Diazotrophic potential among bacterial communities associated with wild and cultivated Agave species

FEMS Microbiology Ecology

Volumn 90, Issue 3, 2014, Pages 844-857

  Desgarennes, Damaris ^a   Garrido, Etzel ^a,b   Torres Gomez, Miryam J ^a   Peña Cabriales, Juan J ^a   Partida Martinez, Laila P ^a  

^a DEPARTAMENTO DE FÍSICA   (Mexico)

^b Department of Obstetrics Gynecology   (United States)

Author keywords

Agaves; DGGE fingerprinting; Diazotrophic bacteria; Endophytes; Plant microorganism interactions

Indexed keywords

AGAVE; BACTERIA (MICROORGANISMS);

NITROGEN; RNA 16S; SOIL;

ACIDOBACTERIA; ACTINOBACTERIA; AGAVE; CHEMISTRY; CLASSIFICATION; DENATURING GRADIENT GEL ELECTROPHORESIS; DNA SEQUENCE; ECOSYSTEM; GENETICS; ISOLATION AND PURIFICATION; MICROBIAL CONSORTIUM; MICROBIOLOGY; NITROGEN FIXATION; NUCLEOTIDE SEQUENCE; PROTEOBACTERIA; SOIL;

ACIDOBACTERIA; ACTINOBACTERIA; AGAVE; BASE SEQUENCE; DENATURING GRADIENT GEL ELECTROPHORESIS; ECOSYSTEM; MICROBIAL CONSORTIA; NITROGEN; NITROGEN FIXATION; PROTEOBACTERIA; RNA, RIBOSOMAL, 16S; SEQUENCE ANALYSIS, DNA; SOIL; SOIL MICROBIOLOGY;

EID: 84914817053     PISSN: 01686496     EISSN: 15746941     Source Type: Journal    
DOI: 10.1111/1574-6941.12438     Document Type: Article

References (73)

