Interaction with soil bacteria affects the growth and amino acid content of piriformospora indica

Exploration of the e ect of soil bacteria on growth and metabolism of beneficial root endophytic fungi is relevant to promote favorable associations between microorganisms of the plant rhizosphere. Hence, the interaction between the plant-growth-promoting fungus Piriformospora indica and di erent so...

Full description

Autores:
Leyva-Rojas, Jorge A.
Coy-Barrera, Ericsson
Hampp, Rüdiger
Tipo de recurso:
Fecha de publicación:
2020
Institución:
Universidad Simón Bolívar
Repositorio:
Repositorio Digital USB
Idioma:
eng
OAI Identifier:
oai:bonga.unisimon.edu.co:20.500.12442/4715
Acceso en línea:
https://hdl.handle.net/20.500.12442/4715
Palabra clave:
Piriformospora indica
Endophytic fungi
Mycorrhiza helper bacteria
Amino acid content
Rights
License
Attribution-NonCommercial-NoDerivatives 4.0 Internacional
id USIMONBOL2_df91155a0285bb44bafd514d2c154d02
oai_identifier_str oai:bonga.unisimon.edu.co:20.500.12442/4715
network_acronym_str USIMONBOL2
network_name_str Repositorio Digital USB
repository_id_str
dc.title.eng.fl_str_mv Interaction with soil bacteria affects the growth and amino acid content of piriformospora indica
title Interaction with soil bacteria affects the growth and amino acid content of piriformospora indica
spellingShingle Interaction with soil bacteria affects the growth and amino acid content of piriformospora indica
Piriformospora indica
Endophytic fungi
Mycorrhiza helper bacteria
Amino acid content
title_short Interaction with soil bacteria affects the growth and amino acid content of piriformospora indica
title_full Interaction with soil bacteria affects the growth and amino acid content of piriformospora indica
title_fullStr Interaction with soil bacteria affects the growth and amino acid content of piriformospora indica
title_full_unstemmed Interaction with soil bacteria affects the growth and amino acid content of piriformospora indica
title_sort Interaction with soil bacteria affects the growth and amino acid content of piriformospora indica
dc.creator.fl_str_mv Leyva-Rojas, Jorge A.
Coy-Barrera, Ericsson
Hampp, Rüdiger
dc.contributor.author.none.fl_str_mv Leyva-Rojas, Jorge A.
Coy-Barrera, Ericsson
Hampp, Rüdiger
dc.subject.eng.fl_str_mv Piriformospora indica
Endophytic fungi
Mycorrhiza helper bacteria
Amino acid content
topic Piriformospora indica
Endophytic fungi
Mycorrhiza helper bacteria
Amino acid content
description Exploration of the e ect of soil bacteria on growth and metabolism of beneficial root endophytic fungi is relevant to promote favorable associations between microorganisms of the plant rhizosphere. Hence, the interaction between the plant-growth-promoting fungus Piriformospora indica and di erent soil bacteria was investigated. The parameters studied were fungal growth and its amino acid composition during the interaction. Fungus and bacteria were confronted in dual cultures in Petri dishes, either through agar or separated by a Perspex wall that only allowed the bacterial volatiles to be e ective. Fungal growth was stimulated by Azotobacter chroococcum, whereas Streptomyces anulatus AcH 1003 inhibited it and Streptomyces sp. Nov AcH 505 had no e ect. To analyze amino acid concentration data, targeted metabolomics was implemented under supervised analysis according to fungal-bacteria interaction and time. Orthogonal partial least squares-discriminant analysis (OPLS-DA) model clearly discriminated P. indica–A. chroococcum and P. indica–S. anulatus interactions, according to the respective score plot in comparison to the control. The most observable responses were in the glutamine and alanine size groups: While Streptomyces AcH 1003 increased the amount of glutamine, A. chroococcum decreased it. The fungal growth and the increase of alanine content might be associated with the assimilation of nitrogen in the presence of glucose as a carbon source. The N-fixing bacterium A. chroococcum should stimulate fungal amino acid metabolism via glutamine synthetase-glutamate synthase (GS-GOGAT). The data pointed to a stimulated glycolytic activity in the fungus observed by the accumulation of alanine, possibly via alanine aminotransferase. The responses toward the growth-inhibiting Streptomyces AcH 1003 suggest an (oxidative) stress response of the fungus.
