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Using native trees and cacti to improve soil potential nitrogen fixation during long-term restoration of arid lands

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Abstract

Background and aims

A major problem in all restoration and rehabilitation projects is to restore the function of the ecosystem. Nitrogen, next to water, is the most limiting factor for productivity of arid terrestrial ecosystems.

Methods

We used a successful restored area, completed 10 years earlier, in comparison with an undisturbed scrubland area and a remaining, disturbed area in the southern Sonoran Desert in Baja California, Mexico. We compared the abundance of the nifH gene, estimated by qPCR, potential N2 fixation activity by acetylene reduction assay, and diversity of diazotrophs by denaturing gradient gel electrophoresis in the rhizosphere of the most representative plant species, the cardon cactus and the mesquite used for restoration.

Results

The abundance of N2-fixing bacteria in the rhizosphere of cardon growing with mesquite had significantly higher abundance of nifH gene than the rhizosphere of cardon that grew separately. Across all samples, the potential N2 fixation was significantly higher in soil samples from the restored site than samples from the undisturbed and disturbed sites.

Conclusions

Successful long-term restoration improved the potential N2 fixation to a level similar to undisturbed lands. Beneficial interactions between cardon and mesquite are a promising venue for desert reforestation by their contribution to improve N2 fixing potential in degraded arid lands and increasing the population of diazotrophs.

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References

  • Bacilio M, Hernandez JP, Bashan Y (2006) Restoration of giant cardon cacti in barren desert soil amended with common compost and inoculated with Azospirillum brasilense. Biol Fertil Soils 43:112–119

    Article  Google Scholar 

  • Bacilio M, Vazquez P, Bashan Y (2011) Water versus spacing: a possible growth preference among young individuals of the giant cardon cactus of the Baja California Peninsula. Environ Exp Bot 70:29–36

    Article  Google Scholar 

  • Bainbridge DA (2007) A guide for desert and dryland restoration: new hope for arid lands. Island Press, Washington, DC, p 416

    Google Scholar 

  • Barron AR, Wurzburger N, Bellenger JP, Wright SJ, Kraepiel AML, Hedin LO (2008) Molybdenum limitation of asymbiotic nitrogen fixation in tropical forest soils. Nat Geosci 2:42–45

    Article  Google Scholar 

  • Bashan Y (1999) Interactions of Azospirillum spp. in soils—a review. Biol Fertil Soils 29:246–256

    Article  CAS  Google Scholar 

  • Bashan Y, de-Bashan LE (2010) Microbial populations of arid lands and their potential for restoration of deserts. In: Dion P (ed) Soil biology and agriculture in the tropics. Soil biology series 21. Chapter 6. Springer, Berlin, pp 109–137

    Chapter  Google Scholar 

  • Bashan Y, Rojas A, Puente ME (1999) Improved establishment and development of three cacti species inoculated with Azospirillum brasilense transplanted into disturbed urban desert soil. Can J Microbiol 45:441–451

    Article  CAS  Google Scholar 

  • Bashan Y, Davis EA, Carrillo A, Linderman RG (2000a) Assessment of VA mycorrhizal inoculum potential in relation to the establishment of cactus seedlings under mesquite nurse-trees in the Sonoran desert. Appl Soil Ecol 14:165–176

    Article  Google Scholar 

  • Bashan Y et al (2000b) A proposal for conservation of exemplary stands of the giant cardon cactus (Pachycereus pringlei [S. Wats Britt. & Ross]) in Baja California Sur, Mexico. Nat Area J 20:197–200

    Google Scholar 

  • Bashan Y, Salazar B, Puente ME (2009a) Responses of native legume desert trees used for reforestation in the Sonoran Desert to plant growth-promoting microorganisms in screen house. Biol Fertil Soils 45:655–662

    Article  Google Scholar 

  • Bashan Y, Salazar BG, Puente ME, Bacilio M, Linderman R (2009b) Enhanced establishment and growth of giant cardon cactus in an eroded field in the Sonoran Desert using native legume trees as nurse plants aided by plant growth-promoting microorganisms and compost. Biol Fertil Soils 45:585–594

    Article  Google Scholar 

  • Bashan Y, Salazar BG, Moreno M, Lopez 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 Manage 102:26–36

    Article  CAS  PubMed  Google Scholar 

  • Belnap J (2002) Nitrogen fixation in biological soil crusts from southeast Utah, USA. Biol Fertil Soils 35:128–135

    Article  CAS  Google Scholar 

  • Buckley DH, Schmidt TM (2001) Environmental factors influencing the distribution of rRNA from Verrucomicrobia in soil. FEMS Microbiol Ecol 35:105–112

