Abstract
Arsenic naturally occurs in the earth’s crust and can be introduced in the environment by human activities. Agricultural practices in arsenic-contaminated environments pose a threat to human health. The contamination of crops contributes to the metalloid’s introduction in the food chain. This study aims to test the hypotheses that the inoculation of a hyperaccumulator rhizobacterial strain, Ochrobactrum tritici As5, to the rhizosphere of rice plants reduces the arsenic presence inside the tissue of the rice plants and reduces the inhibitory effect of the metalloid on the plant’s growth parameters. Inoculation of the hyperaccumulating strain O. tritici As5 showed the lowest concentration of arsenic in the plant’s tissue (2.6 fold lower than sterile plants), compared to the unmodified type O. tritici SCII24 and sterile rice plants. The inoculation of the type strain SCII24 also led to a decrease in arsenic concentration in the plant tissue compared with sterile plants (1.6 fold lower than sterile plants). The difference in arsenic presence in shoots was smaller among treatment groups than in the roots, showing a similar trend. The inoculation of the hyperaccumulator As5 strain alleviated some of the toxic effects of arsenic on shoot growth compared to inoculation of the unmodified type strain. All these findings together, contribute to our understanding of the interplay between arsenic pollution, plants and their rhizobacteria, especially the role of bioaccumulation of metal(oids) by rhizobacteria, and provide important information on the prevention of arsenic uptake by crops and the development of phytostabilizers.
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Alcantara-Martinez N, Figueroa-Martinez F, Rivera-Cabrera F, Gutierrez-Sanchez G, Volke-Sepulveda T (2018) An endophytic strain of Methylobacterium sp. increases arsenate tolerance in Acacia farnesiana (L.) Willd: a proteomic approach. Sci Total Environ 625:762–774
Bilal S, Shahzad R, Khan AL, Kang SM, Imran QM, Al-Harrasi A et al (2018) Endophytic microbial consortia of phytohormones-producing fungus Paecilomyces formosus LHL10 and bacteria Sphingomonas sp. LK11 to Glycine max L. regulates physio-hormonal changes to attenuate aluminum and zinc stresses. Front Plant Sci 9:1273
Bowman AW, Azzalini A (2018) R package ‘sm’: nonparametric smoothing methods (version 2.2–5.6). http://www.stats.gla.ac.uk/~adrian/sm
Branco R, Chung AP, Morais PV (2008) Sequencing and expression of two arsenic resistance operons with different functions in the highly arsenic-resistant strain Ochrobactrum tritici SCII24 T. BMC Microbiol 8:95
Branco R, Sousa T, Piedade AP, Morais PV (2016) Immobilization of Ochrobactrum tritici As5 on PTFE thin films for arsenite biofiltration. Chemosphere 146:330–337
Briat JF (2010) Arsenic tolerance in plants: “Pas de deux” between phytochelatin synthesis and ABCC vacuolar transporters. Proc Natl Acad Sci USA 107:20853–20854
Dell’Amico E, Cavalca L, Andreoni V (2005) Analysis of rhizobacterial communities in perennial Graminaceae from polluted water meadow soil, and screening of metal-resistant, potentially plant growth-promoting bacteria. FEMS Microbiol Ecol 52:153–162
Flanagan SV, Johnston RB, Zheng Y (2012) Arsenic in tube well water in Bangladesh: health and economic impacts and implications for arsenic mitigation. Bull World Health Organ 90:839–846
Fraga H, Guimarães N, Santos JA (2019) Future changes in rice bioclimatic growing conditions in Portugal. Agronomy 9:674
Francisco R, de Abreu P, Plantz BA, Schlegel VL, Carvalho RA, Morais PV (2011) Metal-induced phosphate extracellular nanoparticulate formation in Ochrobactrum tritici 5bvl1. J Hazard Mater 198:31–39
Francisco R, Branco R, Schwab S, Baldani JI, Morais PV (2018) Impact of plant-associated bacteria biosensors on plant growth in the presence of hexavalent chromium. World J Microb Biot 34:12
Ghosh PK, Maiti TK, Pramanik K, Ghosh SK, Mitra S, De TK (2018) The role of arsenic resistant Bacillus aryabhattai MCC3374 in promotion of rice seedlings growth and alleviation of arsenic phytotoxicity. Chemosphere 211:407–419
