in response to maize root exudates. BMC Microbiol. 12:116. doi: 10.1186/1471-2180-12-116
11. Glick, B. R. (2012). Plant growth-promoting bacteria: mechanisms and applications. Scientifica 2012:963401. doi: 10.6064/2012/963401
12. Gómez-Lama Cabanás, C., Schilirò, E., Valverde-Corredor, A., and Mercado-Blanco, J. (2014). The biocontrol endophytic bacterium Pseudomonas fluorescens PICF7 induces systemic defense responses in aerial tissues upon colonization of olive roots. Front. Microbiol. 5:427. doi: 10.3389/fmicb.2014.00427
13. 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
14. Harris, M. A., Clark, J., Ireland, A., Lomax, J., Ashburner, M., Foulger, R., et al. (2004). The gene ontology (GO) database and informatics resource. Nucleic Acids Res. 32(Suppl. 1), D258-D261
15. Harun-Or-Rashid, M., Khan, A., Hossain, M. T., and Chung, Y. R. (2017). Induction of systemic resistance against aphids by endophytic Bacillus velezensis YC7010 via expressing PHYTOALEXIN DEFICIENT4 in Arabidopsis. Front. Plant Sci. 8:211. doi: 10.3389/fpls.2017.00211
16. Helmann, J. D., and Chamberlin, M. J. (1987). DNA sequence analysis suggests that expression of flagellar and chemotaxis genes in Escherichia coli and Salmonella typhimurium is controlled by an alternative sigma factor. Proc. Natl. Acad. Sci. U.S.A. 84, 6422-6424. doi: 10.1073/pnas.84.18.6422
17. Hoskisson, P., Sharples, G., and Hobbs, G. (2003). The importance of amino acids as carbon sources for Micromonospora echinospora (ATCC 15837). Lett. Appl. Microbiol. 36, 268-271. doi: 10.1046/j.1472-765X.2003.01306.x
18. Janczarek, M., Rachwal, K., Marzec, A., Grzadziel, J., and Palusinska-Szysz, M. (2015). Signal molecules and cell-surface components involved in early stages of the legume-rhizobium interactions. Appl. Soil Ecol. 85, 94-113. doi: 10.1111/j.1462-5822.2010.01561.x
19. Jasim, B., Jimtha John, C., Shimil, V., Jyothis, M., and Radhakrishnan, E. (2014). Studies on the factors modulating indole-3-acetic acid production in endophytic bacterial isolates from Piper nigrum and molecular analysis of ipdc gene. J. Appl. Microbiol. 117, 786-799. doi: 10.1111/jam.12569
20. Ji, X., Lu, G., Gai, Y., Zheng, C., and Mu, Z. (2008). Biological control against bacterial wilt and colonization of mulberry by an endophytic Bacillus subtilis strain. FEMS Microbiol. Ecol. 65, 565-573. doi: 10.1111/j.1574-6941.2008.00543.x
21. Jin, H., Yang, X., Yan, Z., Liu, Q., Li, X., Chen, J., et al. (2014). Characterization of rhizosphere and endophytic bacterial communities from leaves, stems and roots of medicinal Stellera chamaejasme L. Syst. Appl. Microbiol. 37, 376-385. doi: 10.1016/j.syapm.2014.05.001
22. Kandel, S. L., Firrincieli, A., Joubert, P. M., Okubara, P., Leston, N. D., McGeorge, K. M., et al. (2017). An in vitro study of bio-control and plant growth promotion potential of Salicaceae endophytes. Front. Microbiol. 8:386. doi: 10.3389/fmicb.2017.00386
23. Kuiper, I., Bloemberg, G. V., Noreen, S., Thomas-Oates, J. E., and Lugtenberg, B. J. (2001). Increased uptake of putrescine in the rhizosphere inhibits competitive root colonization by Pseudomonas fluorescens strain WCS365. Mol. Plant Microbe Interact. 14, 1096-1104. doi: 10.1094/MPMI.2001.14.9.1096
