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Bacterial community structure in the rhizosphere of three cactus species from semi-arid highlands in central Mexico

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Abstract

The nature reserve of Tehuacan-Cuicatlan in central Mexico is known for its diversity and endemism mainly in cactus plants. Although the xerophytic flora is reasonably documented, the bacterial communities associated with these species have been largely neglected. We assessed the diversity and composition of bacterial communities in bulk (non-rhizospheric) soil and the rhizosphere of three cactus plant species: Mammillaria carnea, Opuntia pilifera and Stenocereus stellatus, approached using cultivation and molecular techniques, considering the possible effect of dry and rainy seasons. Cultivation-dependent methods were focused on putative N2-fixers and heterotrophic aerobic bacteria, in the two media tested the values obtained for dry season samples grouped together regardless of the sample type (rhizospheric or non-rhizospheric), these groups also included the non-rhizospheric sample for rainy season, on each medium. These CFU values were smaller and significantly different from those obtained on rhizospheric samples from rainy season. Genera composition among isolates of the rhizospheric samples was very similar for each season, the most abundant taxa being α-Proteobacteria, Actinobacteria and Firmicutes. Interestingly, the genus Ochrobactrum was highly represented among rhizospheric samples, when cultured in N-free medium. The structure of the bacterial communities was approached with molecular techniques targeting partial 16S rRNA sequences such as denaturing gradient gel electrophoresis and serial analysis of ribosomal sequence tags. Under these approaches, the most represented bacterial phyla were Actinobacteria, Proteobacteria and Acidobacteria. The first two were also highly represented when using isolation techniques.

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References

  • Bachar A, Al-Ashhab A, Soares MI, Sklarz MY, Angel R, Ungar ED, Gillor O (2010) Soil microbial abundance and diversity along a low precipitation gradient. Microb Ecol 60:453–461

    Article  PubMed  Google Scholar 

  • Bais HP, Weir TL, Perry LG, Gilroy S, Vivanco JM (2006) The role of root exudates in rhizosphere interactions with plants and other organisms. Annu Rev Plant Biol 57:234–266

    Article  Google Scholar 

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

    CAS  Google Scholar 

  • Berg G, Smalla K (2009) Plant species and soil type cooperatively shape the structure and function of microbial communities in the rhizosphere. FEMS Microbiol Ecol 68:1–13

    Article  PubMed  CAS  Google Scholar 

  • Caballero JM, Onofre J, de los Santos P, Martinez L (2007) The tomato rhizosphere, an environment rich in nitrogen-fixing burkholderia species with capabilities of interest for agriculture and bioremediation. Appl Environ Microbiol 73:5308–5319

    Article  Google Scholar 

  • Carrillo-García A, Bashan Y, Díaz-Rivera E, Bethlenfalvay GJ (2000) Effects of resource-islands 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 

  • Casas A, Barbera G (2002). Mesoamerican domestication and diffusion. In: Park S Nobel (ed) Cacti: Biology and uses, University of California Press. USA, pp 143–162

  • Chakraborty U, Chakraborty BN, Basnet M, Chakraborty AP (2009) Evaluation of Ochrobactrum anthropi TRS-2 and its talc based formulation for enhancement of growth of tea plants and management of brown root rot disease. J Appl Microbiol 107:625–634

    Article  PubMed  CAS  Google Scholar 

  • Chanal A, Chapon V, Benzerara K, Barakat M, Christen R, Achouak W, Barras F, Heulin T (2006) The desert of Tataouine: an extreme environment that hosts a wide diversity of microorganisms and radiotolerant bacteria. Environ Microbiol 8:514–525

    Article  PubMed  CAS  Google Scholar 

  • Chun J, Lee JH, Jung Y, Kim M, Kim S, Kim BK, Lim YW (2007) EzTaxon: a web-based tool for the identification of prokaryotes based on 16S ribosomal RNA gene sequences. Int J Syst Evol Microbiol 57:2259–2261

