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Assessment of the potential role of Streptomyces strains in the revegetation of semiarid sites: the relative incidence of strain origin and plantation site on plant performance and soil quality indicators

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Abstract

We performed a field assay to assess the efficacy of strains of actinobacteria belonging to the Streptomyces genus, isolated from two Mediterranean semiarid sites (Rellano and Calblanque) with different soil characteristics, with regard to the establishment of Rhamnus lycioides L. seedlings in both locations, as well as their effect on soil chemical and microbiological properties 1 year after planting. At the Calblanque site, the inoculation with native strains was more effective than that with allochthonous strains, with respect to increasing shoot dry weight (about 48 and 28 %, respectively, compared to control plants), primarily due to improvements in NPK uptake and plant drought tolerance. However, at Rellano, the efficacy of plant growth promotion was not influenced by the strain origin. The highest increases in the urease, protease, and dehydrogenase activities and in microbial biomass C in response to inoculation with actinobacteria occurred at the Rellano site (about 200, 28, 29, and 30 %, respectively, compared to the respective controls), regardless of the origin of the strain assayed. Strain origin and the biological fertility of the plantation site should be considered in the selection of strains of actinobacteria for use in the revegetation with shrub species in semiarid environments.

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References

  • Abd-Alla MH (1994) Phosphatases and the utilization of organic phosphorus by Rhizobium leguminosarum biovar viceae. Lett Appl Microbiol 18:294–296

    Article  CAS  Google Scholar 

  • Adesemoye AO, Kloepper JW (2009) Plant-microbes interactions in enhanced fertilizer-use efficiency. Appl Microbiol Biotechnol 85:1–12

    Article  PubMed  CAS  Google Scholar 

  • Alegre J, Alonso-Blázquez N, de Andrés EF, Tenorio JL, Ayerbe L (2004) Revegetation and reclamation of soils using wild leguminous shrubs in cold semiarid Mediterranean conditions: litterfall and carbon and nitrogen returns under two aridity regimes. Plant Soil 263:203–2012

    Article  CAS  Google Scholar 

  • Alguacil MM, Caravaca F, Roldán A (2005) Changes in rhizosphere microbial activity mediated by native or allochthonous AM fungi in the reafforestation of a Mediterranean degraded environment. Biol Fertil Soils 41:59–68

    Article  Google Scholar 

  • Alguacil MM, Torres MP, Torrecillas E, Díaz G, Roldán A (2011) Plant type differently promote the arbuscular mycorrhizal fungi biodiversity in the rhizosphere after revegetation of a degraded, semiarid land. Soil Biol Biochem 43:167–173

    Article  CAS  Google Scholar 

  • Anderson JPE, Domsch KH (1978) A physiological method for the quantitative measurement of microbial biomass in soils. Soil Biol Biochem 10:215–221

    Article  CAS  Google Scholar 

  • Antoun H, Kloepper JW (2001) Plant growth-promoting rhizobacteria (PGPR). In: Brenner S, Miller JH (eds) Encyclopedia of genetics. Academic, New York, pp 1477–1480

    Chapter  Google Scholar 

  • Armada E, Roldán A, Azcón R (2014) Differential activity of autochthonous bacteria in controlling drought stress in native Lavandula and Salvia plant species under drought conditions in natural arid soil. Micro Ecol 67:410–420

    Article  CAS  Google Scholar 

  • Bashan Y, Salazar BG, Moreno M, López BR, Linderman RG (2012) Restoration of eroded soil in the Sonoran Desert with native leguminous trees using plant growth-promoting microorganisms and limited amounts of compost and water. J Environ Manag 102:26–36

    Article  CAS  Google Scholar 

  • Bashan Y, Kamnev AA, de-Bashan LE (2013) Tricalcium phosphate is inappropriate as universal selection factor for isolating and testing phosphate-solubilizing bacteria that enhance plant growth: a proposal for an alternative procedure. Biol Fertil Soils 49:465–479

    Article  CAS  Google Scholar 

  • Bashan A, de-Bashan LE, Prabhu SR, Hernandez JP (2014) Advances in plant growth-promoting bacterial inoculant technology: formulations and practical perspectives (1998–2013). Plant Soil 378:1–33