1. Altschul SF, Gish W, Miller W, Myers EW & Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215: 403-410.
2. Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecol 26: 32-46.
3. Andrew DR, Fitak RR, Munguía-Vega A, Racolta A, Martinson VG & Dontsova K (2012) Abiotic factors shape microbial diversity in Sonoran desert soils. Appl Environ Microbiol 78: 7527-7537.
4. Arnold AE, Mejía LC, Kyllo D, Rojas EI, Maynard Z, Robbins N & Herre EA (2003) Fungal endophytes limit pathogen damage in a Tropical tree. P Natl Acad Sci USA 100: 15649-15654.
5. Berger WH & Parker FL (1970) Diversity of planktonic foraminifera in deep-sea sediments. Science 168: 1345-1347.
6. Bever JD, Platt TG & Morton ER (2012) Microbial population and community dynamics on plant roots and their feedbacks on plant communities. Annu Rev Microbiol 66: 265-283.
7. Bodenhausen N, Horton MW & Bergelson J (2013) Bacterial communities associated with the leaves and the roots of Arabidopsis thaliana. PLoS One 8: e56329.
8. Bondoso J, Balagué V, Gasol JM & Lage M (2014) Community composition of the Planctomycetes associated with different macroalgae. FEMS Microbiol Ecol 88: 445-456.
9. Bonfante P & Genre A (2008) Plants and arbuscular mycorrhizal fungi: an evolutionary-developmental perspective. Trends Plant Sci 13: 492-498.
10. Boom A, Sinninge-Damsté JS & de Leeuw JW (2005) Cutan, a common aliphatic biopolymer in cuticles of drought-adapted plants. Org Geochem 36: 595-601.
11. Brundrett MC (2002) Coevolution of roots and mycorrhizas of land plants. New Phytol 154: 275-304.
12. Camargo-Ricalde S, Dhillion SS & Jiménez-González C (2003) Mycorrhizal perennials of the Matorral Xerofilo and the Selva Baja Caducifolia communities in the semiarid Tehuacan-Cuicatlan Valley, Mexico. Mycorrhiza 13: 77-83.
13. Castanheira N, Dourado AC, Alves PI, Cortés-Pallero AM, Delgado-Rodríguez AI, Prazeres A, Borges N, Sánchez C, Barreto-Crespo MT & Fareleira P (2014) Annual ryegrass-associated bacteria with potential for plant growth promotion. Microbiol Res 169: 768-779.
14. Cheplick GP, Clay K & Marks S (1989) Interactions between infection by endophytic fungi and nutrient limitation in the grasses Lolium perenne and Festuca arundinacea. New Phytol 111: 89-97.
15. Clay K (1990) Fungal endophytes of grasses. Annu Rev Ecol Syst 2: 275-297.
16. Colunga-Garcia-Marin P, Larque-Saavedra A, Eguiarte LE & Zizumbo-Villarreal D (2007) En lo Ancestral hay Futuro: Del Tequila, los Mezcales y Otros Agaves, pp. 452. Centro de Investigación Científica de Yucatán A.C, Mexico.
17. Costa R, Götz M, Mrotzek N, Lottmann J, Berg G & Smalla K (2006) Effects of site and plant species on rhizosphere community structure as revealed by molecular analysis of microbial guilds. FEMS Microbiol Ecol 56: 236-249.
18. Csotonyi JT, Swiderski J, Stackebrandt E & Yurkov V (2010) A new environment for aerobic anoxygenic bacteria: biological soil crusts. Environ Microbiol Rep 2: 651-656.
19. Cui M & Nobel PS (1992) Nutrient status, water uptake and gas exchange for three desert succulents infected with mycorrhizal fungi. New Phytol 122: 643-649.
20. Deshmukh AP, Simpson AJ, Hadad CM & Hatcher PG (2005) Insights into the structure of cutin and cutan from Agave americana leaf cuticle using HRMAS NMR spectroscopy. Org Geochem 36: 1072-1085.
21. Edgar RC, Haas BJ, Clemente JC, Quince C & Knight R (2011) uchime improves sensitivity and speed of chimera detection. Bioinformatics 27: 2194-2200.
22. Edwards KJ (2001) Miniprep procedures for the isolation of plant DNA. Molecular Tools for Screening Biodiversity (Karp A, Issac PG & Ingram DS, eds), pp. 22-23. Kluwer Academic Publishers, Dordrecht.
23. Fürnkranz M, Wanek W, Richter A, Abell G, Rasche F & Sessitsch A (2008) Nitrogen fixation by phyllosphere bacteria associated with higher plants and their colonizing epiphytes of a tropical lowland rainforest of Costa Rica. ISME J 2: 561-570.