Hoagland DR, Arnon DI (1950) The water-culture method for growing plants without soil. Circular 347 (California agricultural experiment station)
Hurek T, Reinhold-Hurek B, Van Montagu M, Kellenberger E (1994) Root colonization and systemic spreading of Azoarcus sp. strain BH72 in grasses. J Bacteriol 176:1913–1923
Kofroňová M, Mašková P, Lipavská H (2018) Two facets of world arsenic problem solution: crop poisoning restriction and enforcement of phytoremediation. Planta 48:19–35
Lenth R (2019) emmeans: estimated marginal means, aka least-squares means. R package version 1.4.2. https://CRAN.R-project.org/package=emmeans
Ma Y, Prasad MNV, Rajkumar M, Freitas H (2011) Plant growth promoting rhizobacteria and endophytes accelerate phytoremediation of metalliferous soils. Biotechnol Adv 29:248–258
Madhaiyan M, Poonguzhali S, Sa T (2007) Metal tolerating methylotrophic bacteria reduces nickel and cadmium toxicity and promotes plant growth of tomato (Lycopersicon esculentum L.). Chemosphere 69:220–228
Mandal BK, Suzuki KT (2002) Arsenic round the world: a review. Talanta 58:201–235
Mesa V, Navazas A, González-Gil R, González A, Weyens N, Lauga B, Peláez AI (2017) Use of endophytic and rhizosphere bacteria to improve phytoremediation of arsenic-contaminated industrial soils by autochthonous Betula celtiberica. Appl Environ Microbiol 83:e03411–e3416
Oksanen J, Blanchet FG, Friendly M, Kindt R, Legendre P, McGlinn D et al (2018) Vegan: community ecology package. R package version 2.5-2. https://CRAN.R-project.org/package=vegan
Pandey S, Ghosh PK, Ghosh S, De TK, Maiti TK (2013) Role of heavy metal resistant Ochrobactrum sp. and Bacillus spp. strains in bioremediation of a rice cultivar and their PGPR like activities. J Microbiol 51:11–17
R Core Team (2018) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/
Rucińska-Sobkowiak R (2016) Water relations in plants subjected to heavy metal stresses. Acta Physiol Plant 38(11):257
Seyfferth AL, Webb SM, Andrews JC, Fendorf S (2010) Arsenic localization, speciation, and co-occurrence with iron on rice (Oryza sativa L.) roots having variable Fe coatings. Environ Sci Techol 44:8108–8113
Shahabivand S, Parvaneh A, Aliloo AA (2017) Root endophytic fungus Piriformospora indica affected growth, cadmium partitioning and chlorophyll fluorescence of sunflower under cadmium toxicity. Ecotox Environ Saf 145:496–502
Sousa T, Branco R, Piedade AP, Morais PV (2015) Hyper accumulation of arsenic in mutants of Ochrobactrum tritici silenced for arsenite efflux pumps. PLoS ONE 10:e0131317
Tiwari S, Lata C (2018) Heavy metal stress, signaling, and tolerance due to plant-associated microbes: an overview. Front Plant Sci 9:452
Tsai SL, Singh S, Chen W (2009) Arsenic metabolism by microbes in nature and the impact on arsenic remediation. Curr Opin Biotech 20:659–667
Villacorta PJ (2015) ART: Aligned Rank Transform for nonparametric factorial analysis. R package version 1.0. https://CRAN.R-project.org/package=ART
Wickham H (2016) ggplot2: elegant graphics for data analysis. Springer, New York
Zhao FJ, McGrath SP, Meharg AA (2010) Arsenic as a food chain contaminant: mechanisms of plant uptake and metabolism and mitigation strategies. Annu Rev Plant Biol 61:535–559
Zhuang X, Chen J, Shim H, Bai Z (2007) New advances in plant growth-promoting rhizobacteria for bioremediation. Environ Int 33:406–413
Acknowledgements
This work was supported by CEMMPRE and by Fundação para a Ciência e a Tecnologia (FCT) under the project UID/EMS/00285/2013 and the project ERA-MIN/0002/2015. MM was supported by the ERA-MIN/0002/2015 project through a research fellowship. RB was supported by a FCT Grant SFRH/BPD/110807/2015. We thank Romeu Francisco for critical reading of the manuscript.
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Moens, M., Branco, R. & Morais, P.V. Arsenic accumulation by a rhizosphere bacterial strain Ochrobactrum tritici reduces rice plant arsenic levels. World J Microbiol Biotechnol 36, 23 (2020). https://doi.org/10.1007/s11274-020-2800-0
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DOI: https://doi.org/10.1007/s11274-020-2800-0