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Bacterial community structure and detection of putative plant growth-promoting rhizobacteria associated with plants grown in Chilean agro-ecosystems and undisturbed ecosystems

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Abstract

Soil microorganisms with phytase- and 1-aminocyclopropane-1-carboxylate (ACC) deaminase activities are widely studied as plant growth-promoting rhizobacteria (PGPR). Here, we explored the bacterial community structure and occurrence of putative PGPR in plants grown in agro-ecosystems and undisturbed ecosystems from northern, central, and southern Chile. Total rhizobacterial community structure was evaluated by denaturing gradient gel electrophoresis, and dominant bands present in diverse ecosystems were sequenced. Significant differences in total bacterial communities were shown with some bacterial orders (Enterobacteriales, Actinomycetales, and Rhizobiales) being highly similar to both ecosystems. Twenty-nine putative PGPR, showing phytate- and ACC-degrading activities and production of auxin, were selected from across the sites. Based on 16S rRNA gene sequencing, the putative PGPR were characterized as Enterobacteriales (Enterobacter, Serratia, Pantoea, Rahnella, Leclercia), Pseudomonas, and Bacillus, consistent with previously reported PGPR and endophytic bacteria. Beta-propeller phytase genes with similarity to Bacillus were also identified. PGPR from agro-ecosystems appeared to show higher auxin production compared to those from undisturbed ecosystems. This study demonstrates that putative PGPR are widely distributed across Chilean soils. Further understanding of their contribution to the growth and adaptation of plant hosts to local soil conditions may provide opportunity for development of new PGPR in Chilean agriculture.

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References

  • Acuña J, Jorquera M, Martínez OA, Menezes-Blackburn D, Fernández MT, Marschner P, Greiner R, Mora ML (2011) Indole acetic acid and phytase activity produced by rhizosphere bacilli as affected by pH and metals. J Soil Sci Plant Nutr 11:1–12

    Google Scholar 

  • Acuña JJ, Jorquera MA, Barra PJ, Crowley DE, Mora ML (2013) Selenobacteria selected from the rhizosphere as a potential tool for Se biofortification of wheat crops. Biol Fertil Soils 49:175–185

    Article  Google Scholar 

  • Atkinson NJ, Urwin PE (2012) The interaction of plant biotic and abiotic stresses: from genes to the field. J Exp Bot 63:3523–3543

    Article  PubMed  CAS  Google Scholar 

  • Bakken LR, Frostegård Å (2006) Nucleic acid extraction from soil. In: Smalla K, Nannipieri P (eds) Series on soil biology: nucleic acids and proteins in soil. Springer, Berlin, 50–73 pp

    Google Scholar 

  • Bardhan S, Jose S, Jenkins MA, Webster CR, Udawatta RP, Stehn SE (2012) Microbial community diversity and composition across a gradient of soil acidity in spruce–fir forests of the southern Appalachian Mountains. Appl Soil Ecol 61:60–68

    Article  Google Scholar 

  • Bashan Y, Kamnev AA, de-Bashan LE (2013a) A proposal for isolating and testing phosphate-solubilizing bacteria that enhance plant growth. Biol Fertil Soils 49:1–2

    Article  Google Scholar 

  • Bashan Y, Kamnev AA, de-Bashan LE (2013b) Tricalcium phosphate is inappropriate as a 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 

  • Bausenwein U, Gattinger A, Langer U, Embacher A, Hartmann HP, Sommer M, Munch JC, Schloter M (2008) Exploring soil microbial communities and soil organic matter: variability and interactions in arable soils under minimum tillage practice. Appl Soil Ecol 40:67–77

    Article  Google Scholar 

  • Berendsen RL, Pieterse CMJ, Bakker PA (2012) The rhizosphere microbiome and plant health. Trends Plant Sci 17:478–486

    Article  PubMed  CAS  Google Scholar 

  • Bertsch PM, Bloom PR (1996) Aluminum. In: Bigham JM (ed) Methods of soil analysis, part 3—chemical methods. Soil Science Society of America, Madison, 526-527 pp