publishDate 2020
dc.date.accessioned.none.fl_str_mv 2020-02-10T23:00:13Z
dc.date.available.none.fl_str_mv 2020-02-10T23:00:13Z
dc.date.issued.none.fl_str_mv 2020-01
dc.type.eng.fl_str_mv article
dc.type.coarversion.fl_str_mv http://purl.org/coar/version/c_970fb48d4fbd8a85
dc.type.coar.fl_str_mv http://purl.org/coar/resource_type/c_6501
dc.type.driver.eng.fl_str_mv article
dc.identifier.uri.none.fl_str_mv https://hdl.handle.net/20.500.12442/4715
url https://hdl.handle.net/20.500.12442/4715
dc.language.iso.eng.fl_str_mv eng
language eng
dc.rights.*.fl_str_mv Attribution-NonCommercial-NoDerivatives 4.0 Internacional
dc.rights.coar.fl_str_mv http://purl.org/coar/access_right/c_abf2
dc.rights.uri.*.fl_str_mv http://creativecommons.org/licenses/by-nc-nd/4.0/
rights_invalid_str_mv Attribution-NonCommercial-NoDerivatives 4.0 Internacional
http://creativecommons.org/licenses/by-nc-nd/4.0/
http://purl.org/coar/access_right/c_abf2
dc.format.mimetype.spa.fl_str_mv pdf
dc.publisher.eng.fl_str_mv MDPI
dc.source.eng.fl_str_mv Molecules
dc.source.spa.fl_str_mv Vol. 25, No. 3 (2020)
institution Universidad Simón Bolívar
dc.source.uri.eng.fl_str_mv https://doi.org/10.3390/molecules25030572
bitstream.url.fl_str_mv https://bonga.unisimon.edu.co/bitstreams/60bdc0cc-46db-4b21-b069-6c5bcda9fa8d/download
https://bonga.unisimon.edu.co/bitstreams/92ec7bf6-a727-4076-a27e-396275cebd6c/download
https://bonga.unisimon.edu.co/bitstreams/f1aef860-fdde-4616-ae06-daedae51c28c/download
https://bonga.unisimon.edu.co/bitstreams/8af0133a-24a9-4eca-a272-4610173ae32f/download
https://bonga.unisimon.edu.co/bitstreams/67e4e9f8-d322-4620-bc87-ca25c2f822d4/download
https://bonga.unisimon.edu.co/bitstreams/1041181b-b1b0-4217-a0d5-3426b6c37da7/download
https://bonga.unisimon.edu.co/bitstreams/9abdd51c-8463-4f4d-b07b-85122866d325/download
bitstream.checksum.fl_str_mv 18fb80cc673c7d06703b8d7277d4de56
4460e5956bc1d1639be9ae6146a50347
733bec43a0bf5ade4d97db708e29b185
0744776ab86b707c17556ce13947e5a3
ebcaff34dd16702a07af44c104ec5466
116c3f3c8a6152eefdb909fb439e6b18
4def70d227e3ef3fb66580373ed1bb32
bitstream.checksumAlgorithm.fl_str_mv MD5
MD5
MD5
MD5
MD5
MD5
MD5
repository.name.fl_str_mv Repositorio Digital Universidad Simón Bolívar
repository.mail.fl_str_mv repositorio.digital@unisimon.edu.co
_version_ 1814076092219129856
spelling Leyva-Rojas, Jorge A.6c62ccf2-5642-4dc8-b32a-1a042526f75eCoy-Barrera, Ericsson81b6d0b7-0ff3-4df7-833f-7f955508f90dHampp, Rüdigeread459f0-0624-4885-8fef-dae93fa887682020-02-10T23:00:13Z2020-02-10T23:00:13Z2020-01https://hdl.handle.net/20.500.12442/4715Exploration of the e ect of soil bacteria on growth and metabolism of beneficial root endophytic fungi is relevant to promote favorable associations between microorganisms of the plant rhizosphere. Hence, the interaction between the plant-growth-promoting fungus Piriformospora indica and di erent soil bacteria was investigated. The parameters studied