24. Garcia-Moya E, Romero-Manzanares A & Nobel PS (2011) Highlights for Agave productivity. Bioenergy 3: 4-14.
25. Gentry HS (1982) The Agaves of continental North America, pp. 670. The University of Arizona Press, Tucson.
26. Gottel RN, Castro HF, Kerley M et al. (2011) Distinct microbial communities within the endosphere and rhizosphere of Populus deltoides roots across contrasting soil types. Appl Environ Microbiol 77: 5934-5944.
27. Hardoim PR, Hardoim CCP, van Overbeek LS & van Elsas JD (2012) Dynamics of seed-borne rice endophytes on early plant growth stages. PLoS One 7: e30438.
28. 2 fixation: laboratory and field evaluation. Plant Physiol 43: 1185-1207.
29. Hill MO (1973) Diversity and evenness: a unifying notation and its consequences. Ecology 54: 427-432.
30. Huang Y, Niu B, Gao Y, Fu L & Li W (2010) cd-hit suite: a web server for clustering and comparing biological sequences. Bioinformatics 26: 680-682.
31. Kiers ET & Denison RF (2008) Sanctions, cooperation, and the stability of plant-rhizosphere mutualisms. Annu Rev Ecol Evol Syst 39: 215-236.
32. Kim SJ, Ahn JH, Lee TH, Weon HY, Hong SB, Seok SJ, Whang KS & Kwon SW (2013) Reyranella soli sp. nov., isolated from forest soil, and emended description of the genus Reyranella Pagnier et al., 2011. Int J Syst Evol Microbiol 63: 3164-3167.
33. Kindt R & Code R (2005) Tree Diversity Analysis: A Manual and Software for Common Statistical Methods for Ecological and Biodiversity Studies, pp. 196. World Agroforestry Centre (ICRAF), Nairobi.
34. Kneip C, Lockhart P, Voß C & Maier UG (2007) Nitrogen fixation in eukaryotes - New models for symbiosis. BMC Evol Biol, 7 Available: http://www.biomedcentral.com/1471-2148/7/55. Accessed 20 March 2014.
35. Köberl M, Müller H, Ramadan EM & Berg G (2011) Desert farming benefits from microbial potential in arid soils and promotes diversity and plant health. PLoS One 6: e24452.
36. Lee JC & Whang KS (2014) Reyranella graminifolii sp. nov., isolated from bamboo (Phyllostachys bambusoides) litter. Int J Syst Evol Microbiol 64: 2503-2507.
37. Li W & Godzik A (2006) cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics 22: 1658-1659.
38. Lottmann J, O'Callagham M, Baird D & Walter C (2010) Bacterial and fungal communities in the rhizosphere of field-grown genetically modified pine trees (Pinus radiata D.). Environ Biosafety Res 9: 25-40.
39. Lundberg DS, Lebeis SL, Herrera-Paredes S et al. (2012) Defining the core Arabidopsis thaliana root microbiome. Nature 488: 86-90.
40. Maidak BL, Cole JR, Lilburn TG, Parker CT, Saxman PR, Farris RJ, Garrity GM, Olsen GJ, Schmidt TM & Tiedje JM (2001) The RDP-II (ribosomal database project). Nucleic Acids Res 29: 173-174.
41. Mancilla-Margalli NA & Lopez MG (2006) Water-soluble carbohydrates and fructan structure patterns from Agave and Dasylirion species. J Agric Food Chem 54: 7832-7839.
42. Manly BF (1986) Multivariate Statistical Methods: A Primer, pp. 159. Chapman and Hall, Ltd, London.
43. Marasco R, Rolli E, Ettoumi B, et al. (2012) A drought resistance-promoting microbiome is selected by root system under desert farming. PLoS One 7: e48479.
44. Martinez-Romero E (2009) Coevolution in Rhizobium-Legume symbiosis? DNA Cell Biol 28: 361-370.
45. Martinez-Salvador M, Mata-Gonzalez R, Morales-Nieto C & Valdez-Cepeda R (2012) Agave salmiana plant communities in central Mexico as affected by commercial use. Environ Manage 49: 55-63.
46. Mellado-Mojica E & Lopez MG (2012) Fructan metabolism in A. tequilana Weber blue variety along its developmental cycle in the field. J Agric Food Chem 60: 11704-11713.
47. Mendes LW, Kurame EE, Navarrete AA, van Veen JA & Tsai SM (2014) Taxonomical and functional microbial community selection in soybean rhizosphere. ISME J 8: 1577-1587.
48. Nobel PS (2003) Environmental Biology of Agaves and Cacti, pp. 270. Cambridge University Press, Cambridge.
49. Nocker A, Burr M & Camper A (2007) Genotypic microbial community profiling: a critical technical review. Microb Ecol 54: 276-289.