    Google Scholar 

  • Bhattacharyya PN, Jha DK (2012) Plant growth-promoting rhizobacteria (PGPR): emergence in agriculture. World J Microbiol Biotechnol 28:1327–1350

    Article  PubMed  CAS  Google Scholar 

  • Bissett A, Richardson AE, Baker G, Wakelin S, Thrall PH (2010) Life history determines biogeographical patterns of soil microbial communities over multiple spatial scales. Mol Ecol 19:4315–4327

    Article  Google Scholar 

  • Blaha D, Prigent-Combaret C, Mirza MS, Moënne-Loccoz Y (2006) Phylogeny of the 1-aminocyclopropane-1-carboxylic acid deaminase-encoding gene acdS in phytobeneficial and pathogenic Proteobacteria and relation with strain biogeography. FEMS Microbiol Ecol 56:455–470

    Article  PubMed  CAS  Google Scholar 

  • Briceño G, Jorquera MA, Demanet R, Mora ML, Durán N, Palma G (2010) Effect of cow slurry amendment on atrazine dissipation and bacterial community structure in an agricultural Andisol. Sci Total Environ 408:2833–2839

    Article  PubMed  Google Scholar 

  • Bulgarelli D, Schlaeppi K, Spaepen S, van Themaat EVL, Schulze-Lefert P (2013) Structure and functions of the bacterial microbiota of plants. Annu Rev Plant Biol 64:807–838

    Article  PubMed  CAS  Google Scholar 

  • Cea M, Jorquera M, Rubilar O, Langer H, Tortella G, Diez MC (2010) Bioremediation of soil contaminated with pentachlorophenol by Anthracophyllum discolor and its effect on soil microbial community. J Hazard Mater 181:315–323

    Article  PubMed  CAS  Google Scholar 

  • Cesco S, Mimmo T, Tonon G, Tomasi R, Pinton R, Terzano R, Neumann G, Weisskopf L, Renella G, Landi L, Nannipieri P (2012) Plant-borne flavonoids released into the rhizosphere: impact on soil bio-activities related to plant nutrition. A review. Biol Fertil Soils 48:123–150

    Article  CAS  Google Scholar 

  • Drees KP, Neilson JW, Betancourt JL, Quade J, Henderson DA, Pryor BM, Maier RM (2006) Bacterial community structure in the hyperarid core of the Atacama Desert, Chile. Appl Environ Microbiol 72:7902–7908

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Duan J, Müller KM, Charles TC, Vesely S, Glick BR (2009) 1-Aminocyclopropane-1-carboxylate (ACC) deaminase genes in rhizobia from southern Saskatchewan. Microb Ecol 57:423–436

    Article  PubMed  CAS  Google Scholar 

  • Fierer N, Jackson RB (2006) The diversity and biogeography of soil bacterial communities. Proc Natl Acad Sci U S A 103:626–631

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Glick BR (2004) Bacterial ACC deaminase and the alleviation of plant stress. Adv Appl Microbiol 56:291–312

    Article  PubMed  CAS  Google Scholar 

  • Grover M, Ali SZ, Sandhya V, Rasul A, Venkateswarlu B (2011) Role of microorganisms in adaptation of agriculture crops to abiotic stresses. World J Microbiol Biotechnol 27:1231–1240

    Article  Google Scholar 

  • Hamaki T, Suzuki M, Fudou R, Jojima Y, Kajiura T, Tabuchi A, Sen K, Shibai H (2005) Isolation of novel bacteria and actinomycetes using soil-extract agar medium. J Biosci Bioeng 99:485–492

    Article  PubMed  CAS  Google Scholar 

  • Huang H, Shi P, Wang Y, Luo H, Shao N, Wang G, Yang P, Yao B (2009) Diversity of beta-propeller phytase genes in the intestinal contents of grass carp provides insight into the release of major phosphorus from phytate in nature. Appl Environ Microbiol 75:1508–1516

