Free Standard AU & NZ Shipping For All Book Orders Over $80!
Register      Login
Soil Research Soil Research Society
Soil, land care and environmental research
RESEARCH ARTICLE

Comparison of plant growth-promoting rhizobacteria in a pine forest soil and an agricultural soil

Víctor M. Flores-Núñez A , Enriqueta Amora-Lazcano A , Angélica Rodríguez-Dorantes B , Juan A. Cruz-Maya C and Janet Jan-Roblero A D
+ Author Affiliations
- Author Affiliations

A Departamento de Microbiología, Escuela Nacional de Ciencias Biológicas, Instituto Politécnico Nacional, Prolongación de Carpio y Plan de Ayala s/n. Col. Sto. Tomás, Ciudad de México, 11340, México.

B Departamento de Botánica, Escuela Nacional de Ciencias Biológicas, Instituto Politécnico Nacional, Prolongación de Carpio y Plan de Ayala s/n. Col. Sto. Tomás, Ciudad de México, 11340, México.

C Unidad Profesional Interdisciplinaria en Ingeniería y Tecnologías Avanzadas, Instituto Politécnico Nacional, Av. IPN 2580, Col. La Laguna Ticoman, Ciudad de México, 07340, México.

D Corresponding author. Email: jjan_r@yahoo.com.mx

Soil Research 56(4) 346-355 https://doi.org/10.1071/SR17227
Submitted: 26 August 2017  Accepted: 26 November 2017   Published: 10 April 2018

Abstract

The load and diversity of plant growth-promoting rhizobacteria (PGPR) are used as biomarkers to evaluate the health and quality of the soil. In the present study, the diversity of PGPRs and the physicochemical properties of the soil were used as comparative biomarkers in two adjacent soils (a pine forest soil and an agricultural soil) of the same region in Mexico City in order to investigate the effects of land use change. Bacterial diversity and physicochemical properties differed between the two soils. In the pine forest soil, PGPR were distributed at similar proportions in the Proteobacteria (29.41%), Actinobacteria (29.41%) and Firmicutes (35.29%) phyla, whereas the remaining PGPR were in Bacteroidetes (5.88%). In the agricultural soil, most PGPR belonged to the Phylum Firmicutes (50%), with the remaining belonging to Proteobacteria (22.73%), Actinobacteria (18.18%) and Bacteroidetes (9.09%). Percentages of bacteria producing indole acetic acid (90.91%) and siderophores (40.91%) were higher in agricultural soil. A canonical correspondence analysis (CCA) was used to correlate PGPR with the physicochemical characteristics of the soils. The CCA revealed that differences between both soils and the physicochemical properties of the soils affected isolated bacterial species and their distribution. These results demonstrate that the PGPR are correlated with the physicochemical properties of the soil, exhibiting differences between an agricultural soil and a pine forest soil.

Additional keywords: canonical coordinate analysis, physicochemical properties.


References

Adesemoye AO, Obini M, Ugoji EO (2008) Comparison of plant growth-promotion with Pseudomonas aeruginosa and Bacillus subtilis in three vegetables. Brazilian Journal of Microbiology 39, 423–426.
Comparison of plant growth-promotion with Pseudomonas aeruginosa and Bacillus subtilis in three vegetables.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3sbnvVSgsw%3D%3D&md5=5c0cd0705053ece3545d57394abe5a9fCAS |

Ahemad M, Khan MS (2011) Functional aspects of plant growth promoting rhizobacteria: recent advancements. Microbiology Insights 1, 39–54.
Functional aspects of plant growth promoting rhizobacteria: recent advancements.Crossref | GoogleScholarGoogle Scholar |

Atlas RM (2010) ‘Handbook of microbiological media.’ 4th edn. (CRC and ASM Press: Washington DC, USA)

Barajas-Aceves M, Dendooven L (2001) Nitrogen, carbon and phosphorus mineralization in soils from semi-arid highlands of central Mexico amended with tannery sludge. Bioresource Technology 77, 121–130.
Nitrogen, carbon and phosphorus mineralization in soils from semi-arid highlands of central Mexico amended with tannery sludge.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXis1Orurg%3D&md5=a7eb352fd422f8810efddd2d1191155fCAS |

Barriuso J, Ramos SB, Lucas JA, Probanza LA, García-Villaraco A, Gutiérrez MFJ (2008) Ecology, genetic diversity and screening strategies of plant growth promoting rhizobacteria (PGPR). In ‘Plant–bacteria interactions. Strategies and techniques to promote plant growth’. (Ed. I. Ahmad.) pp. 1–18. (Wiley: Weinheim, Germany)

Beaulieu C (2001) Actinomycetes, promising tools to control plant diseases and to promote plant growth. Phytoprotection 82, 85–102.
Actinomycetes, promising tools to control plant diseases and to promote plant growth.Crossref | GoogleScholarGoogle Scholar |

