Abstract
Plant growth promoting microorganisms (PGPMs) of the plant root zone microbiome have received limited attention in hydroponic cultivation systems. In the framework of a project aimed at the development of a biological life support system for manned missions in space, we investigated the effects of PGPMs on four common food crops (durum and bread wheat, potato and soybean) cultivated in recirculating hydroponic systems for a whole life cycle. Each crop was inoculated with a commercial PGPM mixture and the composition of the microbial communities associated with their root rhizosphere, rhizoplane/endosphere and with the recirculating nutrient solution was characterised through 16S- and ITS-targeted Illumina MiSeq sequencing. PGPM addition was shown to induce changes in the composition of these communities, though these changes varied both between crops and over time. Microbial communities of PGPM-treated plants were shown to be more stable over time. Though additional development is required, this study highlights the potential benefits that PGPMs may confer to plants grown in hydroponic systems, particularly when cultivated in extreme environments such as space.
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Olympios CM (1999) Overview of soilless culture: advantages, constraints, and perspectives. In: Choukr-Allah R (ed) Protected cultivation in the Mediterranean region. CIHEAM / IAV Hassan II, Paris, pp 307–324
Lee S, Lee J (2015) Beneficial bacteria and fungi in hydroponic systems: types and characteristics of hydroponic food production methods. Sci Hortic 195:206–215. doi:10.1016/j.scienta.2015.09.011
Godia F, Fossen A, Peiro E, Gerbi O, Dussap G, Leys N, Arnau C, Milian E (2014) MELiSSA Pilot Plant: a facility for ground demonstration of a closed life support system. 40th COSPAR Scientific Assembly, Moscow, Russia
Paradiso R, De Micco V, Buonomo R, Aronne G, Barbieri G, De Pascale S (2014) Soilless cultivation of soybean for Bioregenerative Life-Support Systems: a literature review and the experience of the MELiSSA Project – food characterisation phase I. Plant Biol 16:69–78. doi:10.1111/plb.12056
De Micco V, Buonomo R, Paradiso R, De Pascale S, Aronne G (2012) Soybean cultivar selection for Bioregenerative Life Support Systems (BLSS) – theoretical selection. Adv Space Res 49:1415–1421. doi:10.1016/j.asr.2012.02.022
Vessey JK (2003) Plant growth promoting rhizobacteria as biofertilizers. Plant Soil 255:571–586. doi:10.1023/a:1026037216893
Calvo P, Nelson L, Kloepper JW (2014) Agricultural uses of plant biostimulants. Plant Soil 383:3–41. doi:10.1007/s11104-014-2131-8
Dasgan HY, Aydoner G, Akyol M (2012) Use of some microorganisms as bio-fertilizers in soilless grown squash for saving chemical nutrients. International Society for Horticultural Science (ISHS), Leuven, pp 155–162
Rouphael Y, Franken P, Schneider C, Schwarz D, Giovannetti M, Agnolucci M, Pascale SD, Bonini P, Colla G (2015) Arbuscular mycorrhizal fungi act as biostimulants in horticultural crops. Sci Hortic 196:91–108. doi:10.1016/j.scienta.2015.09.002
Ruzzi M, Aroca R (2015) Plant growth-promoting rhizobacteria act as biostimulants in horticulture. Sci Hortic 196:124–134. doi:10.1016/j.scienta.2015.08.042
Stewart-Wade S (2011) Plant pathogens in recycled irrigation water in commercial plant nurseries and greenhouses: their detection and management. Irrigation Sci 29:267–297. doi:10.1007/s00271-011-0285-1