    Article  CAS  PubMed  Google Scholar 

  • Carrillo AE, Li CY, Bashan Y (2002) Increased acidification in the rhizosphere of cactus seedlings induced by Azospirillum brasilense. Naturwissenschaften 89:428–432

    Article  CAS  PubMed  Google Scholar 

  • Carrillo-Garcia A, Leon de la Luz JL, Bashan Y, Bethlenfalvay GJ (1999) Nurse plants, mycorrhizae, and plant establishment in a disturbed area of the Sonoran Desert. Restor Ecol 7:321–335

    Article  Google Scholar 

  • Carrillo-Garcia A, Bashan Y, Diaz-Rivera E, Bethlenfalvay GJ (2000) Effects of resource island soils, competition, and inoculation with Azospirillum on survival and growth of Pachycereus pringlei, the giant cactus of the Sonoran Desert. Restor Ecol 8:65–73

    Article  Google Scholar 

  • Cusack DF, Silver W, McDowell WH (2009) Biological nitrogen fixation in two tropical forests: ecosystem level patterns and effects of nitrogen fertilization. Ecosystems 12:1299–1315

    Article  CAS  Google Scholar 

  • DeGrood SH, Claassen VP, Scow KM (2005) Microbial community composition on native and drastically disturbed serpentine soils. Soil Biol Biochem 37:1427–1435

    Article  CAS  Google Scholar 

  • Diallo MD, Willems A, Vloemans N, Cousin S, Vandekerckhove TT, de Lajudie P, Neyra M, Vyverman W, Gillis M, Van der Gucht K (2004) Polymerase chain reaction denaturing gradient gel electrophoresis analysis of the N2-fixing bacterial diversity in soil under Acacia tortilis ssp. raddian and Balanites aegyptiaca in the dryland part of Senegal. Environ Microbiol 6:400–415

    Article  CAS  Google Scholar 

  • Drezner TD (2006) The regeneration of a protected Sonoran Desert cactus since 1800 A.D. over 50,000 km2 of its range. Plant Ecol 183:171–176

    Article  Google Scholar 

  • Felker P, Clark PR (1980) Nitrogen fixation (acetylene reduction) and cross inoculation in 12 Prosopis (mesquite) species. Plant Soil 57:177–186

    Article  CAS  Google Scholar 

  • Grandlic CJ, Mendez MO, Chorover J, Machado B, Maier RM (2008) Identification of plant growth-promoting bacteria suitable for phytostabilization of mine tailings. Environ Sci Technol 42:2079–2084

    Article  CAS  PubMed  Google Scholar 

  • Gundlapally SR, Garcia-Pichel F (2006) The community and phylogenetic diversity of biological soil crusts in the Colorado Plateau studied by molecular fingerprinting and intensive cultivation. Microb Ecol 52:345–357

    Article  PubMed  Google Scholar 

  • Halvorson JJ, Bolton H Jr, Smith JL, Rossi RE (1994) Geostatistical analysis of resource islands under Artemisia tridentata in the shrub-steppe. Great Basin Nat 54:313–328

    Google Scholar 

  • Hernandez J-P, de-Bashan LE, Rodriguez DJ, Rodriguez Y, Bashan Y (2009) Growth promotion of the freshwater microalga Chlorella vulgaris by the nitrogen-fixing, plant growth-promoting bacterium Bacillus pumilus from arid zone soils. Eur J Soil Biol 45:88–93

    Article  CAS  Google Scholar 

  • Jackson ML (1958) Soil chemical analysis. Prentice-Hall, Upper Saddle River, NJ, pp 146–151

    Google Scholar 

  • LeBauer DS, Treseder KK (2008) Nitrogen limitation of net primary productivity in terrestrial ecosystems is globally distributed. Ecology 89:371–379

    Article  PubMed  Google Scholar 

  • León de la Luz JL, Coria Benet R, Cruz Estrada M (1996) Fenologia floral de una comunidad arido-tropical de Baja California Sur, México (Floral phenology of an arid-tropical community of Baja California Sur, Mexico). Acta Botánica Mexicana 35:45–64 (in Spanish)

    Google Scholar 

  • Lopez BR, Bashan Y, Bacilio M (2011) Endophytic bacteria of Mammillaria fraileana, an endemic rock-colonizing cactus of the Southern Sonoran Desert. Arch Microbiol 193:527–541

    Article  CAS  PubMed  Google Scholar 

  • Lopez BR, Tinoco-Ojanguren C, Bacilio M, Mendoza A, Bashan Y (2012) Endophytic bacteria of the rock-dwelling cactus Mammillaria fraileana affect plant growth and mobilization of elements from rocks. Environ Exp Bot 81:26–36