24. Kuiper, I., Lagendijk, E. L., Bloemberg, G. V., and Lugtenberg, B. J. (2004). Rhizoremediation: a beneficial plant-microbe interaction. Mol. Plant Microbe Interact. 17, 6-15. doi: 10.1094/MPMI.2004.17.1.6
25. Lagesen, K., Hallin, P., Rødland, E. A., Stærfeldt, H.-H., Rognes, T., and Ussery, D. W. (2007). RNAmmer: consistent and rapid annotation of ribosomal RNA genes. Nucleic Acids Res. 35, 3100-3108. doi: 10.1093/nar/gkm160
26. Lakshmanan, V., Castaneda, R., Rudrappa, T., and Bais, H. P. (2013). Root transcriptome analysis of Arabidopsis thaliana exposed to beneficial Bacillus subtilis FB17 rhizobacteria revealed genes for bacterial recruitment and plant defense independent of malate efflux. Planta 238, 657-668. doi: 10.1007/s00425-013-1920-2
27. Lee, S., Flores-Encarnacion, M., Contreras-Zentella, M., Garcia-Flores, L., Escamilla, J., 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
28. Lowe, T. M., and Eddy, S. R. (1997). tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res. 25, 955-964. doi: 10.1093/nar/25.5.0955
29. Lugtenberg, B. J., Dekkers, L., and Bloemberg, G. V. (2001). Molecular determinants of rhizosphere colonization by Pseudomonas. Annu. Rev. Phytopathol. 39, 461-490. doi: 10.1146/annurev.phyto.39.1.461
30. Malfanova, N., Lugtenberg, B., and Berg, G. (2013). Bacterial Endophytes: Who and Where, and What are they Doing there? Hoboken, NJ: Wiley-Blackwell
31. Mark, G. L., Dow, J. M., Kiely, P. D., Higgins, H., Haynes, J., Baysse, C., et al. (2005). Transcriptome profiling of bacterial responses to root exudates identifies genes involved in microbe-plant interactions. Proc. Natl. Acad. Sci. U.S.A. 102, 17454-17459. doi: 10.1073/pnas.0506407102
32. Martinez, J. L., Sanchez, M. B., Martinez-Solano, L., Hernandez, A., Garmendia, L., Fajardo, A., et al. (2009). Functional role of bacterial multidrug efflux pumps in microbial natural ecosystems. FEMS Microbiol. Rev. 33, 430-449. doi: 10.1111/j.1574-6976.2008.00157.x
33. Mirel, D. B., and Chamberlin, M. J. (1989). The Bacillus subtilis flagellin gene (hag) is transcribed by the sigma 28 form of RNA polymerase. J. Bacteriol. 171, 3095-3101. doi: 10.1128/jb.171.6.3095-3101.1989
34. Molina-Henares, A. J., Krell, T., Eugenia Guazzaroni, M., Segura, A., and Ramos, J. L. (2006). Members of the IclR family of bacterial transcriptional regulators function as activators and/or repressors. FEMS Microbiol. Rev. 30, 157-186. doi: 10.1111/j.1574-6976.2005.00008.x
35. Mónica, R., and Esperanza, M.-R. (2006). Bacterial endophytes and their interactions with Hosts. Mol. Plant Microbe Interact. 19, 827-837. doi: 10.1094/MPMI-19-0827
36. Moreno, R., Martínez-Gomariz, M., Yuste, L., Gil, C., and Rojo, F. (2009). The Pseudomonas putida Crc global regulator controls the hierarchical assimilation of amino acids in a complete medium: evidence from proteomic and genomic analyses. Proteomics 9, 2910-2928. doi: 10.1002/pmic.200800918
37. Namy, O., Mock, M., and Fouet, A. (1999). Co-existence of clpB and clpC in the Bacillaceae. FEMS Microbiol. Lett. 173, 297-302. doi: 10.1111/j.1574-6968.1999.tb13517.x