were fungal growth and its amino acid composition during the interaction. Fungus and bacteria were confronted in dual cultures in Petri dishes, either through agar or separated by a Perspex wall that only allowed the bacterial volatiles to be e ective. Fungal growth was stimulated by Azotobacter chroococcum, whereas Streptomyces anulatus AcH 1003 inhibited it and Streptomyces sp. Nov AcH 505 had no e ect. To analyze amino acid concentration data, targeted metabolomics was implemented under supervised analysis according to fungal-bacteria interaction and time. Orthogonal partial least squares-discriminant analysis (OPLS-DA) model clearly discriminated P. indica–A. chroococcum and P. indica–S. anulatus interactions, according to the respective score plot in comparison to the control. The most observable responses were in the glutamine and alanine size groups: While Streptomyces AcH 1003 increased the amount of glutamine, A. chroococcum decreased it. The fungal growth and the increase of alanine content might be associated with the assimilation of nitrogen in the presence of glucose as a carbon source. The N-fixing bacterium A. chroococcum should stimulate fungal amino acid metabolism via glutamine synthetase-glutamate synthase (GS-GOGAT). The data pointed to a stimulated glycolytic activity in the fungus observed by the accumulation of alanine, possibly via alanine aminotransferase. The responses toward the growth-inhibiting Streptomyces AcH 1003 suggest an (oxidative) stress response of the fungus.pdfengMDPIAttribution-NonCommercial-NoDerivatives 4.0 Internacionalhttp://creativecommons.org/licenses/by-nc-nd/4.0/http://purl.org/coar/access_right/c_abf2MoleculesVol. 25, No. 3 (2020)https://doi.org/10.3390/molecules25030572Piriformospora indicaEndophytic fungiMycorrhiza helper bacteriaAmino acid contentInteraction with soil bacteria affects the growth and amino acid content of piriformospora indicaarticlearticlehttp://purl.org/coar/version/c_970fb48d4fbd8a85http://purl.org/coar/resource_type/c_6501Deveau, A.; Bonito, G.; Uehling, J.; Paoletti, M.; Becker, M.; Bindschedler, S.; Hacquard, S.; Hervé, V.; Labbé, J.; Lastovetsky, O.A.; et al. Bacterial-fungal interactions: Ecology, mechanisms and challenges. FEMS Microbiol. Rev. 2018, 42, 335–352.Churchland, C.; Grayston, S.J. Specificity of plant-microbe interactions in the tree mycorrhizosphere biome and consequences for soil cycling. Front. Microbiol. 2014, 5, 1–20.Bonfante, P.; Anca, I.-A. Plants,mycorrhizal fungi, and bacteria: a network of interactions. Annu. Rev. Microbiol. 2009, 63, 363–383.Kim, M.; Yoon, H.; Kim, Y.E.; Kim, Y.J.; Kong, W.S.; Kim, J.G. Comparative analysis of bacterial diversity and communities inhabiting the fairy ring of Tricholoma matsutake by barcoded pyrosequencing. J. Appl. Microbiol. 2014, 117, 699–710.Schrey, S.D.; Tarkka, M.T. Friends and foes: Streptomycetes as modulators of plant disease and symbiosis. Antonie van Leeuwenhoek, Int. J. Gen. Mol. Microbiol. 