Blažka P, Fischer Z (2014) Moisture, water holding, drying and wetting in forest soils. Open Journal of Soil Science 4, 174–184.
Moisture, water holding, drying and wetting in forest soils.Crossref | GoogleScholarGoogle Scholar |

Camacho C, Coulouris G, Avagyan V, Ma N, Papadopoulos J, Bealer K, Madden T (2009) BLAST+: architecture and applications. BMC Bioinformatics 10,
BLAST+: architecture and applications.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhsF2gu7jP&md5=31b337c026abcef0cb9f1eccf8a11f4aCAS | (Article no. 421)

Castanheira N, Dourado AC, Kruz S, Alves PIL, Delgado-Rodríguez AI, Pais I, Semedo J, Scotti-Campos P, Sánchez C, Borges N, Carvalho G, Barreto-Crespo MT, Fareleira P (2016) Plant growth-promoting Burkholderia species isolated from annual ryegrass in Portuguese soils. Journal of Applied Microbiology 120, 724–739.
Plant growth-promoting Burkholderia species isolated from annual ryegrass in Portuguese soils.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XjsFeju7o%3D&md5=d74be2b99b2c673c961e23ab09424ed3CAS |

Da Costa PB, Granada CE, Ambrosini A, Moreira F, de Souza R, dos Passos JF, Arruda L, Passaglia LM (2014) A model to explain plant growth promotion traits: a multivariate analysis of 2,211 bacterial isolates. PLoS One 9, e116020
A model to explain plant growth promotion traits: a multivariate analysis of 2,211 bacterial isolates.Crossref | GoogleScholarGoogle Scholar |

Delgado-Baquerizo M, Reich PB, Khachane AN, Campbell CD, Thomas N, Freitag TE, Abu Al-Soud W, Sørensen S, Bardgett RD, Singh BK (2017) It is elemental: soil nutrient stoichiometry drives bacterial diversity. Environmental Microbiology 19, 1176–1188.
It is elemental: soil nutrient stoichiometry drives bacterial diversity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2sXksFaktLc%3D&md5=b5b13970501d713a86e9aac6fa1eefc9CAS |

Franco-Correa M, Quintana A, Duque C, Suarez C, Rodríguez MX, Barea JM (2010) Evaluation of actinomycete strains for key traits related with plant growth promotion and mycorrhiza helping activities. Applied Soil Ecology 45, 209–217.
Evaluation of actinomycete strains for key traits related with plant growth promotion and mycorrhiza helping activities.Crossref | GoogleScholarGoogle Scholar |

Galtier N, Gouy M, Gautier C (1996) SEAVIEW and PHYLO_WIN: Two graphic tools for sequence alignment and molecular phylogeny. Computer Applications in the Biosciences 12, 543–548.
SEAVIEW and PHYLO_WIN: Two graphic tools for sequence alignment and molecular phylogeny.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXhtlWktLw%3D&md5=f8e698e6190ca2bd8449c9f735277099CAS |

Gkorezis P, Daghio M, Franzetti A, Van Hamme JD, Sillen W, Vangronsveld J (2016) The interaction between plants and bacteria in the remediation of petroleum hydrocarbons: an environmental perspective. Frontiers in Microbiology 7,
The interaction between plants and bacteria in the remediation of petroleum hydrocarbons: an environmental perspective.Crossref | GoogleScholarGoogle Scholar |

Gombeer S, Ramond JB, Eckardt FD, Seely M, Cowan DA (2015) The influence of surface soil physicochemistry on the edaphic bacterial communities in contrasting terrain types of the Central Namib Desert. Geobiology 13, 494–505.
The influence of surface soil physicochemistry on the edaphic bacterial communities in contrasting terrain types of the Central Namib Desert.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXht1yhsLvJ&md5=f0f1f566d4141c086078df32f13afdb8CAS |

Huot H, Joyner J, Córdoba A, Shaw RK, Wilson MA, Walter R, Muth TR, Cheng Z (2017) Characterizing urban soils in New York City: profile properties and bacterial communities. Journal of Soils and Sediments 17, 393–407.
Characterizing urban soils in New York City: profile properties and bacterial communities.Crossref | GoogleScholarGoogle Scholar |

Khalid A, Arshad M, Zahir ZA (2004) Screening plant growth-promoting rhizobacteria for improving growth and yield of wheat. Journal of Applied Microbiology 96, 473–480.
Screening plant growth-promoting rhizobacteria for improving growth and yield of wheat.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD2c%2Fntlykuw%3D%3D&md5=fd8297dcccab1dcc1c6299c379e9c79fCAS |