    Article  PubMed  CAS  Google Scholar 

  • Dávila P, Arizmendi M, Valiente-Banuet A, Villaseñor J, Casas A, Lira R (2002) Biological diversity in the Tehuacan-Cuicatlan valley. Mex Biodivrs Conserv 11:421–442

    Article  Google Scholar 

  • Enge K, Whiteford S (1989) The keepers of water and earth: Mexican rural social organization and irrigation, pp 179–222. University of Texas Press, Austin

    Google Scholar 

  • Felsenstein J. (1993). Phylip (Phylogeny Inference Package) version 3.57c. Dept. of Genetics, University of Washington, Seattle. http://evolution.genetics.washington.edu/phylip.html

  • Felske A, Engelen B, Nübel U, Backhaus H (1996) Direct ribosome isolation from soil to extract bacterial rRNA for community analysis. Appl Environ Microbiol 62:4162–4167

    PubMed  CAS  Google Scholar 

  • Haichar FE, Marol C, Berge O, Rangel-Castro JI, Prosser JI, Balesdent J, Heulin T, Achouak W (2008) Plant host habitat and root exudates shape soil bacterial community structure. ISME J 2:1221–1230

    Article  PubMed  CAS  Google Scholar 

  • Herman RP, Provencio K, Torrez R, Seager GM (1994) Seasonal and spatial population dynamics of the nitrogen-efficient guild in a desert Baja grassland. Appl Environ Microbiol 60:1160–1165

    PubMed  CAS  Google Scholar 

  • Holland S (2003) Analytic Rarefaction. http://www.uga.edu/strata/software/index.html

  • Huber T, Faulkner G, Hugenholtz P (2004) Bellerophon; a program to detect chimeric sequences in multiple sequence alignments. Bioinformatics 20:2317–2319

    Article  PubMed  CAS  Google Scholar 

  • Instituto Nacional de Estadística, Geografía e Informática (2005) Carta Topográfica, 1:250,000. Oaxaca, E 14–9. (INEGI). www.inegi.org.mx

  • Jones K, Bangs D (1985) Nitrogen fixation by free living heterotrophic bacteria in oak forest: the effect of liming. Soil Biol Biochem 17:705–709

    Article  CAS  Google Scholar 

  • Kempers AJ (1974) Determination of sub-microquantities of ammonium and nitrates in soils with phenol, sodium nitroprusside and hypochlorite. Geoderma 12:201–206

    Article  CAS  Google Scholar 

  • Kumar S, Dudley J, Nei M, Tamura K (2008) MEGA: a biologist-centric software for evolutionary analysis of DNA and protein sequences. Brief Bioinform 9:299–306

    Article  PubMed  CAS  Google Scholar 

  • Kysela DT, Palacios C, Sogin ML (2005) Serial analysis of V6 ribosomal sequence tags (SARST-V6): a method for efficient, high-throughput analysis of microbial community composition. Environ Microbiol 7:356–364

    Article  PubMed  CAS  Google Scholar 

  • Lebuhn M, Achouak W, Schloter M, Berge O, Meier H, Barakat M, Hartmann A, Heulin T (2000) Taxonomic characterization of Ochrobactrum sp. isolates from soil samples and wheat roots, and description of Ochrobactrum tritici sp. nov. and Ochrobactrum grignonense sp. nov. Int J Syst Evol Microbiol 50:2207–2223

    Article  PubMed  CAS  Google Scholar 

  • López-Galindo F, Muñoz-Iniestra D, Hernández-Moreno M, Soler-Aburto A, Castillo López MC, Hernández-Arzate I (2003) Análisis integral de la toposecuencia y su influencia en la distribución de la vegetación y la degradación del suelo en la subcuenca de Zapotitlán de las Salinas, Puebla. Boletín de la Sociedad Geológica Mexicana LVI, pp 19–41

  • Mnasri B, Tajini F, Trabelsi M, Aouani ME, Mhamdi R (2007) Rhizobium gallicum as an efficient symbiont for bean cultivation. Agron Sustain Dev 27:331–336