    Article  CAS  Google Scholar 

  • Benabdellah K, Abbas Y, Abourouh M, Aroca R, Azcón R (2011) Influence of two bacterial isolates from degraded and non-degraded soils and arbuscular mycorrhizae fungi isolated from semi-arid zone on the growth of Trifolium repens under drought conditions: mechanisms related to bacterial effectiveness. Eur J Soil Biol 47:303–309

    Article  Google Scholar 

  • Brink RHJ, Dubach P, Lynch DL (1960) Measurement of carbohydrates in soil hydrolyzates with anthrone. Soil Sci 89:157–166

    Article  CAS  Google Scholar 

  • Caravaca F, Barea JM, Figueroa D, Roldán A (2002) Assessing the effectiveness of mycorrhizal inoculation and soil compost addition for reafforestation with Olea europaea subsp. sylvestris through changes in soil biological and physical parameters. Appl Soil Ecol 20:107–118

    Article  Google Scholar 

  • Caravaca F, Barea JM, Palenzuela J, Figueroa D, Alguacil MM, Roldán A (2003) Establishment of shrub species in a degraded semiarid site after inoculation with native or allochthonous arbuscular mycorrhizal fungi. Appl Soil Ecol 22:103–111

    Article  Google Scholar 

  • Caravaca F, Alguacil MM, Azcón R, Parladé J, Torres P, Roldán A (2005a) Establishment of two ectomycorrhizal shrub species in a semiarid site after in situ amendment with sugar beet, rock phosphate, and Aspergillus niger. Microb Ecol 49:73–82

    Article  PubMed  CAS  Google Scholar 

  • Caravaca F, Alguacil MM, Barea JM, Roldán A (2005b) Survival of inocula and native AM fungi species associated with shrubs in a degraded Mediterranean ecosystem. Soil Biol Biochem 37:227–233

    Article  CAS  Google Scholar 

  • Conn VM, Franco CMM (2004) Effect of microbial inoculants on the indigenous actinobacterial endophyte population in the roots of wheat as determined by terminal restriction fragment length polymorphism. Appl Environ Microbiol 70:6407–6413

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • de-Bashan LE, Hernandez JP, Bashan Y (2012) The potential contribution of plant growth-promoting bacteria to reduce environmental degradation—a comprehensive evaluation. Appl Soil Ecol 61:171–189

    Article  Google Scholar 

  • De Vasconcellos RLF, Cardoso EJBN (2009) Rhizospheric streptomycetes as potential biocontrol agents of Fusarium and Armillaria pine rot and as PGPRf or Pinus taeda. BioControl 54:807–816

    Article  Google Scholar 

  • Downs MR, Nadelhoffer KJ, Melillo JM, Aber JD (1993) Foliar and fine root nitrate reductase activity in seedlings of four forest tree species in relation to nitrogen availability. Trees 7:233–236

    Article  Google Scholar 

  • Fernández C, Alonso C, Babín MM, Pro J, Carbonell G, Tarazona JV (2004) Ecotoxicological assessment of doxycycline in aged pig manure using multispecies soil systems. Sci Total Environ 323:63–69

    Article  PubMed  CAS  Google Scholar 

  • Franco-Correa M, Quintana A, Duque C, Suarez C, Rodríguez MX, Barea J (2010) Evaluation of actinomycete strains for key traits related with plant growth promotion and mycorrhiza helping activities. Appl Soil Ecol 45:209–217

    Article  Google Scholar 

  • García C, Hernández T, Costa F (1997) Potential use of dehydrogenase activity as an index of microbial activity in degraded soils. Commun Soil Sci Plant Anal 28:123–134

    Article  Google Scholar 

  • Ghani AD, Dexter M, Perrott KW (2003) Hot water extractable carbon in soils: a sensitive measurement determining impacts of fertilization, grazing and cultivation. Soil Biol Biochem 35:1231–1243

    Article  CAS  Google Scholar 

  • Giovannetti M, Mosse B (1980) An evaluation of techniques for measuring vesicular–arbuscular mycorrhizal infection in roots. New Phytol 84:489–499