    Article  CAS  Google Scholar 

  • Macedo MO, Resende AS, Garcia PC, Boddey R, Jantalia CP, Urquiaga S, Campello EFC, Franco AA (2008) Changes in soil C and N stocks and nutrient dynamics 13 years after recovery of degraded land using leguminous nitrogen-fixing trees. Forest Ecol Manag 255:1516–1524

    Article  Google Scholar 

  • Marshall VM, Lewis MM, Ostendorf LB (2012) Buffel grass (Cenchrus ciliaris) as an invader and threat to biodiversity in arid environments: a review. J Arid Environ 78:1–12

    Article  Google Scholar 

  • Moore R, Russell R (1990) The ‘Three Norths’ forest protection system—China. Agroforest Syst 10:71–88

    Article  Google Scholar 

  • Nagy ML, Pérez A, Garcia-Pichel F (2005) The prokaryotic diversity of biological soil crusts in the Sonoran Desert (Organ Pipe Cactus National Monument, AZ). FEMS Microbiol Ecol 54:233–245

    Article  CAS  PubMed  Google Scholar 

  • Padilla FM, Pugnaire FI (2006) The role of nurse plants in the restoration of degraded environments. Front Ecol Environ 4:196–202

    Article  Google Scholar 

  • Perea MC, Ezcurra E, León de la Luz JL (2005) Functional morphology of a sarcocaulescent desert scrub in the Bay of La Paz, Baja California Sur, Mexico. J Arid Environ 62:413–426

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Peterjohn WT, Schlesinger WH (1990) Nitrogen loss from deserts in the southwestern United States. Biogeochemistry 10:67–79

    Article  Google Scholar 

  • Poly F, Monrozier LJ, Bally R (2001) Improvement in the RFLP procedure for studying the diversity of nifH genes in communities of nitrogen fixers in soil. Res Microbiol 152:95–103

    Article  CAS  PubMed  Google Scholar 

  • Ponder F, Tadros M (2002) Phospholipid fatty acids in forest soil four years after organic matter removal and soil compaction. Appl Soil Ecol 19:173–182

    Article  Google Scholar 

  • Posada D, Crandall KA (1998) MODELTEST: testing the model of DNA substitution. Bioinformatics 14:817–818

    Article  CAS  PubMed  Google Scholar 

  • Puente ME, Li CY, Bashan Y (2004) Microbial populations and activities in the rhizoplane of rock-weathering desert plants. II. Growth promotion of cactus seedlings. Plant Biol 6:643–650

    Article  CAS  PubMed  Google Scholar 

  • Puente ME, Li CY, Bashan Y (2009a) Rock-degrading endophytic bacteria in cacti. Environ Exp Bot 66:389–401

    Article  CAS  Google Scholar 

  • Puente ME, Li CY, Bashan Y (2009b) Endophytic bacteria in cacti seeds can improve the development of cactus seedlings. Environ Exp Bot 66:402–408

    Article  CAS  Google Scholar 

  • R Development Core Team (2008) R: A language and environment for statistical computing. R Foundation for Statistical Computing ISBN 3–900051–07–0., http://www.R-project.org

    Google Scholar 

  • Reed SC, Cleveland CC, Townsend AR (2011) Functional ecology of free-living nitrogen fixation: a contemporary perspective. Annu Rev Evol Syst 42:489–512

    Article  Google Scholar 

  • Requena N, Perez-Solis E, Azcón-Aguilar C, Jeffries P, Barea JM (2001) Management of indigenous plant-microbe symbioses aids restoration of desertified ecosystems. Appl Environ Microbiol 67:495–498

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Röling WFM (2007) Do microbial numbers count? Quantifying the regulation of biogeochemical fluxes by population size and cellular activity. FEMS Microbiol Ecol 62:202–210

    Article  PubMed  Google Scholar 

  • Ruiz-Jaen MC, Aide TM (2005) Restoration success: how is it being measured? Restor Ecol 13:569–577

    Article  Google Scholar 

  • Simonet P, Grosjean MC, Misra AK, Nazaret S, Cournoyer B, Normand P (1991) Frankia genus-specific characterization by polymerase chain reaction. Appl Environ Microbiol 57:3278–3286

    CAS  PubMed  PubMed Central  Google Scholar 

  • Simpson FB, Burris RH (1984) A nitrogen pressure of 50 atmospheres does not prevent evolution of hydrogen by nitrogenase. Science 224:1095–1097

    Article  CAS  PubMed  Google Scholar 

  • Solís-Domínguez FA, Valentín-Vargas A, Chorover J, Maier RM (2011) Effect of arbuscular mycorrhizal fungi on plant biomass and the rhizosphere microbial community structure of mesquite grown in acidic lead/zinc mine tailings. Sci Total Environ 409:1009–1016