    Article  CAS  Google Scholar 

  • Muyzer G, Brinkhoff T, Nübel U, Santegoeds C, Schäfer H, Wawer C (1998) Denaturing Gradient Gel Electrophoresis (DGGE) in Microbial Ecology. Chap. 3.4.4. In: Akkermans ADL, van Elsas JD, de Bruijn FJ (eds) Molecular Microbial Ecology Manual. Kluwer Academic Publishers, Dordrecht, pp 1–27

    Google Scholar 

  • Ngom A, Nakagawa Y, Sawada H, Tsukahara J, Wakabayashi S, Uchiumi T, Nuntagij A, Kotepong S, Suzuki A, Higashi S, Abe M (2004) A novel symbiotic nitrogen-fixing member of the Ochrobactrum clade isolated from root nodules of Acacia mangium. J Gen Appl Microbiol 50:17–27

    Article  PubMed  CAS  Google Scholar 

  • Nunan N, Daniell TJ, Singh BK, Papert A, McNicol JW, Prosser JI (2005) Links between plant and rhizoplane bacterial communities in grassland soils, characterized using molecular techniques. Appl Environ Microbiol 71:6784–6792

    Article  PubMed  CAS  Google Scholar 

  • Príncipe A, Alvarez F, Castro MG, Zachi L, Fischer SE, Mori GB, Jofr E (2007) Biocontrol and PGPR features in native strains isolated from saline soils of Argentina. Curr Microbiol 55:314–322

    Article  PubMed  Google Scholar 

  • Puente ME, Bashan Y (1993) Effect of inoculation with Azospirillum brasilense strains on the germination and seedlings growth of the giant columnar Cardon cactus (Pachycereus pringlei). Symbiosis 15:49–60

    Google Scholar 

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

    Article  CAS  Google Scholar 

  • Ramírez-Saad H, Akkermans W, Akkermans ADL (1996) DNA Extraction from Actinorhizal Nodules. Chap. 1.4.4. In: Manual Molecular Microbial Ecology, Akkermans ADL, van Elsas JD, de Bruijn F (eds) Kluwer Academic Publishers. The Netherlands, Dordrecht, pp 1–11

    Google Scholar 

  • Ramírez-Saad HC, Janse J, Akkermans ADL (1998) Root nodules of Ceanothus caeruleus contain both the N2-fixing Frankia endophyte and a phylogenetically related Nod-/Fix-actinomycete. Can J Microbiol 44:140–148

    Google Scholar 

  • Ramírez-Saad HC, Sessitsch A, de Vos WM, Akkermans ADL (2000) Bacterial community changes and enrichment of uncultured Burkholderia-like bacteria induced by chlorinated benzoates in a Peat-forest soil-microcosm. Syst Appl Microbiol 23:591–598

    Article  PubMed  Google Scholar 

  • Recagno E (2001) Conocimiento y conservación de las Mamilarias endémicas del valle de Tehuacán-Cuicatlán. Informe de Proyecto R166, CONABIO, Mexico pp 3–7

  • Rennie RJ (1981) A single medium for the isolation of acetylene reducing (dinitrogen fixing) bacteria from soil. Can J Microbiol 27:8–14

    Article  PubMed  CAS  Google Scholar 

  • Ros M, Pascual JA, Moreno JL, Hernandez MT, Garcia C (2009) Evaluation of microbial community activity, abundance and structure in a semiarid soil under cadmium pollution at laboratory level. Water Air Soil Pollut 203:229–242

    Article  CAS  Google Scholar 

  • Rosselló-Mora R, Aman R (2001) The species concept for prokaryotes. FEMS Microbiol Rev 25:39–67

    Article  PubMed  Google Scholar 

  • Rzedowski J (1991) Diversidad y orígenes de la flora fanerogámica de México. Acta Bot Mex 14:3–21

    Google Scholar 

  • Sanguinetti CJ, Dias Nieto E, Simpson AJG (1994) Rapid silver staning and recovery of PCR products separated on polyacrilamyde gels. Biotechniques 17:915–919