Settanni L, Miceli A, Francesca N, Cruciata M, Moschetti G (2013) Microbiological investigation of Raphanus sativus L. grown hydroponically in nutrient solutions contaminated with spoilage and pathogenic bacteria. Int J Food Microbiol 160:344–352
Compant S, Duffy B, Nowak J, Clément C, Barka EA (2005) Use of plant growth-promoting bacteria for biocontrol of plant diseases: principles, mechanisms of action, and future prospects. Appl Environ Microbiol 71:4951–4959. doi:10.1128/aem.71.9.4951-4959.2005
Owen D, Williams AP, Griffith GW, Withers PJA (2015) Use of commercial bio-inoculants to increase agricultural production through improved phosphorus acquisition. Appl Soil Ecol 86:41–54. doi:10.1016/j.apsoil.2014.09.012
Houlden A, Timms-Wilson TM, Day MJ, Bailey MJ (2008) Influence of plant developmental stage on microbial community structure and activity in the rhizosphere of three field crops. FEMS Microbiol Ecol 65:193–201. doi:10.1111/j.1574-6941.2008.00535.x
Clegg CD (2006) Impact of cattle grazing and inorganic fertiliser additions to managed grasslands on the microbial community composition of soils. Appl Soil Ecol 31:73–82. doi:10.1016/j.apsoil.2005.04.003
Dunfield KE, Germida JJ (2003) Seasonal changes in the rhizosphere microbial communities associated with field-grown genetically modified canola (Brassica napus). Appl Environ Microbiol 69:7310–7318. doi:10.1128/aem.69.12.7310-7318.2003
Chaparro JM, Badri DV, Vivanco JM (2014) Rhizosphere microbiome assemblage is affected by plant development. ISME J 8:790–803. doi:10.1038/ismej.2013.196
O’Neill TM, Deery SJ, Scott G, Dickinson M (2014) Monitoring tomato root microorgansisms. International Society for Horticultural Science (ISHS), Leuven, pp 81–88
Garland JL, Levine LH, Yorio NC, Adams JL, Cook KL (2000) Graywater processing in recirculating hydroponic systems: phytotoxicity, surfactant degradation, and bacterial dynamics. Water Res 34:3075–3086. doi:10.1016/S0043-1354(00)00085-3
Cirou A, Mondy S, An S, Charrier A, Sarrazin A, Thoison O, DuBow M, Faure D (2012) Efficient biostimulation of native and introduced quorum-quenching rhodococcus erythropolis populations is revealed by a combination of analytical chemistry, microbiology, and pyrosequencing. Appl Environ Microbiol 78:481–492. doi:10.1128/aem.06159-11
Molina LG, Cordenonsi da Fonseca G, Morais GLD, de Oliveira LFV, Carvalho JB, Kulcheski FR, Margis R (2012) Metatranscriptomic analysis of small RNAs present in soybean deep sequencing libraries. Genet Mol Biol 35:292–303
Ding J, Zhang Y, Zhang H, Li X, Sun Z, Liao Y, Xia X, Zhou Y, Shi K, Yu J (2014) Effects of Fusarium oxysporum on rhizosphere microbial communities of two cucumber genotypes with contrasting Fusarium wilt resistance under hydroponic condition. Eur J Plant Pathol 140:643–653. doi:10.1007/s10658-014-0494-6
Degnan PH, Ochman H (2012) Illumina-based analysis of microbial community diversity. ISME J 6:183–194, http://www.nature.com/ismej/journal/v6/n1/suppinfo/ismej201174s1.html
Stasiak M, Gidzinski D, Jordan M, Dixon M (2012) Crop selection for advanced life support systems in the ESA MELiSSA program: durum wheat (Triticum turgidum var durum). Adv Space Res 49:1684–1690. doi:10.1016/j.asr.2012.03.001
Moore G, Griffith C, Peters A (2000) Bactericidal properties of ozone and its potential application as a terminal disinfectant. J Food Prot 63:1100–1106
Hoagland D, Arnon D (1950) The water-culture method for growing plants without soil. California Agri Experiment Stat 347:32
