Desiccation-Tolerant Rhizobacteria Maintain their Plant Growth- Promoting Capability after Experiencing Extreme Water Stress

Bacteria from rhizosphere have the potential to promote the growth of plants, and could be used as inoculants to increase the crop profitability. However, under drought stress conditions, the number of bacteria associated to seeds could decrease below the minimal number of bacteria required to obtain a positive plant response. At the present work, the capability of 28 rhizospheric bacterial strains to tolerate 18 days of air desiccation stress (at 30oC and 50% of relative humidity) was evaluated. Results showed different levels of bacterial tolerance and five categories were proposed based on the bacterial survival ratio to air desiccation (BSRad): highly tolerant bacteria (BSRad˃80), tolerant (60 (40 bacteria were selected to inoculate maize seeds. After inoculation, seeds were subjected to desiccation conditions for 18 days and then sown in sterile vermiculite and watered with MS solution. Only highly tolerant strains were able to survive associated to seeds under desiccation conditions keeping their beneficial traits such as, bacterial adherence, colonization and plant growth promotion. In contrast, the very-low tolerant bacterial strain was not able to colonize the rhizosphere nor promote the growth of the plants. Tolerant bacteria to desiccation have desirable traits in comparison to non-tolerant bacteria, because they could be more stable in powder presentations of inoculants without need of protectants, they could survive with higher numbers in soils with low water availability keeping their ability to promote the plant-growth until the end of adverse conditions; when the seed germination take place.
{"references":["Morales-García Y-E, Duque E, Rodríguez-Andrade O, et al. (2010) Bacterias preservadas, una fuente importante de recursos biotecnológicos. Bio Tecnol 14:11-29.","Lin W, Bazylinski DA, Xiao T, et al. (2014) Life with compass: diversity and biogeography of magnetotactic bacteria. Environ Microbiol 16: 2646-2658.","Pace NR (1997) A molecular view of microbial diversity and the biosphere. Science 276: 734-740.","Strom SL (2008) Microbial ecology of ocean biogeochemistry: a community perspective. Science 320: 1043-1045.","de Bruijn FJ (2015) Biological Nitrogen Fixation BTPrinciples of Plant-Microbe Interactions: Microbes for Sustainable Agriculture. In: Lugtenberg B editor Cham: Springer International Publishing 215-224.","Lugtenberg B, Kamilova F (2009) Plant-Growth-Promoting Rhizobacteria. Annu Rev Microbiol 63: 541-556.","Glick BR, Glick BR (2012) Plant growth-promoting bacteria: Mechanisms and Applications. Scientifica (Cairo) 1-15.","Kuiper I, Lagendijk EL, Bloemberg G V, et al. (2004) Rhizoremediation : A Beneficial Plant-Microbe Interaction. Mol Plant Microb Int 17: 6-15.","Gerhardt KE, Huang XD, Glick BR, et al. (2009) Phytoremediation and rhizoremediation of organic soil contaminants: Potential and challenges. Plant Sci 176: 20-30.","Beneduzi A, Ambrosini A, Passaglia LMP (2012) Plant growth-promoting rhizobacteria (PGPR): Their potential as antagonists and biocontrol agents. Genet Mol Biol 35: 1044- 1051.","Pieterse CMJ, Zamioudis C, Berendsen RL, et al. (2014) Induced Systemic Resistance by Beneficial Microbes. Annu Rev Phytopathol 52: 347-375.","Wu L, Wu HJ, Qiao J, et al. (2015) Novel routes for improving biocontrol activity of Bacillus based bioinoculants. Front Microbiol 6: 1-13.","Chemier JA, Fowler ZL, Koffas MAG, et al. (2009) Trends in microbial synthesis of natural products and biofuels. Adv Enzymol Relat Areas Mol Biol 76: 151-217.","Leroy F, De Vuyst L (2004) Lactic acid bacteria as functional starter cultures for the food fermentation industry. Trends Food Sci Technol 15: 67-78.","Chookietwattana K, Maneewan K (2012) Selection of efficient salt-tolerant bacteria containing ACC deaminase for promotion of tomato growth under salinity stress. Soil Environ 31: 