    Google Scholar 

  • Schloss PD, Larget BR, Handelsman J (2004) Integration of microbial ecology and statistics: a test to compare gene libraries. Appl Environ Microbiol 70:5485–5492

    Article  PubMed  CAS  Google Scholar 

  • Singleton DR, Furlong MA, Rathbun SL, Whitman WB (2001) Quantitative comparison of 16S rRNA gene sequence libraries from enviromental samples. Appl Environ Microbiol 67:4374–4376

    Article  PubMed  CAS  Google Scholar 

  • Sliwinski MK, Goodman RM (2003) Comparison of Crenarchaeal consortia inhabiting the rhizosphere of diverse terrestrial plants with those in bulk soil in native environments. Appl Environ Microbiol 70:1821–1826

    Article  Google Scholar 

  • Smalla K, Wieland G, Buchner A, Zock A, Parzy J, Kaiser S, Roskot N, Heuer H, Berg G (2001) Bulk and rhizosphere soil bacterial communities studied by denaturing gradient gel electrophoresis: plant-dependent enrichment and seasonal shifts revealed. Appl Environ Microbiol 67:4742–4751

    Article  PubMed  CAS  Google Scholar 

  • Somers E, Vanderleyden J, Srinivisam M (2004) Rhizosphere bacterial signaling: a love parade beneath our feet. Crit Rev Microbiol 30:205–240

    Article  PubMed  CAS  Google Scholar 

  • Stotzky G (1997) Soil as an Environment for Microbial Life. In: Van Elsas JD, Trevors JT, Wellington EMH (eds) Modern Soil Microbiology, pp 1–20. Marcel Dekker Inc, New York

    Google Scholar 

  • Tripathi AK, Verma SC, Chowdhury SP, Lebuhn M, Gattinger A, Schloter M (2006) Ochrobactrum oryzae sp. nov., an endophytic bacterial species isolated from deep-water rice in India. Int J Syst Evol Microbiol 56:1677–1680

    Article  PubMed  CAS  Google Scholar 

  • Trubat R, Cortina J, Vilagrosa A (2010) Nursery fertilization affects seedling traits but not field performance in Quercus suber L. J Arid Environ 74:491–497

    Article  Google Scholar 

  • Trujillo ME, Willems A, Abril A, Planchuelo AM, Rivas R, Ludeña D, Mateos PF, Martínez-Molina E, Velázquez E (2005) Nodulation of Lupinus albus by strains of Ochrobactrum lupini sp. nov. Appl Environ Microbiol 71:1318–1327

    Article  PubMed  CAS  Google Scholar 

  • Yechieli A, Oren A, Yair A (1995) The effect of water distribution on bacterial numbers and microbial activity along a hill slope, northern Negev. Isr Adv Geoecol 28:193–207

    Google Scholar 

  • Zhang Z, Schwartz S, Wagner L, Miller W (2000) A greedy algorithm for aligning DNA sequences. J Comput Biol 7:203–214

    Article  PubMed  CAS  Google Scholar 

  • Zurdo-Piñeiro JL, Rivas R, Trujillo ME, Vizcaíno N, Carrasco JA, Chamber M, Palomares A, Mateos PF, Martínez-Molina E, Velázquez E (2007) Ochrobactrum cytisi sp. nov., isolated from nodules of Cytisus scoparius in Spain. Int J Syst Evol Microbiol 57:784–788

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

This work received financial support from Foundation BBVA, trough project BIOCON 04-084. F.A.G. received fellowships from CONACyT and COMECyT (Mexico), for PhD studies.

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Correspondence to Hugo C. Ramírez-Saad.

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Aguirre-Garrido, J.F., Montiel-Lugo, D., Hernández-Rodríguez, C. et al. Bacterial community structure in the rhizosphere of three cactus species from semi-arid highlands in central Mexico. Antonie van Leeuwenhoek 101, 891–904 (2012). https://doi.org/10.1007/s10482-012-9705-3

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