38. Neher, O. T., Johnston, M. R., Zidack, N. K., and Jacobsen, B. J. (2009). Evaluation of Bacillus mycoides isolate BmJ and B. mojavensis isolate 203-7 for the control of anthracnose of cucurbits caused by Glomerella cingulata var. orbiculare. Biol. Control 48, 140-146. doi: 10.1016/j.biocontrol.2008.08.012
39. Pangesti, N., Pineda, A., Dicke, M., and Loon, J. (2015). Variation in plant-mediated interactions between rhizobacteria and caterpillars: potential role of soil composition. Plant Biol. 17, 474-483. doi: 10.1111/plb.12265
40. Phillips, D. A., Joseph, C. M., and Maxwell, C. A. (1992). Trigonelline and stachydrine released from alfalfa seeds activate NodD2 protein in Rhizobium meliloti. Plant Physiol. 99, 1526-1531. doi: 10.1104/pp.99.4.1526
41. Prashar, P., Kapoor, N., and Sachdeva, S. (2013). Rhizosphere: its structure, bacterial diversity and significance. Rev. Environ. Sci. Bio/Technol. 13, 63-77. doi: 10.1007/s11157-013-9317-z
42. Prieto, P., Schiliro, E., Maldonado-Gonzalez, M. M., Valderrama, R., Barroso-Albarracin, J. B., and Mercado-Blanco, J. (2011). Root hairs play a key role in the endophytic colonization of olive roots by Pseudomonas spp. with biocontrol activity. Microb. Ecol. 62, 435-445. doi: 10.1007/s00248-011-9827-6
43. Rosconi, F., Davyt, D., Martínez, V., Martínez, M., Abin-Carriquiry, J. A., Zane, H., et al. (2013). Identification and structural characterization of serobactins, a suite of lipopeptide siderophores produced by the grass endophyte Herbaspirillum seropedicae. Environ. Microbiol. 15, 916-927. doi: 10.1111/1462-2920.12075
44. Rosenblueth, M., and Martínez-Romero, E. (2004). Rhizobium etli maize populations and their competitiveness for root colonization. Arch. Microbiol. 181, 337-344. doi: 10.1007/s00203-004-0661-9
45. Santos, F., Peñaflor, M. F. G., Paré, P. W., Sanches, P. A., Kamiya, A. C., Tonelli, M., et al. (2014). A novel interaction between plant-beneficial rhizobacteria and roots: colonization induces corn resistance against the root herbivore Diabrotica speciosa. PLoS ONE 9:e113280. doi: 10.1371/journal.pone.0113280
46. Santoyo, G., Moreno-Hagelsieb, G., Orozco-Mosqueda Mdel, C., and Glick, B. R. (2016). Plant growth-promoting bacterial endophytes. Microbiol. Res. 183, 92-99. doi: 10.1016/j.micres.2015.11.008
47. Schaefer, A. L., Oda, Y., Coutinho, B. G., Pelletier, D. A., Weiburg, J., Venturi, V., et al. (2016). A LuxR homolog in a cottonwood tree endophyte that activates gene expression in response to a plant signal or specific peptides. mBio 7:e01101-16. doi: 10.1128/mBio.01101-16
48. Shidore, T., Dinse, T., Ohrlein, J., Becker, A., and Reinhold-Hurek, B. (2012). Transcriptomic analysis of responses to exudates reveal genes required for rhizosphere competence of the endophyte Azoarcus sp. strain BH72. Environ. Microbiol. 14, 2775-2787. doi: 10.1111/j.1462-2920.2012.02777.x
49. Siguier, P., Pérochon, J., Lestrade, L., Mahillon, J., and Chandler, M. (2006). ISfinder: the reference centre for bacterial insertion sequences. Nucleic Acids Res. 34(Suppl. 1), D32-D36. doi: 10.1093/nar/gkj014
50. Song, Y., Tong, Z., Wang, J., Wang, L., Guo, Z., Han, Y., et al. (2004). Complete genome sequence of Yersinia pestis strain 91001, an isolate avirulent to humans. DNA Res. 11, 179-197. doi: 10.1093/dnares/11.3.179