50. North GB, Brinton EK & Garrett TY (2008) Contractile roots in succulent monocots: convergence, divergence and adaptation to limited rainfall. Plant, Cell Environ 31: 1179-1189.
51. Obledo EN, Barragán-Barragán LB, Gutiérrez-González P, Ramírez-Hernández BC, Ramírez JJ & Rodríguez-Garay B (2003) Increased photosynthetic efficiency generated by fungal symbiosis in Agave victoria-reginae. Plant Cell Tissue Organ Cult 74: 237-241.
52. Oksanen J, Guillaume-Blanchet F, Kindt R et al. (2013) vegan: community ecology package. R package, version 2.0-9. http://CRAN.R-project.org/package=vegan.
53. Oldroyd GE & Downie JA (2008) Coordinating nodule morphogenesis with rhizobial infection in Legumes. Annu Rev Plant Biol 59: 519-546.
54. Pagnier I, Raoult D & La Scola B (2011) Isolation and characterization of Reyranella massiliensis gen. nov., sp. nov. from fresh water samples by using an amoeba co-culture procedure. Int J Syst Evol Microbiol 61: 2151-2154.
55. Partida-Martinez LP & Heil M (2011) The microbe-free plant: fact or artifact? Front Plant Sci 2: 100.
56. Peiffer JA, Spor A, Koren O, Jin Z, Tringe SG, Dangl JL, Buckler ES & Ley RE (2013) Diversity and heritability of the maize rhizosphere microbiome under field conditions. P Natl Acad Sci USA 110: 6548-6553.
57. Pimienta-Barrios E, Zañudo-Hernández J & López-Alcocer E (2009) Efecto de las micorrizas arbusculares en el crecimiento, fotosíntesis y anatomía foliar de plantas jóvenes de Agave tequilana. Acta Bot Mex 89: 63-78.
58. Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, Peplies J & Glockner FO (2013) The silva ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res 41: 590-596.
59. Quinn GP & Keough MJ (2002) Experimental Design and Data Analysis for Biologists, pp. 537. Cambridge University Press, New York, NY.
60. R Core Team (2013) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/.
61. Ravenscroft N, Cescutti P, Hearshaw MA, Ramsout R, Rizzo R & Timme EM (2009) Structural analysis of fructans from Agave americana grown in South Africa for spirit production. J Agric Food Chem 57: 3995-4003.
62. Redecker D, Kodner R & Graham LE (2000) Glomalean fungi from the Ordovician. Science 289: 1920-1921.
63. Remy W, Taylor TN, Hass H & Kerp H (1994) Four hundred-million-year-old vesicular arbuscular mycorrhizae. P Natl Acad Sci USA 91: 11841-11843.
64. Rennie RJ (1981) A single medium for the isolation of acetylene-reducing (dinitrogenfixing) bacteria from soils. Can J Microbiol 27: 8-14.
65. Rodriguez RJ, Henson J, van Volkenburgh E, Hoy M, Wright L, Beckwith F, Kim YO & Redman RS (2008) Stress tolerance in plants via habitat-adapted symbiosis. ISME J 2: 404-416.
66. Rodriguez RJ, Freeman DC, McArthur ED, Kim YO & Redman RS (2009) Symbiotic regulation of plant growth, development and reproduction. Commun Integr Biol 2: 141-143.
67. Rogel MA, Ormeño-Orrillo E & Martinez-Romero E (2011) Symbiovars in Rhizobia reflect bacterial adaptation to Legumes. Syst Appl Microbiol 34: 96-104.
68. Ruiz S, Adriano L, Ovando I, Navarro C & Salvador M (2011) Biofertilization of micropropagated Agave tequilana: effect on plant growth and production of hydrolytic enzymes. Afr J Biotechnol 10: 9631-9639.
69. Shade A & Handelsman J (2012) Beyond the Venn diagram: the hunt for a core microbiome. Environ Microbiol 14: 4-12.
70. Shakya M, Gottel N, Castro H et al. (2013) A multifactor analysis of fungal and bacterial community structure in the root microbiome of mature Populus deltoides trees. PLoS One 8: e76382.
71. Valenzuela A (2011) A new agenda for blue Agave landraces: food, energy and tequila. Bioenergy 3: 15-24.
72. Venables WN & Ripley BD (2002) Modern Applied Statistics with S, pp. 497. Springer, New York, NY.
73. Winogradsky S (1935) The method in soil microbiology as illustrated by studies on Azotobacter and the nitrifying organisms. Soil Sci 40: 59-76.