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Iwamoto T, Tani K, Nakamura K, Suzuki Y, Kitagawa M, Eguchi M, Nasu M (2000) Monitoring impact of in situ biostimulation treatment on groundwater bacterial community by DGGE. FEMS Microbiol Ecol 32:129–141

    Article  PubMed  CAS  Google Scholar 

  • Jha CK, Annapurna K, Saraf M (2012) Isolation of rhizobacteria from Jatropha curcas and characterization of produced ACC deaminase. J Basic Microbiol 52:285–295

    Article  PubMed  CAS  Google Scholar 

  • Jorquera MA, Hernández MT, Rengel Z, Marschner P, Mora ML (2008) Isolation of culturable phosphobacteria with both phytate-mineralization and phosphate-solubilization activity from the rhizosphere of plants grown in a volcanic soil. Biol Fertil Soils 44:1025–1034

    Article  CAS  Google Scholar 

  • Jorquera MA, Hernández M, Martínez O, Marschner P, Mora ML (2010) Detection of aluminium tolerance plasmids and microbial diversity in the rhizosphere of plants grown in acidic volcanic soil. Eur J Soil Biol 46:255–263

    Article  CAS  Google Scholar 

  • Jorquera MA, Crowley DE, Marschner P, Greiner R, Fernández MT, Romero D, Menezes-Blackburn D, Mora ML (2011) Identification of β-propeller phytase-encoding genes in culturable Paenibacillus and Bacillus spp. from the rhizosphere of pasture plants on volcanic soils. FEMS Microbiol Ecol 75:163–172

    Article  PubMed  CAS  Google Scholar 

  • Jorquera MA, Shaharoona B, Nadeem SM, Mora ML, Crowley DE (2012) Plant growth-promoting rhizobacteria associated with ancient clones of creosote bush (Larrea tridentata). Microb Ecol 64:1008–1017

    Article  PubMed  Google Scholar 

  • Jorquera MA, Martínez OA, Marileo LG, Acuña JJ, Saggar S, Mora ML (2013) Effect of nitrogen and phosphorus fertilization on the composition of rhizobacterial communities of two Chilean Andisol pastures. World J Microbiol Biotechnol 30:99–107

    Article  PubMed  Google Scholar 

  • Kamala-Kannan S, Lee KJ, Park SM, Chae JC, Yun BS, Lee YH, Park YJ, Oh BT (2010) Characterization of ACC deaminase gene in Pseudomonas entomophila strain PS-PJH isolated from the rhizosphere soil. J Basic Microbiol 50:200–205

    PubMed  CAS  Google Scholar 

  • Kang BG, Kim WT, Yun HS, Chang SC (2010) Use of plant growth-promoting rhizobacteria to control stress responses of plant roots. Plant Biotechnol Rep 4:179–183

    Article  Google Scholar 

  • Kerovuo J, Lauraeus M, Nurminen P, Kalkkinen N, Apajalahti J (1998) Isolation, characterization, molecular gene cloning, and sequencing of a novel phytase from Bacillus subtilis. Appl Environ Microbiol 64:2079–2085

    PubMed  CAS  PubMed Central  Google Scholar 

  • Lim BL, Yeung P, Cheng C, Hill JE (2007) Distribution and diversity of phytate-mineralizing bacteria. ISME J 1:321–330

    PubMed  CAS  Google Scholar 

  • Lombard N, Prestat E, van Elsas JD, Simonet P (2011) Soil-specific limitations for access and analysis of soil microbial communities by metagenomics. FEMS Microbiol Ecol 78:31–49

    Article  PubMed  CAS  Google Scholar 

  • Marschner P, Yang CH, Lieberei R, Crowley DE (2001) Soil and plant specific effects on bacterial community composition in the rhizosphere. Soil Biol Biochem 33:1437–1445

    Article  CAS  Google Scholar 

  • Martínez OA, Jorquera MA, Crowley DE, Mora ML (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

    Article  Google Scholar 

  • Martínez-Viveros O, Jorquera MA, Crowley DE, Gajardo G, Mora ML (2010) Mechanisms and practical considerations involved in plant growth promotion by rhizobacteria. J Soil Sci Plant Nutr 10:293–319