2008, 94, 11–19.Xing, R.; Yan, H.Y.; Gao, Q.B.; Zhang, F.Q.; Wang, J.L.; Chen, S.L. Microbial communities inhabiting the fairy ring of Floccularia luteovirens and isolation of potential mycorrhiza helper bacteria. J. Basic Microbiol. 2018, 58, 554–563.Garbaye, J. Helper bacteria: A new dimension to the mycorrhizal symbiosis. New Phytol. 1994, 128, 197–210.Takács, T.; Cseresnyés, I.; Kovács, R.; Parádi, I.; Kelemen, B.; Szili-Kovács, T.; Füzy, A. Symbiotic e ectivity of dual and tripartite associations on soybean (Glycine max L. Merr.) cultivars inoculated with Bradyrhizobium japonicum and AM Fungi. Front. Plant Sci. 2018, 9, 1–14.Turrini, A.; Avio, L.; Giovannetti, M.; Agnolucci, M. Functional complementarity of arbuscular mycorrhizal fungi and associated microbiota: The challenge of translational research. Front. Plant Sci. 2018, 9, 10–13.Maier, A.; Riedlinger, J.; Fiedler, H.-P.; Hampp, R. Actinomycetales bacteria from a spruce stand: Characterization and effects on growth of root symbiotic and plant parasitic soil fungi in dual culture. Mycol. Prog. 2004, 3, 129–136.Riedlinger, J.; Schrey, S.D.; Tarkka, M.T.; Hampp, R.; Kapur, M.; Fiedler, H.-P. Auxofuran, a novel metabolite that stimulates the growth of fly agaric, is produced by the mycorrhiza helper bacterium Streptomyces strain AcH 505. Appl. Environ. Microbiol. 2006, 72, 3550–3557.Keilhofer, N.; Nachtigall, J.; Kulik, A.; Ecke, M.; Hampp, R.; Süssmuth, R.D.; Fiedler, H.P.; Schrey, S.D. Streptomyces AcH 505 triggers production of a salicylic acid analogue in the fungal pathogen Heterobasidion abietinum that enhances infection of Norway spruce seedlings. Antonie van Leeuwenhoek Int. J. Gen. Mol. Microbiol. 2018, 111, 691–704.Varma, A.; Verma, S.; Sudha; Sahay, N.; Bütehorn, B.; Franken, P. Piriformospora indica, a cultivable plant-growth-promoting root endophyte. Appl. Environ. Microbiol. 1999, 65, 2741–2744.Franken, P. The plant strengthening root endophyte Piriformospora indica: Potential application and the biology behind. Appl. Microbiol. Biotechnol. 2012, 96, 1455–1464.Gill, S.S.; Gill, R.; Trivedi, D.K.; Anjum, N.A.; Sharma, K.K.; Ansari, M.W.; Ansari, A.A.; Johri, A.K.; Prasad, R.; Pereira, E.; et al. Piriformospora indica: Potential and significance in plant stress tolerance. Front. Microbiol. 2016, 7, 1–20.Pham, G.H.; Singh, A.; Malla, R.; Kumari, R.; Prasad, R.; Sachdev, M.; Rexer, K.H.; Kost, G.; Luis, P.; Kaldorf, M.; et al. Interaction of Piriformospora indica with diverse microorganisms and plants. In Plant Surface Microbiology; Springer: Berlin/Heidelberg, Germany, 2008; pp. 237–265. ISBN 9783540740506.Bonfante, P.; Genre, A. Mechanisms underlying beneficial plant–fungus interactions in mycorrhizal symbiosis. Nat. Commun. 