Kim WI, Cho WK, Kim SN, Chu H, Ryu KY, Yun JC, Park CS (2011) Genetic diversity of cultivable plant growth-promoting rhizobacteria in Korea. Journal of Microbiology and Biotechnology 21, 777–790.
Genetic diversity of cultivable plant growth-promoting rhizobacteria in Korea.Crossref | GoogleScholarGoogle Scholar |

Kumar A, Prakash A, Johri BN (2011) Bacillus as PGPR in crop ecosystem. In ‘Bacteria in agrobiology: crop ecosystems’. (Ed. D. K. Maheshwari.) pp. 37–59. (Springer: Berlin, Germany)

Kumar A, Kumar A, Devi S, Patil S, Payal C, Negi S (2012) Isolation, screening and characterization of bacteria from rhizospheric soils for different plant growth promotion (PGP) activities: an in vitro study. Recent Research in Science and Technology 4, 1–5.

Lambert B, Joos H, Dierickx S, Vantomme R, Swings J, Kersters K, Montagu VM (1990) Identification and plant interaction of a Phyllobacterium sp., a predominant rhizobacterium of young sugar beet plants. Applied and Environmental Microbiology 56, 1093–1102.

Lau JA, Lennon JT (2012) Rapid responses of soil microorganisms improve plant fitness in novel environments. Proceedings of the National Academy of Sciences of the United States of America 109, 14058–14062.
Rapid responses of soil microorganisms improve plant fitness in novel environments.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhsVegt7nN&md5=1d2d6ccd7eadcd4010d5895baf29eadbCAS |

Liu X, Herbert SJ, Hashemi AM, Zhang X, Ding G (2006) Effects of agricultural management on soil organic matter and carbon transformation – a review. Plant, Soil and Environment 52, 531–543.

McSpadden Gardener BB (2004) Ecology of Bacillus and Paenibacillus spp. in agricultural ecosystems. Phytopathology 94, 1252–1258.
Ecology of Bacillus and Paenibacillus spp. in agricultural ecosystems.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhtVWlurbK&md5=fd02bf61c17dac5c5bb4b4969d669322CAS |

Mergaert J, Swings J (2005) Phyllobacteriaceae fam. nov. In ‘Bergey’s manual of systematics of Archaea and Bacteria’. (Ed. W. B. Whitman.) pp. 1–3. (John Wiley & Sons in association with Bergey’s Manual Trust: New York, NY, USA)

Nannipieri P, Ascher J, Ceccherini MT, Landi L, Pietramellara G, Renella G (2003) Microbial diversity and soil functions. European Journal of Soil Science 54, 655–670.
Microbial diversity and soil functions.Crossref | GoogleScholarGoogle Scholar |

Neumann D, Heuer A, Hemkemeyer M, Martens R, Tebbe CC (2013) Response of microbial communities to long-term fertilization depends on their microhabitat. FEMS Microbiology Ecology 86, 71–84.
Response of microbial communities to long-term fertilization depends on their microhabitat.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhsVWrtb7P&md5=069146d77b06f3fc9f496d85861ad84aCAS |

Nimnoi P, Pongsilp N (2009) Genetic diversity and plant-growth promoting ability of the indole-3-acetic acid (IAA) synthetic bacteria isolated from agricultural soil as well as rhizosphere, rhizoplane and root tissue of Ficus religiosa L., Leucaena leucocephala and Piper sarmentosum Roxb. Research Journal of Agriculture and Biological Sciences 5, 29–41.

Oksanen J, Blanchet FG, Friendly M, Kindt R, Legendre P, McGlinn D, Minchin PR, O’Hara RB, Simpson GL, Solymos M, Stevens HH, Szoecs E, Wagner H (2016) Vegan: community ecology package. R package version 2.4-0. Available at https://cran.r-project.org/web/packages/vegan/ [verified June 2016].

R Core Team (2014) R: A language and environment for statistical computing. (R Foundation for Statistical Computing: Vienna, Austria.) Available at http://www.R-project.org/ [verified October 2015].

Relman DA (1993) Universal bacterial 16S rDNA amplification and sequencing. In ‘Diagnostic molecular microbiology: principles and applications’. (Eds D. H. Persing, T. F. Smith, F. C. Tenover, T. T. White) pp. 489–495 (American Society for Microbiology: Washington DC, USA)

Rhoades JD, Mantghi NA, Shause PJ, Alves W (1989) Estimating soil salinity from saturated soil-paste electrical conductivity. Soil Science Society of America Journal 53, 428–433.
Estimating soil salinity from saturated soil-paste electrical conductivity.Crossref | GoogleScholarGoogle Scholar |