Paradiso R, Buonomo R, De Micco V, Aronne G, Palermo M, Barbieri G, De Pascale S (2012) Soybean cultivar selection for Bioregenerative Life Support Systems (BLSSs) – Hydroponic cultivation. Adv Space Res 50:1501–1511. doi:10.1016/j.asr.2012.07.025
Dougher TAO, Bugbee B (1997) Effect of lamp type and temperature on development, carbon partitioning and yield of soybean. Adv Space Res 20:1895–1899. doi:10.1016/S0273-1177(97)00857-0
Wheeler RM, Mackowiak CL, Stutte GW, Sager JC, Yorio NC, Ruffe LM, Fortson RE, Dreschel TW, Knott WM, Corey KA (1996) NASA’s biomass production chamber: a testbed for bioregenerative life support studies. Adv Space Res 18:215–224. doi:10.1016/0273-1177(95)00880-N
Wheeler RM, Mackowiak CL, Stutte GW, Yorio NC, Ruffe LM, Sager JC, Prince RP, Knott WM (2008) Crop productivities and radiation use efficiencies for bioregenerative life support. Adv Space Res 41:706–713. doi:10.1016/j.asr.2007.06.059
Colla G, Rouphael Y, Cardarelli M, Tullio M, Rivera C, Rea E (2008) Alleviation of salt stress by arbuscular mycorrhizal in zucchini plants grown at low and high phosphorus concentration. Biol Fertility Soils 44:501–509. doi:10.1007/s00374-007-0232-8
Bashan Y (1986) Significance of timing and level of inoculation with rhizosphere bacteria on wheat plants. Soil Biol Biochem 18:297–301. doi:10.1016/0038-0717(86)90064-7
Fernandez-Orozco R, Frias J, Zielinski H, Piskula MK, Kozlowska H, Vidal-Valverde C (2008) Kinetic study of the antioxidant compounds and antioxidant capacity during germination of Vigna radiata cv. emmerald, Glycine max cv. jutro and Glycine max cv. merit. Food Chem 111:622–630. doi:10.1016/j.foodchem.2008.04.028
Gbikpi PJ, Crookson RK (1981) A whole-plant indicator of soybean physiological maturity. Crop Sci 21:469–472. doi:10.2135/cropsci1981.0011183X002100030030x
Barillot CD, Sarde C-O, Bert V, Tarnaud E, Cochet N (2013) A standardized method for the sampling of rhizosphere and rhizoplan soil bacteria associated to a herbaceous root system. Ann Microbiol 63:471–476. doi:10.1007/s13213-012-0491-y
Paszkowski U, Gutjahr C (2013) Multiple control levels of root system remodeling in arbuscular mycorrhizal symbiosis. Front Plant Sci 4
Klindworth A, Pruesse E, Schweer T, Peplies J, Quast C, Horn M, Glöckner FO (2013) Evaluation of general 16S ribosomal RNA gene PCR primers for classical and next-generation sequencing-based diversity studies. Nucleic Acids Res 41(1):e1.doi:10.1093/nar/gks808
Toju H, Tanabe AS, Yamamoto S, Sato H (2012) High-coverage ITS Primers for the DNA-based identification of ascomycetes and basidiomycetes in environmental samples. PLoS ONE 7:e40863. doi:10.1371/journal.pone.0040863
Robideau GP, De Cock AWAM, Coffey MD, Voglmayr H, Brouwer H, Bala K, Chitty DW, Désaulniers N, Eggertson QA, Gachon CMM, Hu C-H, KKüpper FC, Rintoul TL, Sarhan E, Verstappen ECP, Zhang Y, Bonants PJM, Ristaino JB, Lévesque CA (2011) DNA barcoding of oomycetes with cytochrome c oxidase subunit I and internal transcribed spacer. Mol Ecol Resour 11(6):1002–1011
Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Peña AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Turnbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336. doi:10.1038/nmeth.f.303
Camarinha-Silva A, Jáuregui R, Chaves-Moreno D, Oxley APA, Schaumburg F, Becker K, Wos-Oxley ML, Pieper DH (2014) Comparing the anterior nare bacterial community of two discrete human populations using Illumina amplicon sequencing. Environ Microbiol 16:2939–2952. doi:10.1111/1462-2920.12362