    Article  Google Scholar 

  • Gulías J, Traveset A (2012) Altitudinal variation in the reproductive performance of the Mediterranean shrub Rhamnus lycioides L. J Plant Ecol 5:330–336

    Article  Google Scholar 

  • Hamdali H, Hafidi M, Virolle MJ, Ouhdouch Y (2008a) Rock phosphate-solubilizing actinomycetes: screening for plant growth-promoting activities. World J Microb Biotechnol 24:2565–2575

    Article  CAS  Google Scholar 

  • Hamdali H, Hafidi M, Virolle MJ, Ouhdouch Y (2008b) Growth promotion and protection against damping-off of wheat by two rock phosphate solubilizing actinomycetes in a P-deficient soil under greenhouse conditions. Appl Soil Ecol 40:510–517

    Article  Google Scholar 

  • Hardy RWF, Holsten RD, Jackson EK, Burns RC (1968) The acetylene-ethylene assay for N2 fixation: laboratory and field evaluation. Plant Physiol 43:1185–1207

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hrynkiewicz K, Baum C (2011) The potential of rhizosphere microorganisms to promote the plant growth in disturbed soils. In: Malik A, Groham E (eds) Environmental protection strategies for sustainable development. Springer Science + Business Media BV Inc, Torun, pp 35–64

    Google Scholar 

  • Jog R, Pandya M, Nareshkumar G, Rajkumar S (2014) Mechanism of phosphate solubilization and antifungal activity of Streptomyces spp. isolated from wheat roots and rhizosphere and their application in improving plant growth. Microbiol SGM 160:778–788

    Article  CAS  Google Scholar 

  • Kim KY, Jordan D, McDonald GA (1998) Effect of phosphate-solubilizing bacteria and vesicular-arbuscular mycorrhizae on tomato growth and soil microbiota activity. Biol Fertil Soils 26:79–87

    Article  CAS  Google Scholar 

  • Lebron I, McGiffen ME Jr, Suarez DL (2012) The effect of total carbon on microscopic soil properties and implications for crop production. J Arid Land 4:251–259

    Article  Google Scholar 

  • Li X, She Y, Sun B, Song H, Zhu Y, Lv Y, Song H (2010) Purification and characterization of a cellulase-free, thermostable xylanase from Streptomyces rameus L2001 and its biobleaching effect on wheat straw pulp. Biochem Eng J 52:71–78

  • Madene A, Jacquot M, Scher J, Desobry S (2006) Flavour encapsulation and controlled release—a review. Int J Sci Tech 41:1–21

    CAS  Google Scholar 

  • Mengual C, Schoebitz M, Azcón R, Roldán A (2014) Microbial inoculants and organic amendment improves plant establishment and soil rehabilitation under semiarid conditions. J Environ Manag 134:1–7

    Article  CAS  Google Scholar 

  • Minotti G, Aust SD (1987) The requirement for iron (III) in the initiation of lipid peroxidation by iron (II) and hydrogen peroxide. J Biol Chem 262:1098–1104

    PubMed  CAS  Google Scholar 

  • Nannipieri P, Ceccanti B, Cervelli S, Matarese E (1980) Extraction of phosphatase, urease, proteases, organic-carbon, and nitrogen from soil. Soil Sci Soc Am J 44:1011–1016

    Article  CAS  Google Scholar 

  • Naseby DC, Lynch JM (1997) Rhizosphere soil enzymes as indicators of perturbations caused by enzyme substrate addition and inoculation of a genetically modified strain of Pseudomonas fluorescens on wheat seed. Soil Biol Biochem 29:1353–1362

    Article  CAS  Google Scholar 

  • Nazir R, Semenov AV, Sarigul N, van Elsas JD (2013) Bacterial community establishment in native and non-native soils and the effect of fungal colonization. Microbiol Discov. doi:10.7243/2052-6180-1-8

    Google Scholar 

  • Ortiz N, Armada E, Duque E, Roldán A, Azcón R (2014) Contribution of arbuscular mycorrhizal fungi and/or bacteria to enhancing plant drought tolerance under natural soil conditions: effectiveness of autochthonous or allochthonous strains. J Plant Physiol. doi:10.1016/j.jplph.2014.08.019