Roesti D, Gaur R, Johri BN, Imfeld G, Sharma S, Kawaljeet K, Aragno M (2006) Plant growth stage, fertiliser management and bio-inoculation of arbuscular mycorrhizal fungi and plant growth promoting rhizobacteria affect the rhizobacterial community structure in rain-fed wheat fields. Soil Biology & Biochemistry 38, 1111–1120.
Plant growth stage, fertiliser management and bio-inoculation of arbuscular mycorrhizal fungi and plant growth promoting rhizobacteria affect the rhizobacterial community structure in rain-fed wheat fields.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XjvFSis7g%3D&md5=c51036c2b4d53cb9408b51418a7cb201CAS |

Ruíz-Valdiviezo VM, Luna-Guido M, Galzy A, Gutiérrez-Miceli FA, Dendooven L (2010) Greenhouse gas emissions and C and N mineralization in soils of Chiapas (México) amended with leaves of Jatropha curcas L. Applied Soil Ecology 46, 17–25.
Greenhouse gas emissions and C and N mineralization in soils of Chiapas (México) amended with leaves of Jatropha curcas L.Crossref | GoogleScholarGoogle Scholar |

Sessitsch Sessitsch Sessitsch Sessitsch Sessitsch Sessitsch Sessitsch Sessitsch Sessitsch Sessitsch Sessitsch Sessitsch (2005) Burkholderia phytofirmans sp. nov., a novel plant-associated bacterium with plant-beneficial properties. International Journal of Systematic and Evolutionary Microbiology 55, 1187–1192.
Burkholderia phytofirmans sp. nov., a novel plant-associated bacterium with plant-beneficial properties.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXltlOmu70%3D&md5=d63f589ccbb754b279286c7721f81e64CAS |

Sessitsch A, Weilharter A, Gerzabek MH, Kirchmann H, Kandeler E (2001) Microbial population structures in soil particle size fractions of a long-term fertilizer field experiment. Applied and Environmental Microbiology 67, 4215–4224.
Microbial population structures in soil particle size fractions of a long-term fertilizer field experiment.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXmslWisL0%3D&md5=35c2bc687b9610b570b1b493ec2fd311CAS |

Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution 28, 2731–2739.
MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXht1eiu73K&md5=e9cace87eadabe4cfc1968e97c7cb5dbCAS |

Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research 25, 4876–4882.
The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXntFyntQ%3D%3D&md5=8171eeb44f02bff091aab5f76f6a73b3CAS |

Torsvik V, Øvreås L (2007) Microbial phylogeny and diversity in soil. In ‘Modern soil microbiology’. (Eds J. D. Elsas, J. K. Jansson, J. T. Trevors.) pp. 41–47. (CRC Press: Boca Raton, FL, USA)

Vásquez-Murrieta MS, Migueles-Garduño I, Franco-Hernández O, Govaerts B, Dendooven L (2006) C and N mineralization and microbial biomass in heavy-metal contaminated soil. European Journal of Soil Biology 42, 89–98.
C and N mineralization and microbial biomass in heavy-metal contaminated soil.Crossref | GoogleScholarGoogle Scholar |

Vejan P, Abdullah R, Khadiran T, Ismail S, Nasrulhaq-Boyce A (2016) Role of plant growth promoting rhizobacteria in agricultural sustainability – a review. Molecules (Basel, Switzerland) 21,
Role of plant growth promoting rhizobacteria in agricultural sustainability – a review.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XhsFeisbnE&md5=35baa1ec9d85394bf821e9c6cdf3349dCAS |

Whittles CL, Little RC (1950) A colorimetric method for the determination of potassium and its application to the analysis of soil extracts. Journal of the Science of Food and Agriculture 1, 323–326.
A colorimetric method for the determination of potassium and its application to the analysis of soil extracts.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaG3MXit1KhsQ%3D%3D&md5=45ea891dc0d255af32ec8a0a3ee5058fCAS |

Wilson K (2001) Unit 2.4: preparation of genomic DNA from bacteria. In ‘Current protocols in molecular biology’. Chapter 2: Unit 2.4: 2.4.1–2.4.5. (John Wiley & Sons: New York, NY, USA)

Xu LH, Li QR, Jiang CL (1996) Diversity of soil actinomycetes in Yunnan, China. Applied and Environmental Microbiology 62, 244–248.

Yoon SH, Ha SM, Kwon S, Lim J, Kim Y, Seo H, Chun J (2017) Introducing EzBioCloud: a taxonomically united database of 16S rRNA and whole genome assemblies. International Journal of Systematic and Evolutionary Microbiology 67, 1613–1617.
Introducing EzBioCloud: a taxonomically united database of 16S rRNA and whole genome assemblies.Crossref | GoogleScholarGoogle Scholar |

Zhang L, Xu Z (2008) Assessing bacterial diversity in soil: A brief review. Journal of Soils and Sediments 8, 379–388.
Assessing bacterial diversity in soil: A brief review.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhsVyntb3O&md5=28ef306c1cd92e546e678bbf8cd543eaCAS |