    Article  PubMed  PubMed Central  Google Scholar 

  • Solórzano L (1969) Determination of ammonia in natural water by the phenolhypochlorite method. Limnol Oceanogr 14:799–801

    Article  Google Scholar 

  • Sprent JI, Gehlot HS (2010) Nodulated legumes in arid and semi-arid environments: are they important? Plant Ecolog Divers 3:211–219

    Article  Google Scholar 

  • Strickland JDH, Parsons TR (1972) A practical handbook of seawater analysis. Editorial Fisheries Research Board of Canada, Ottawa, No.167

    Google Scholar 

  • Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599

    Article  CAS  PubMed  Google Scholar 

  • Toledo G, Rojas A, Bashan Y (2001) Monitoring of black mangrove restoration with nursery-reared seedlings on an arid coastal lagoon. Hydrobiologia 444:101–109

    Article  Google Scholar 

  • Valentín-Vargas A, Chorover J, Maier RM (2013) A new standard-based polynomial interpolation (SBPIn) method to address gel-to-gel variability for the comparison of multiple denaturing gradient gel electrophoresis profile matrices. J Microbiol Methods 92:173–177

    Article  PubMed  PubMed Central  Google Scholar 

  • Venables WN, Ripley BD (2002) Modern Applied Statistics with S, 4th edn. Springer, New York

  • Vitousek PM, Cassman K, Cleveland C, Crews T, Field CB, Grimm NB, Howarth RW, Marino R, Martinelli L, Rastetter EB, Sprent JI (2002) Towards an ecological understanding of biological nitrogen fixation. Biogeochemistry 57(58):1–45

    Article  Google Scholar 

  • Vovides AG, Bashan Y, López-Portillo JA, Guevara R (2011) Nitrogen fixation in preserved, reforested, naturally regenerated and impaired mangroves as an indicator of functional restoration in mangroves in an arid region of Mexico. Restor Ecol 19:236–244

    Article  Google Scholar 

  • Yeager CM, Kornosky JL, Housman DC, Grote EE, Belnap J, Kuske CR (2004) Diazotrophic community structure and function in two successional stages of biological soil crusts from the Colorado Plateau and Chihuahuan Desert. Appl Environ Microbiol 70:973–983

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgments

We are grateful to personnel at CIBNOR: Manuel Moreno for assistance in sample collection and statistical analysis, Juan-Pablo Hernandez and Blanca López for their help with molecular, sequencing work, and logistic support; Luz de-Bashan for advice concerning DGGE, Jose-Luis Leon de la Luz for botanical advice; and Ira Fogel for English and editorial suggestions and at Benemérita Universidad Autónoma de Puebla: Lucía López Reyes and Guadalupe Medina de la Rosa for help and advice concerning gas chromatography. This study was supported by 2013 UC Mexus-CONACYT Collaborative Research Grant “Searching for bacteria living in the rhizosphere of native desert plants in the Sonoran Desert that restore soil fertility to degraded land in Baja California” and writing time for Y.B. provided by The Bashan Foundation, USA. N.E.L.L. is a recipient of a CONACYT postdoctoral fellowship (44810). This is contribution 2016-009 from the Bashan Institute of Science, USA.

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Authors and Affiliations

  1. Environmental Microbiology Group, The Northwestern Center for Biological Research (CIBNOR), Av. IPN 195, La Paz, B.C.S., 23096, Mexico

    Nguyen E. Lopez-Lozano & Yoav Bashan

  2. División de Ciencias Ambientales, Instituto Potosino de Investigación Científica y Tecnológica (IPICyT), Camino a la Presa San José 2055, Lomas 4ta. sección, San Luis Potosí, S.L.P., 78216, Mexico

    Nguyen E. Lopez-Lozano

  3. Laboratorio de Microbiología de Suelos, Centro de Investigaciones en Ciencias Microbiológicas, Benemérita Universidad Autónoma de Puebla, Edificio 103-E. Ciudad Universitaria, Puebla, Puebla, 72570, Mexico

    Moisés G. Carcaño-Montiel

  4. The Bashan Institute of Science, 1730 Post Oak Court, Auburn, AL, 36830, USA

    Yoav Bashan

  5. Department of Entomology and Plant Pathology, Auburn University, 301 Funchess Hall, Auburn, AL, 36849, USA

    Yoav Bashan

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  1. Nguyen E. Lopez-Lozano
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  2. Moisés G. Carcaño-Montiel
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  3. Yoav Bashan
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Correspondence to Yoav Bashan.

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Lopez-Lozano, N.E., Carcaño-Montiel, M.G. & Bashan, Y. Using native trees and cacti to improve soil potential nitrogen fixation during long-term restoration of arid lands. Plant Soil 403, 317–329 (2016). https://doi.org/10.1007/s11104-016-2807-3

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