2010, 1, 48.Wang, W.; Shi, J.; Xie, Q.; Jiang, Y.; Yu, N.; Wang, E. Nutrient exchange and regulation in arbuscular mycorrhizal symbiosis. Mol. Plant 2017, 10, 1147–1158.Johansson, J.F.; Paul, L.R.; Finlay, R.D. Microbial interactions in the mycorrhizosphere and their significance for sustainable agriculture. FEMS Microbiol. Ecol. 2004, 48, 1–13.Kumar Bhuyan, S.; Bandyopadhyay, P.; Kumar, P.; Kumar Mishra, D.; Prasad, R.; Kumari, A.; Chandra Upadhyaya, K.; Varma, A.; Kumar Yadava, P. Interaction of Piriformospora indica with Azotobacter chroococcum. Sci. Rep. 2015, 5, 1–13.Bhattacharyya, P.N.; Jha, D.K. Plant growth-promoting rhizobacteria (PGPR): Emergence in agriculture. World J. Microbiol. Biotechnol. 2012, 28, 1327–1350.Shishehbor, M.; Madani, H.; Ardakani, M.R. Effect of vermicompost and biofertilizers on yield and yield components of common millet (Panicum miliaceum). Ann. Biol. Res. 2013, 4, 174–180.Vafadar, F.; Amooaghaie, R.; Otroshy, M. Effects of plant-growth-promoting rhizobacteria and arbuscular mycorrhizal fungus on plant growth, stevioside, NPK, and chlorophyll content of Stevia rebaudiana. J. Plant Interact. 2014, 9, 128–136.Sharma, S.D.; Sharma, N.C.; Sharma, C.L.; Kumar, P.; Chandel, A. Glomus-Azotobacter symbiosis in apple under reduced inorganic nutrient fertilization for sustainable and economic orcharding enterprise. Sci. Hortic. (Amsterdam) 2012, 146, 175–181.Arora, M.; Saxena, P.; Choudhary, D.K.; Abdin, M.Z.; Varma, A. Dual symbiosis between Piriformospora indica and Azotobacter chroococcum enhances the artemisinin content in Artemisia annua L. World J. Microbiol. Biotechnol. 2016, 32, 19.Maheshwari, D.K.; Dubey, R.C.; Aeron, A.; Kumar, B.; Kumar, S.; Tewari, S.; Arora, N.K. Integrated approach for disease management and growth enhancement of Sesamum indicum L. utilizing Azotobacter chroococcum TRA2 and chemical fertilizer. World J. Microbiol. Biotechnol. 2012, 28, 3015–3024.Schrey, S.D.; Salo, V.; Raudaskoski, M.; Hampp, R.; Nehls, U.; Tarkka, M.T. Interaction with mycorrhiza helper bacterium Streptomyces sp. AcH 505 modifies organisation of actin cytoskeleton in the ectomycorrhizal fungus Amanita muscaria (fly agaric). Curr. Genet. 2007, 52, 77–85.Walther, A.; Wendland, J. Apical localization of actin patches and vacuolar dynamics in Ashbya gossypii depend on the WASP homologWal1p. J. Cell Sci. 2004, 117, 4947–4958.Jones, S.E.; Elliot, M.A. Streptomyces Exploration: Competition, volatile communication and new bacterial behaviours. Trends Microbiol. 2017, 25, 522–531.Tyc, O.; Song, C.; Dickschat, J.S.; Vos, M.; Garbeva, P. The ecological role of volatile and soluble secondary metabolites produced by soil bacteria. Trends Microbiol. 2017, 25, 280–292.Adams, A.S.; Currie, C.R.; Cardoza, Y.; Klepzig, K.D.; Ra a, K.F. Effects of symbiotic bacteria and tree chemistry on the growth and reproduction of bark beetle fungal symbionts. Can. J. For. Res. 2009, 39, 1133–1147.Rainey, P.B. Effect of Pseudomonas putida on hyphal growth of Agaricus bisporus. Mycol. Res. 1991, 95, 699–704.Schrey, S.D.; Schellhammer, M.; Ecke, M.; Hampp, R.; Tarkka, M.T. Mycorrhiza helper bacterium Streptomyces AcH 505 induces differential gene expression in the ectomycorrhizal fungus Amanita muscaria. New Phytol. 