30-36.","He H, Chen Y, Li X, et al. (2017) Influence of salinity on microorganisms in activated sludge processes: A review. Int Biodeterior Biodegradation 119: 520–527.","Khan MY, Zahir ZA, Naeem AH, et al. (2017) Preliminary investigations on selection of synergistic halotolerant plant growth promoting rhizobacteria for inducing salinity tolerance in wheat. Pak J Bot 49: 1541-1551.","Molina-Romero D, Baez A, Quintero-Hernández V, et al. (2017) Compatible bacterial mixture, tolerant to desiccation, improves maize plant growth. PLoS One 12: 0187913.","Vilchez S, Manzanera M (2011) Biotechnological uses of desiccation-tolerant microorganisms for the rhizoremediation of soils subjected to seasonal drought. Appl Microbiol Biotechnol 91: 1297.","Streeter JG (2003) Effect of trehalose on survival of Bradyrhizobium japonicum during desiccation. J Appl Microbiol 95: 484-491.","Casteriano A, Wilkes MA, Deaker R (2013) Physiological changes in rhizobia after growth in peat extract may. Appl Environ Microbiol 79: 3998-4007.","Chang W, Mortel M Van De, et al. (2007) Alginate production by Pseudomonas putida creates a hydrated microenvironment and contributes to biofilm architecture and stress tolerance under water-limiting conditions. J Bacteriol 189: 8290-8299.","Mortel M Van De, Chang W-S, Halverson LJ (2005) Differential tolerance of Pseudomonas putida biofilm and planktonic cells to desiccation. Biofilms 1: 361-368.","Sandhya V, Grover M, Reddy G, et al. (2009) Alleviation of drought stress effects in sunflower seedlings by the exopolysaccharides producing Pseudomonas putida strain GAP-P45. Biol Fertil Soils 46: 17-26.","Alpert P (2005) The limits and frontiers of desiccationtolerant life. Integr Comp Biol 45: 685-695.","Potts M (1994) Desiccation tolerance of prokaryotes. Microbiol Mol Biol Rev 58: 755-805.","Danks H V (2000) Dehydration in dormant insects. J Insect Physiol 46: 837-852.","Potts M (2001) Desiccation tolerance: a simple process? Trends Microbiol 9: 553-559.","Morales YE, Juárez D, Aragón C, et al. (2011) Growth response of maize plantlets inoculated with Enterobacter spp as a model for alternative agriculture. Rev Argent Microbiol 43: 287-293.","Reis VM, Estrada de los Santos P, Vogel J, et al. (2004) Burkholderia tropica sp. Nov a novel nitrogen-fixing, plantassociated bacterium. Int J Syst Evol Microbiol 54: 2155-2162.","Caballero-Mellado J, Martínez-Aguilar L, Paredes-Valdez G, et al. (2004) Burkholderia unamae sp. nov., an N2-fixing rhizospheric and endophytic species. Int J Syst Evol Microbiol 54: 1165-1172.","Perin L, Martínez-Aguilar L, Paredes-Valdez G, et al. (2006) Burkholderia silvatlantica sp. nov., a diazotrophic bacterium associated with sugar cane and maize. Int J Syst Evol Microbiol 56:1931-1937.","Baldani J, Caruso L, Baldani VLD, et al. (1997) Recent advances in BNF with non-legume plants. Soil Biol Biochem 29: 911-922.","Reinhold B, Hurek T, Fendrik I, et al. (1987) Azospirillum halopraeferens sp Nov, a nitrogen-fixing organism associated with roots of Kallar Grass (Leptochloa fusca Kunth). Int J Syst Evol Microbiol 37: 43-51.","Böltner D, Godoy P, Muñoz-Rojas J, et al. (2008) Rhizoremediation of lindane by root-colonizing Sphingomonas. Microb Biotechnol 1: 87-93.","Rosenblueth M, Martínez L, Silva J, et al. (2004) A novel species with clinical and plant-associated isolates. Syst Appl Microbiol 27: 27-35.","Nakazawa T (2002) Travels of a Pseudomonas, from Japan around the world. Environ Microbiol 4: 782-786.","Ramos-González M-I, Godoy P, Alaminos M, et al. (2001) Physiological Characterization of Pseudomonas putida DOTT1E Tolerance top-Hydroxybenzoate. Appl Environ Microbiol 67: 4338–4341.","Muñoz-Rojas J, Caballero-Mellado J (2003) Population Dynamics of Gluconacetobacter diazotrophicus in sugarcane cultivars and its effect on plant growth. Microb Ecol 46: 454- 464.","Fuentes-Ramírez LE, Caballero-Mellado J, Sepúlveda J, et al. (1999) Colonization of sugarcane by Acetobacter diazotrophicus