    Article  Google Scholar 

  • Mayak S, Tirosh T, Glick BR (2004a) Plant growth-promoting bacteria confer resistance in tomato plants to salt stress. Plant Physiol Biochem 42:565–572

    Article  PubMed  CAS  Google Scholar 

  • Mayak S, Tirosh T, Glick BR (2004b) Plant growth-promoting bacteria that confer resistance to water stress in tomatoes and peppers. Plant Sci 166:525–530

    Article  CAS  Google Scholar 

  • Mendes LW, Kuramae EE, Navarrete AA, van Veen JA, Tsai SM (2014) Taxonomical and functional microbial community selection in soybean rhizosphere. ISME J. doi:10.1038/ismej.2014.17

    Google Scholar 

  • Mullen MD (2005) Phosphorus in soils: biological interactions. In: Hillel D, Rosenzweig C, Powlson D, Scow K, Singer M, Sparks D (eds) Encyclopedia of soils in the environment, vol 3, Academic. Elsevier Ltd., Oxford, pp 210–215

    Google Scholar 

  • Murphy J, Riley JP (1962) A modified single solution method for the determination of phosphate in natural waters. Anal Chim Acta 27:31–36

    Article  CAS  Google Scholar 

  • Nadeem SM, Zahir ZA, Naveed M, Ashraf M (2010) Microbial ACC-deaminase: prospects and applications for inducing salt tolerance in plants. CRC Crit Rev Plant Sci 29:360–393

    Article  CAS  Google Scholar 

  • Nakamura K, Hiraishi A, Yoshimi Y et al (1995) Microlunatus phosphovorus gen. nov., sp. nov., a new gram-positive polyphosphate-accumulating bacterium isolated from activated sludge. Int J Syst Bacteriol 45:17–22

    Article  PubMed  CAS  Google Scholar 

  • Neilson JW, Quade J, Ortiz M, Nelson WM, Legatzki A, Tian F, LaComb M, Betancourt JL, Wing RA, Soderlund CA, Maier RM (2012) Life at the hyperarid margin: novel bacterial diversity in arid soils of the Atacama Desert, Chile. Extremophiles 16:553–566

    Article  PubMed  Google Scholar 

  • Palacios O, 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 

  • Pastorelli R, Piccolo R, Simoncini S, Landi S (2013) New primers for denaturing gradient gel electrophoresis analysis of nitrate-reducing bacterial community in soil. Pedosphere 23:340–349

    Article  CAS  Google Scholar 

  • Patten CL, Glick BR (2002) Role of Pseudomonas putida indole acetic acid in development of the host plant root system. Appl Environ Microbiol 68:3795–3801

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Peace TA, Brock KV, Stills HF Jr (1994) Comparative analysis of the 16S rRNA gene sequence of the putative agent of proliferative ileitis of hamsters. Int J Syst Bacteriol 44:832–835

    Article  PubMed  CAS  Google Scholar 

  • Penrose DM, Glick BR (2003) Methods for isolating and characterizing ACC deaminase-containing plant growth-promoting rhizobacteria. Physiol Plant 118:10–15

    Article  PubMed  CAS  Google Scholar 

  • Ramond JB, Tshabuse F, Bopda CW, Cowan DA, Tuffin MI (2013) Evidence of variability in the structure and recruitment of rhizospheric and endophytic bacterial communities associated with arable sweet sorghum (Sorghum bicolor (L) Moench). Plant Soil 372:265–278

    Article  CAS  Google Scholar 

  • Richardson AE (2001) Prospects for using soil microorganisms to improve the acquisition of phosphorus by plants. Aust J Plant Physiol 28:897–906

    Google Scholar 

  • Richardson AE, Simpson RJ (2011) Soil microorganisms mediating phosphorus availability update on microbial phosphorus. Plant Physiol 156:989–996

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Saul-Tcherkas V, Unc A, Steinberger Y (2013) Soil microbial diversity in the vicinity of desert shrubs. Microb Ecol 65:689–699