    PubMed  Google Scholar 

  • Ouahmane L, Hafidi M, Thioulouse J, Ducousso M, Kisa M, Prin Y, Galiana A, Boumezzough A, Duponnois R (2006) Improvement of Cupressus atlantica Gaussen growth by inoculation with native arbuscular mycorrhizal fungi. J Appl Microbiol 103:683–690

    Article  Google Scholar 

  • Ouahmane L, Thioulouse M, Hafidi M, Prin Y, Ducousso M, Galiana A, Plenchette C, Kisa M, Duponnois R (2007) Soil functional diversity and P solubilization from rock phosphate after inoculation with native or allochthonous arbuscular mycorrhizal fungi. For Ecol Manag 241:200–2008

    Article  Google Scholar 

  • Palacios OA, Bashan Y, de-Bashan LE (2014) Proven and potential involvement of vitamins in interactions of plants with plant growth-promoting bacteria—an overview. Biol Fertil Soils 50:415–432

    Article  CAS  Google Scholar 

  • Pereira e Silva MC, Semenov AV, van Elsas JD, Salles JF (2011) Seasonal variations in the diversity and abundance of diazotrophic communities across soils. FEMS Microbiol Ecol 77:57–68

    Article  PubMed  CAS  Google Scholar 

  • Phillips JM, Hayman DS (1970) Improved procedures for clearing roots and staining parasitic and vesicular–arbuscular mycorrhizal fungi for rapid assessment of infection. Trans Br Mycol Soc 55:158–161

    Article  Google Scholar 

  • Pili Y, Mimmo T, Tomasi N, Terzano R, Cesco S, Crecchio C (2015) Microbial interactions in the rhizosphere: beneficial influences of plant growth-promoting rhizobacteria on nutrient acquisition process. A review. Biol Fertil Soils 51:403–415

    Article  CAS  Google Scholar 

  • Porcel R, Azcón R, Ruiz-Lozano JM (2004) Evaluation of the role of genes encoding for Δ1-pyrroline-5-carboxylate synthetase (P5CS) during drought stress in arbuscular mycorrhizal Glycine max and Lactuca sativa plants. Physiol Mol Plant Pathol 65:211–221

    Article  CAS  Google Scholar 

  • Premono M, Moawad AM, Vlek PLG (1996) Effect of phosphate-solubilizing Pseudomonas putida on the growth of maize and its survival in the rhizosphere. Indones J Crop Sci 11:13–23

    Google Scholar 

  • Puente ME, Bashan Y, Li CY, Lebsky VK (2004) Microbial populations and activities in the rhizoplane of rock-weathering desert plants. I. Root colonization and weathering of igneous rocks. Plant Biol 6:629–642

    Article  PubMed  CAS  Google Scholar 

  • Roldán A, Carrasco L, Caravaca F (2006) Stability of desiccated rhizosphere soil aggregates of mycorrhizal Juniperus oxycedrus grown in a desertified soil amended with a composted organic residue. Soil Biol Biochem 38:2722–2730

    Article  CAS  Google Scholar 

  • Roldán A, García-Orenes F, Lax A (1994) An incubation experiment to determinate factors involving aggregation changes in an arid soil receiving urban refuse. Soil Biol Biochem 26:1699–1707

    Article  Google Scholar 

  • Ruiz-Lozano JM, Azcón R (1996) Mycorrhizal colonization and drought stress as factors affecting nitrate reductase activity in lettuce plants. Agric Ecosyst Environ 60:175–181

    Article  CAS  Google Scholar 

  • Schoebitz M, Mengual C, Roldán A (2014) Combined effects of clay immobilized Azospirillum brasilense and Pantoea dispersa and organic olive residue on plant performance and soil properties in the revegetation of a semiarid area. Sci Total Environ 466:67–73

    Article  PubMed  CAS  Google Scholar 

  • Schreiner RP (2007) Effects of native and nonnative arbuscular mycorrhizal fungi on growth and nutrient uptake of ‘Pinot noir’ (Vitis vinifera L.) in two soils with contrasting levels of phosphorus. Appl Soil Ecol 36:205–215