51. Taghavi, S., Wu, X., Ouyang, L., Zhang, Y. B., Stadler, A., McCorkle, S., et al. (2015). Transcriptional responses to sucrose mimic the plant-associated lifestyle of the plant growth promoting endophyte Enterobacter sp. 638. PLoS ONE 10:e0115455. doi: 10.1371/journal.pone.0115455
52. Tatusov, R. L., Fedorova, N. D., Jackson, J. D., Jacobs, A. R., Kiryutin, B., Koonin, E. V., et al. (2003). The COG database: an updated version includes eukaryotes. BMC Bioinformatics 4:41. doi: 10.1186/1471-2105-4-41
53. Timm, C. M., Campbell, A. G., Utturkar, S. M., Jun, S. R., Parales, R. E., Tan, W. A., et al. (2015). Metabolic functions of Pseudomonas fluorescens strains from Populus deltoides depend on rhizosphere or endosphere isolation compartment. Front. Microbiol. 6:1118. doi: 10.3389/fmicb.2015.01118
54. van Peer, R., Punte, H. L., de Weger, L. A., and Schippers, B. (1990). Characterization of root surface and endorhizosphere pseudomonads in relation to their colonization of roots. Appl. Environ. Microbiol. 56, 2462-2470
55. 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
56. Wilson, A. C., Perego, M., and Hoch, J. A. (2007). New transposon delivery plasmids for insertional mutagenesis in Bacillus anthracis. J. Microbiol. Methods 71, 332-335. doi: 10.1016/j.mimet.2007.09.006
57. Xie, S., Wu, H., Chen, L., Zang, H., Xie, Y., and Gao, X. (2015). Transcriptome profiling of Bacillus subtilis OKB105 in response to rice seedlings. BMC Microbiol. 15:21. doi: 10.1186/s12866-015-0353-4
58. Yi, H.-S., Yang, J. W., and Ryu, C.-M. (2013). ISR meets SAR outside: additive action of the endophyte Bacillus pumilus INR7 and the chemical inducer, benzothiadiazole, on induced resistance against bacterial spot in field-grown pepper. Front. Plant Sci. 4:122. doi: 10.3389/fpls.2013.00122
59. Yi, Y., and Kuipers, O. P. (2017). Development of an efficient electroporation method for rhizobacterial Bacillus mycoides strains. J. Microbiol. Methods 133, 82-86. doi: 10.1016/j.mimet.2016.12.022
60. Zerbino, D. R., and Birney, E. (2008). Velvet: algorithms for de novo short read assembly using de Bruijn graphs. Genome Res. 18, 821-829. doi: 10.1101/gr.074492.107
61. Zhang, N., Wang, D., Liu, Y., Li, S., Shen, Q., and Zhang, R. (2014). Effects of different plant root exudates and their organic acid components on chemotaxis, biofilm formation and colonization by beneficial rhizosphere-associated bacterial strains. Plant Soil 374, 689-700. doi: 10.1007/s11104-013-1915-6
62. Zhang, N., Yang, D., Wang, D., Miao, Y., Shao, J., Zhou, X., et al. (2015). Whole transcriptomic analysis of the plant-beneficial rhizobacterium Bacillus amyloliquefaciens SQR9 during enhanced biofilm formation regulated by maize root exudates. BMC Genomics 16:685. doi: 10.1186/s12864-015-1825-5
63. Zhou, Y., Liang, Y., Lynch, K. H., Dennis, J. J., and Wishart, D. S. (2011). PHAST: a fast phage search tool. Nucleic Acids Res. 39(Suppl. 2), W347-W352. doi: 10.1093/nar/gkr485
64. Zinser, E. R., and Kolter, R. (1999). Mutations enhancing amino acid catabolism confer a growth advantage in stationary phase. J. Bacteriol. 181, 5800-5807