    Article  PubMed  Google Scholar 

  • Shoebitz M, Ribaudo CM, Pardo MA, Cantore ML, Ciampi L, Curá JA (2009) Plant growth promoting properties of a strain of Enterobacter ludwigii isolated from Lolium perenne rhizosphere. Soil Biol Biochem 41:1768–1774

    Article  CAS  Google Scholar 

  • Somerfield PJ (2008) Identification of the Bray–Curtis similarity index: comment on Yoshioka (2008). Mar Ecol Prog Ser 372:303–306

    Article  Google Scholar 

  • Steen I (1998) Phosphorus availability in the 21st century: management of a non-renewable resource. Phosphorus Potassium 217:25–31

    Google Scholar 

  • Timmusk S, Paalme V, Pavlicek T, Bergquist J, Vangala A, Danilas T, Nevo E (2011) Bacterial distribution in the rhizosphere of wild barley under contrasting microclimates. PLoS ONE 6:e17968. doi:10.1371/journal.pone.0017968

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Turner BL, Papházy MJ, Haygarth PM, McKelvie ID (2002) Inositol phosphates in the environment. Philos Trans R Soc Lond B Biol Sci 357:449–469

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Tye AJ, Siu FKY, Leung TYC, Lim BL (2002) Molecular cloning and the biochemical characterization of two novel phytases from B. subtilis 168 and B. licheniformis. Appl Microbiol Biotechnol 59:190–207

    Article  PubMed  CAS  Google Scholar 

  • Vacheron J, Desbrosses G, Bouffaud ML, Touraine B, Moënne-Loccoz Y, Muller D, Legendre L, Wisniewski-Dyé F, Prigent-Combaret C (2013) Plant growth-promoting rhizobacteria and root system functioning. Front Plant Sci 4:1–19

    Article  Google Scholar 

  • van Elsas JD, Boersma FGH (2011) A review of molecular methods to study the microbiota of soil and the mycosphere. Eur J Soil Biol 47:77–87

    Article  Google Scholar 

  • Van Kauwenbergh SJ (2010) World phosphate rock reserves and resources. International Fertilizer Development Centre, 48 pp. Muscle Shoals, Alabama, USA

  • Warncke D, Brown JR (1998) Potassium and other basic cations. In: Brown JR (ed) Recommended chemical soil test procedures for the North Central Region. NCR Publication No. 221. Missouri Agricultural Experiment Station, Columbia, 31–33 pp

    Google Scholar 

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Acknowledgments

Chilean Government financed this study through project Fondecyt No. 1120505 and 1141247. The authors would like thank to Dr. Howard Langer and M.Sc. Loreto Manosalva for valuable logistical support during sampling of Conguillio National Park and Patagonia, respectively.

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Authors and Affiliations

  1. Scientific and Technological Bioresource Nucleus (BIOREN), Universidad de La Frontera, Ave. Francisco Salazar 01145, Temuco, Chile

    Milko A. Jorquera, Nitza G. Inostroza, Daniela C. Campos & María L. Mora

  2. Programa de Doctorado en Ciencias de Recursos Naturales, Universidad de La Frontera, Ave. Francisco Salazar 01145, Temuco, Chile

    Lorena M. Lagos, Patricio J. Barra, Luis G. Marileo & Joaquin I. Rilling

  3. Department of Environmental Sciences, University of California Riverside, 900 University Ave, Riverside, CA, 92521, USA

    David E. Crowley

  4. CSIRO Plant Industry, PO Box 1600, Canberra, Australia, 2601

    Alan E. Richardson

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  1. Milko A. Jorquera
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  2. Nitza G. Inostroza
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Correspondence to Milko A. Jorquera.

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Jorquera, M.A., Inostroza, N.G., Lagos, L.M. et al. Bacterial community structure and detection of putative plant growth-promoting rhizobacteria associated with plants grown in Chilean agro-ecosystems and undisturbed ecosystems. Biol Fertil Soils 50, 1141–1153 (2014). https://doi.org/10.1007/s00374-014-0935-6

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