is inhibited by high N-fertilization. FEMS Microbiol Ecol 29: 17-128","Rodríguez-Cáceres EA (1982) Improved Medium for Isolation of Azospirillum spp. Appl Environ Microbiol 44: 990- 1001","Muñoz-Rojas J, Fuentes-Ramírez LE, Caballero-Mellado J (2005) Antagonism among Gluconacetobacter diazotrophicus strains in culture media and in endophytic association. FEMS Microbiol Ecol 54: 57-66.","Muñoz-Rojas J, Bernal P, Duque E, et al. (2006) Involvement of cyclopropane fatty acids in the response of Pseudomonas putida KT2440 to freeze-drying. Appl Environ Microbiol 72: 472-7.","Corral-Lugo A, Morales-García YE, Pazos-Rojas LA, et al. (2012) Cuantificación de bacterias cultivables mediante el método de \"Goteo en Placa por Sellado (o estampado) Masivo\". Rev Col Biotecnol 14: 147-56.","Rojas-Tapias D, Ortiz-Vera M, Rivera D, et al. (2013) Evaluation of three methods for preservation of Azotobacter chroococcum and Azotobacter vinelandii. Univ Sci 18: 129-139.","Figueredo F, Abrevaya XC, Cortón E (2015) A new P. putida instrumental toxicity bioassay. Environ Monit Assess 187: 1–13.","Chiselita O, Svetlana B, Bîrsa M, et al. (2016) Viability and antimicrobial activity of Streptomyces strains from NCNM after lyophilization. Stud Univ Mold 1: 61-71.","Rodríguez-Andrade O, Fuentes-Ramírez LE, Morales- García YE, et al. (2015) The decrease in the population of Gluconacetobacter diazotrophicus in sugarcane after nitrogen fertilization is related to plant physiology in split root experiments. Rev Argentina Microbiol 47: 335-343.","Rainey FA, Ray K, Ferreira M, et al. (2005) Extensive diversity of ionizing-radiation-resistant bacteria recovered from Sonoran Desert soil and description of nine new species of the genus Deinococcus obtained from a single soil sample. Appl Environ Microbiol 71: 5225-5235.","Ramadoss D, Lakkineni VK, Bose P, et al. (2013) Mitigation of salt stress in wheat seedlings by halotolerant bacteria isolated from saline habitats. Springerplus 2: 6.","Miyamoto-Shinohara Y, Sukenobe J, Imaizumi T, et al. (2008) Survival of freeze-dried bacteria. J Gen Appl Microbiol 54: 9-24.","Baez-Rogelio A, Morales-García YE, Quintero-Hernández V, et al. (2017) Next generation of microbial inoculants for agriculture and bioremediation. Microb Biotechnol 10: 19-21.","van Ham R, O'Callaghan M, Geurts R, et al. (2016) Soil moisture deficit selects for desiccation tolerant Rhizobium leguminosarum bv. trifolii. Appl Soil Ecol 108: 371-380.","Velázquez-Hernández ML, Baizabal-Aguirre VM, Cruz- Vázquez F et al. (2011) Gluconacetobacter diazotrophicus levansucrase is involved in tolerance to NaCl, sucrose and desiccation, and in biofilm formation. Arch Microbiol 193: 137- 149.","Alpert P (2006) Constraints of tolerance : why are desiccationtolerant organisms so small or rare ? J Exp Biol 209: 1575-1584.","Elliott J, Deryng D, Müller C, et al. (2014) Constraints and potentials of future irrigation water availability on agricultural production under climate change. Proc Natl Acad Sci 111: 3239- 3244.","Talbi C, Sánchez C, Hidalgo-Garcia A, et al. (2012) Enhanced expression of Rhizobium etli cbb3 oxidase improves drought tolerance of common bean symbiotic nitrogen fixation. J Exp Bot 63: 5035-5043.","Thakur R, Sharma KC, Gulati A, et al. (2017) Stress-tolerant Viridibacillus arenosi strain IHB B 7171 from Tea rhizosphere as a potential broad-spectrum microbial inoculant. Indian J Microbiol 57: 195-200.","Sandra C-P, Rebeca BR (2015) Polymers selection for a liquid inoculant of Azospirillum brasilense based on the Arrhenius thermodynamic model. African J Biotechnol 33: 2547-2553.","Bashan Y, De-Bashan LE, Prabhu SR (2016) Superior Polymeric Formulations and Emerging Innovative Products of Bacterial Inoculants for Sustainable Agriculture and the Environment BT - Agriculturally Important Microorganisms: Commercialization and Regulatory Requirements in Asia. In: Singh HB, Sarma BK, Keswani C, editors. Singapore: Springer Singapore; 15-46."]}