Magoč T, Salzberg SL (2011) FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27:2957–2963. doi:10.1093/bioinformatics/btr507
Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26:2460–2461. doi:10.1093/bioinformatics/btq461
Wickham H (2009) ggplot2: elegant graphics for data analysis. Springer, New York
Core Team R (2015) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna
Sumayo M, Hahm M-S, Ghim S-Y (2013) Determinants of plant growth-promoting Ochrobactrum lupini KUDC1013 involved in induction of systemic resistance against Pectobacterium carotovorum subsp. carotovorum in Tobacco Leaves. Plant Pathol J 29:174–181. doi:10.5423/ppj.si.09.2012.0143
Xiao C, Chi R, He H, Qiu G, Wang D, Zhang W (2009) Isolation of phosphate-solubilizing fungi from phosphate mines and their effect on wheat seedling growth. Appl Biochem Biotechnol 159:330–342. doi:10.1007/s12010-009-8590-3
Choudhary DK, Johri BN (2009) Interactions of Bacillus spp. and plants – with special reference to induced systemic resistance (ISR). Microbiol Res 164:493–513. doi:10.1016/j.micres.2008.08.007
Albareda M, Dardanelli MS, Sousa C, Megías M, Temprano F, Rodríguez-Navarro DN (2006) Factors affecting the attachment of rhizospheric bacteria to bean and soybean roots. FEMS Microbiol Lett 259:67–73. doi:10.1111/j.1574-6968.2006.00244.x
Benizri E, Baudoin E, Guckert A (2001) Root colonization by inoculated plant growth-promoting rhizobacteria. Biocontrol Sci Technol 11:557–574. doi:10.1080/09583150120076120
Martínez OA, Jorquera MA, Crowley DE, Luz Mora M (2011) Influence of nitrogen fertilisation on pasture culturable rhizobacteria occurrence and the role of environmental factors on their potential PGPR activities. Biol Fertil Soils 47:875–885. doi:10.1007/s00374-011-0593-x
Compant S, Clément C, 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
Rodríguez-Navarro DN, Dardanelli MS, Ruíz-Saínz JE (2007) Attachment of bacteria to the roots of higher plants. FEMS Microbiol Lett 272:127–136. doi:10.1111/j.1574-6968.2007.00761.x
Rattray E, Tyrrell J, Prosser J, Glover L, Killham K (1993) Effect of soil bulk density and temperature on wheat rhizosphere colonisation by lux-marked Pseudomonas fluorescens. Eur J Soil Biol 29:73–82
Beauchamp C, Kloepper J, Antoun H (1993) Detection of genetically engineered bioluminescent pseudomonads in potato rhizosphere at different temperatures. Microb Rel 1:203–207
Dimitrieva GY, Crawford RL, Yüksel GÜ (2006) The nature of plant growth-promoting effects of a pseudoalteromonad associated with the marine algae Laminaria japonica and linked to catalase excretion. J Appl Microbiol 100:1159–1169. doi:10.1111/j.1365-2672.2006.02831.x
Franks A, Egan S, Holmström C, James S, Lappin-Scott H, Kjelleberg S (2006) Inhibition of fungal colonization by Pseudoalteromonas tunicata provides a competitive advantage during surface colonization. Appl Environ Microbiol 72:6079–6087. doi:10.1128/aem.00559-06
Rao D, Webb JS, Kjelleberg S (2005) Competitive interactions in mixed-species biofilms containing the marine bacterium Pseudoalteromonas tunicata. Appl Environ Microbiol 71:1729–1736. doi:10.1128/aem.71.4.1729-1736.2005
Folman LB, Postma J, Veen JA (2001) Ecophysiological characterization of rhizosphere bacterialcommunities at different root locations and plant developmental stages of cucumber grown on rockwool. Microb Ecol 42:586–597. doi:10.1007/s00248-001-0032-x