2005, 168, 205–216.Becker, D.M.; Bagley, S.T.; Podila, G.K. Effects of mycorrhizal-associated Streptomycetes on growth of Laccaria bicolor, Cenococcum geophilum, and Armillaria species and on gene expression in Laccaria bicolor. Mycologia 1999, 91, 33.Martin, F.; Ramstedt, M.; Söderhäll, K.; Canet, D. Carbohydrate and amino acid metabolism in the ectomycorrhizal ascomycete Sphaerosporella brunnea during glucose utilization: A 13C NMR Study. Plant Physiol. 1988, 86, 935–940.Breuninger, M.; Trujillo, C.G.; Serrano, E.; Fischer, R.; Requena, N. Different nitrogen sources modulate activity but not expression of glutamine synthetase in arbuscular mycorrhizal fungi. Fungal Genet. Biol. 2004, 41, 542–552.Márquez, A.J.; Betti, M.; Ottonello, S.; Bonfante, P.; Montanini, B.; Balestrini, R. Distinctive properties and expression profiles of glutamine synthetase from a plant symbiotic fungus. Biochem. J. 2003, 373, 357–368.Botton, B.; Chalot, M.; Garnier, A.; Martin, F. L’assimilation de l’azote minéral chez les ectomycorhizes. Acta Bot. Gall. 1994, 141, 469–481.Martin, F.; Canet, D. Biosynthesis of amino acids during [13C]glucose utilization by the ectomycorrhizal ascomycete Cenococciiin geophiluin monitored by 13C nuclear magnetic resonance. Physiol Vég 1986, 24, 209–218.Ceccaroli, P.; Saltarelli, R.; Cesari, P.; Pierleoni, R.; Sacconi, C.; Vallorani, L.; Rubini, P.; Stocchi, V.; Martin, F. Carbohydrate and amino acid metabolism in Tuber borchii mycelium during glucose utilization: A 13C NMR study. Fungal Genet. Biol. 2003, 39, 168–175.Kim, J.K.; Mulrooney, S.B.; Hausinger, R.P. The UreEF fusion protein provides a soluble and functional form of the UreF urease accessory protein. J. Bacteriol. 2006, 188, 8413–8420.Fichman, Y.; Gerdes, S.Y.; Kovács, H.; Szabados, L.; Zilberstein, A.; Csonka, L.N. Evolution of proline biosynthesis: Enzymology, bioinformatics, genetics, and transcriptional regulation. Biol. Rev. 2015, 90, 1065–1099.Ahmad, I.; Carleton, T.; Malloch, D.; Hellebust, J. Nitrogen metabolism in the ectomycorrhizal fungus Laccaria bicolor (R. Mre.) Orton. New Phytol. 1990, 116, 431–441.Pati, B.R.; Sengupta, S.; Chandra, A.K. Studies on the amino acids released by phyllosphere diazotrophic bacteria. Microbiol. Res. 1994, 149, 287–290.Thuler, D.S.; Floh, E.I.S.; Handro,W.; Barbosa, H.R. Beijerinckia derxii releases plant growth regulators and amino acids in synthetic media independent of nitrogenase activity. J. Appl. Microbiol. 2003, 95, 799–806.Pócsi, I.; Prade, R.A.; Penninckx, M.J. Glutathione, altruistic metabolite in fungi. In Advances in Microbial Physiology; Academic Press: Cambridge, MA, USA, 2004; Volume 49, pp. 1–76. ISBN 0120277492.Ono, B.; Shirahige, Y.; Nanjoh, A.; Andou, N.; Ohue, H.; Ishino-Arao, Y. Cysteine biosynthesis in Saccharomyces cerevisiae: Mutation that confers cystathionine beta-synthase deficiency. J. Bacteriol. 