    Article  Google Scholar 

  • Shishido M, Chanway CP (1998) Forest soil community responses to plant growth-promoting rhizobacteria and spruce seedlings. Biol Fertil Soils 26:179–186

    Article  Google Scholar 

  • SSS (2010) Keys to soil taxonomy, 1st edn. USDA. Natural Resources Conservation Service, Washington

    Google Scholar 

  • Tabatabai MA (1982) Soil enzymes. In: Page AL, Miller EM, Keeney DR (eds) Methods of soil analysis. ASA and SSSA, Madison, WI, pp 501–538

  • Tabatabai MA, Bremner JM (1969) Use of p-nitrophenyl phosphate for assay of soil phosphatase activity. Soil Biol Biochem 1:301–307

    Article  CAS  Google Scholar 

  • Tarkka MT, Lehr NA, Hampp R, Schrey SD (2008) Plant behavior upon contact with streptomycetes. Plant Signal Behav 3:917–919

    Article  PubMed  PubMed Central  Google Scholar 

  • Tarkka MT, Feldhahn L, Buscot F, Wubeta T (2015) Genome sequence of the mycorrhiza helper bacterium Streptomyces sp. strain AcH 505. Genome Announc. doi:10.1128/genomeA.01386-14

    Google Scholar 

  • Trabelsi D, Mengoni A, Ammar HB, Mhamdi R (2011) Effect of on-field inoculation of Phaseolus vulgaris with rhizobia on soil bacterial communities. FEMS Microbiol Ecol 77:211–222

    Article  PubMed  CAS  Google Scholar 

  • Valdés M, Pérez NO, de los Santos Estrada P, Caballero-Mellado J, Pena-Cabriales JJ, Normand P, Hirsch AM (2005) Non-Frankia actinomycetes isolated from surface-sterilized roots of Casuarina equisetifolia fix nitrogen. Appl Environ Microbiol 71:460–466

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Vassilev N, Eichler-Lobermann B, Vassileva M (2012) Stress tolerant P solubilizing microorganisms. Appl Microbiol Biotechnol 95:851–859

    Article  PubMed  CAS  Google Scholar 

  • Vassilev N, Vassileva M, Lopez A, Martos V, Reyes A, Maksimovic I, Eichler-Löbermann B, Malusà E (2015) Unexploited potential of some biotechnological techniques for biofertilizer production and formulation. Appl Microbiol Biotechnol. doi:10.1007/s00253-015-6656-4

    PubMed  Google Scholar 

  • Zhao SJ, Xu CC, Zhou Q, Meng QW (1994) Improvements of method for measurement of malondialdehyde in plant tissue. Plant Physiol Commun 30:07–210

    Google Scholar 

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Acknowledgments

This research was supported by “Plan Nacional” Spain (project numbers AGL2012-39057-CO2-01). C. Mengual was supported by the “Formación de Personal Investigador” programme (Ministerio de Economía y Competitividad, Spain). M. Schoebitz would like to thank the National Commission for Scientific and Technological Research of Chile (CONICYT) for the postdoctoral fellowship.

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The authors declare that they have no conflict of interest.

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  1. Department of Soil and Water Conservation, CSIC—Centro de Edafología y Biología Aplicada del Segura, P.O. Box 164, Campus de Espinardo, 30100, Murcia, Spain

    Carmen Mengual, Fuensanta Caravaca & Antonio Roldán

  2. Department of Soils and Natural Resources, Faculty of Agronomy, University of Concepción, Casilla 160-C, Concepción, Chile

    Mauricio Schoebitz

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  1. Carmen Mengual
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  2. Mauricio Schoebitz
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  3. Fuensanta Caravaca
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Correspondence to Carmen Mengual.

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Mengual, C., Schoebitz, M., Caravaca, F. et al. Assessment of the potential role of Streptomyces strains in the revegetation of semiarid sites: the relative incidence of strain origin and plantation site on plant performance and soil quality indicators. Biol Fertil Soils 52, 53–64 (2016). https://doi.org/10.1007/s00374-015-1052-x

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