Ross KA, Feazel LM, Robertson CE, Fathepure BZ, Wright KE, Turk-MacLeod RM, Chan MM, Held NL, Spear JR, Pace NR (2012) Phototrophic phylotypes dominate mesothermal microbial mats associated with hot springs in Yellowstone National Park. Microb Ecol 64:162–170. doi:10.1007/s00248-012-0012-3
Köhler T, Dietrich C, Scheffrahn RH, Brune A (2012) High-resolution analysis of gut environment and bacterial microbiota reveals functional compartmentation of the gut in wood-feeding higher termites (Nasutitermes spp.). Appl Environ Microbiol 78:4691–4701. doi:10.1128/aem.00683-12
Doornbos RF, van Loon LC, Bakker PAHM (2012) Impact of root exudates and plant defense signaling on bacterial communities in the rhizosphere. a review. Agron Sustain Dev 32:227–243. doi:10.1007/s13593-011-0028-y
Biate D, Kumari A, Annapurna K, Kumar L, Ramadoss D, Reddy K, Naik S (2015) Legume root exudates: their role in symbiotic interactions. In: Arora NK (ed) Plant microbes symbiosis: applied facets. Springer, India, pp 259–271
Bais HP, Weir TL, Perry LG, Gilroy S, Vivanco JM (2006) The role of root exudates in rhizosphere interactions with plants and other organsisms. Annu Rev Plant Biol 57:233–266. doi:10.1146/annurev.arplant.57.032905.105159
Hartmann A, Schmid M, Tuinen D, Berg G (2008) Plant-driven selection of microbes. Plant Soil 321:235–257. doi:10.1007/s11104-008-9814-y
De-la-Peña C, Badri DV, Lei Z, Watson BS, Brandão MM, Silva-Filho MC, Sumner LW, Vivanco JM (2010) Root secretion of defense-related proteins is development-dependent and correlated with flowering time. J Biol Chem 285:30654–30665. doi:10.1074/jbc.M110.119040
Micallef SA, Channer S, Shiaris MP, Colón-Carmona A (2009) Plant age and genotype impact the progression of bacterial community succession in the Arabidopsis rhizosphere. Plant Signal Behav 4:777–780. doi:10.4161/psb.4.8.9229
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This research was supported by the MELiSSA project from the European Space Agency under contract no. 400010819/13/NL/JC.
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Fig. S1
Rarefaction curves (±SD) representing the number of OTUs discovered in control (red) and inoculated (blue) durum wheat, and control (yellow) and inoculated (green) soybean. (GIF 189 kb)
Fig. S2
Rarefaction curves (±SD) representing the number of OTUs discovered in control (red) and inoculated (blue) bread wheat, control (green) and inoculated (purple) soybean, and in the Myco Madness PGPM mix (yellow). (GIF 176 kb)
Fig. S3
PCoA analysis showing Bray-Curtis similarity values of evenly sub-sampled bread wheat- (A), durum wheat- (B), potato- (C) and soybean- associated (D) communities. NS_treat= nutrient solution samples treated with Myco Madness, NS_con= control nutrient solution samples, En_Con= control endosphere/rhizoplane samples, En_Treat= endosphere/rhizoplane samples from Myco Madness-treated plants, Ex_Con= control rhizosphere samples, Ex_Treat= rhizosphere samples from Myco Madness-treated plants. (GIF 52 kb)
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Sheridan, C., Depuydt, P., De Ro, M. et al. Microbial Community Dynamics and Response to Plant Growth-Promoting Microorganisms in the Rhizosphere of Four Common Food Crops Cultivated in Hydroponics. Microb Ecol 73, 378–393 (2017). https://doi.org/10.1007/s00248-016-0855-0
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DOI: https://doi.org/10.1007/s00248-016-0855-0