1988, 170, 5883–5889.Savin, M.A.; Flavin, M. Cystationine synthesis in yeast: An alternative pathway for homocysteine biosynthesis. J. Bacteriol. 1972, 112, 299–303.Riedlinger, J. Die stoffichen Grundlagen der Modulation des Myzelwachstums von symbiotischen und pathogenen Pilzen durch Streptomyceten; Eberhard-Karls University of Tübingen: Tübingen, Germany, 2006.Ogita, A.; Matsumoto, K.; Fujita, K.; Usuki, Y.; Hatanaka, Y.; Tanaka, T. Synergistic fungicidal activities of amphotericin B andN-methyl-N”-dodecylguanidine: Aconstituent of polyol macrolide antibiotic niphimycin. J. Antibiot. (Tokyo) 2007, 60, 27–35.Käfer, E. Meiotic and mitotic recombination in Aspergillus and its chromosomal aberrations. Adv. Genet. 1977, 19, 33–131.Pilot, G.; Stransky, H.; Bushey, D.F.; Pratelli, R.; Ludewig, U.;Wingate, V.P.; Frommer,W.B. Overexpression of GLUTAMINE DUMPER1 leads to hypersecretion of glutamine from hydathodes of Arabidopsis leaves. Plant Cell 2004, 16, 1827–1840.ORIGINALPDF.pdfPDF.pdfPDFapplication/pdf3520442https://bonga.unisimon.edu.co/bitstreams/60bdc0cc-46db-4b21-b069-6c5bcda9fa8d/download18fb80cc673c7d06703b8d7277d4de56MD51CC-LICENSElicense_rdflicense_rdfapplication/rdf+xml; charset=utf-8805https://bonga.unisimon.edu.co/bitstreams/92ec7bf6-a727-4076-a27e-396275cebd6c/download4460e5956bc1d1639be9ae6146a50347MD52LICENSElicense.txtlicense.txttext/plain; charset=utf-8381https://bonga.unisimon.edu.co/bitstreams/f1aef860-fdde-4616-ae06-daedae51c28c/download733bec43a0bf5ade4d97db708e29b185MD53TEXTInteraction_With_Soil_Bacteria_Affects_Growth.pdf.txtInteraction_With_Soil_Bacteria_Affects_Growth.pdf.txtExtracted texttext/plain52984https://bonga.unisimon.edu.co/bitstreams/8af0133a-24a9-4eca-a272-4610173ae32f/download0744776ab86b707c17556ce13947e5a3MD54PDF.pdf.txtPDF.pdf.txtExtracted texttext/plain56506https://bonga.unisimon.edu.co/bitstreams/67e4e9f8-d322-4620-bc87-ca25c2f822d4/downloadebcaff34dd16702a07af44c104ec5466MD56THUMBNAILInteraction_With_Soil_Bacteria_Affects_Growth.pdf.jpgInteraction_With_Soil_Bacteria_Affects_Growth.pdf.jpgGenerated Thumbnailimage/jpeg1603https://bonga.unisimon.edu.co/bitstreams/1041181b-b1b0-4217-a0d5-3426b6c37da7/download116c3f3c8a6152eefdb909fb439e6b18MD55PDF.pdf.jpgPDF.pdf.jpgGenerated Thumbnailimage/jpeg5409https://bonga.unisimon.edu.co/bitstreams/9abdd51c-8463-4f4d-b07b-85122866d325/download4def70d227e3ef3fb66580373ed1bb32MD5720.500.12442/4715oai:bonga.unisimon.edu.co:20.500.12442/47152024-08-14 21:51:53.972http://creativecommons.org/licenses/by-nc-nd/4.0/Attribution-NonCommercial-NoDerivatives 4.0 Internacionalopen.accesshttps://bonga.unisimon.edu.coRepositorio Digital Universidad Simón Bolívarrepositorio.digital@unisimon.edu.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