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Seed Endophytes of Jasione montana: Arsenic Detoxification Workers in an Eco-friendly Factory

  • María del Carmen MolinaEmail author
  • James Francis WhiteJr
  • Kathryn L. Kingsley
  • Natalia González-Benítez
Chapter

Abstract

Arsenic (As) is a toxic compound for human health and ecosystems. Some organisms have developed different strategies to live in environments contaminated with arsenic (As-tolerant organisms). Some prokaryotes are able to use arsenic as a donor or acceptor of electrons through respiratory processes (arsenic oxidizer and reducer bacteria). Certain plants can accumulate it in their tissues (accumulative plants) or imply their uptake and favor their exclusion (exclusion plants). Some fungi and bacteria are able to metabolize organic forms less toxic and volatile it. These mechanisms allow plants, prokaryotes and fungi to develop in environments with high concentrations of As. It is known that microbiota (especially rhizosphere and endosphere) can help plants to survive under arsenic stress conditions. However, little is known about the contribution of seed endophytes in the germination capacity and early development of seedling plants under As conditions. This chapter shows a brief review on the role of endophytic bacteria in the adaptation of plants to As stress conditions. Endophytic bacteria from seeds, obtained from plants that grow in As-contaminated soils, have showed that many of them promote the growth of the plant, have antifungal activity, and are AsV reducer bacteria, with the ability to metabolize arsenic to organic forms. We suggest that they have an important role in germination and early development when the seeds fall into an As-contaminated environment.

Keywords

Endophyte Arsenic stress Seed Plant growth promoting bacteria Metaorganism 

Notes

Acknowledgments

The authors thank Dr. M. Bergen (Rutgers University) and Dr. S.K. Verma (Banaras Hindu University) for his invaluable help and collaboration. Molina, M.C. greatly thanks Rutgers University for her time there as a Visiting Scientist.

References

  1. Abbas G, Murtaza B, Bibi I et al (2018) Arsenic uptake, toxicity, detoxification, and speciation in plants: physiological, biochemical, and molecular aspects. Int J Environ Res Public Health 15:59.  https://doi.org/10.3390/ijerph15010059CrossRefPubMedCentralGoogle Scholar
  2. Akinsanya M, Goh JK, Lim SP et al (2015) Metagenomics study of endophytic bacteria in Aloe vera using next-generation technology. Genom Data 6:159–163.  https://doi.org/10.1016/j.gdata.2015.09.004CrossRefPubMedPubMedCentralGoogle Scholar
  3. Asher CJ, Reay PF (1979) Arsenic uptake by barley seedlings. Aust J Plant Physiol 6:459–466Google Scholar
  4. Bakhat HF, Zia Z, Fahad S et al (2017) Arsenic uptake, accumulation and toxicity in rice plants: possible remedies for its detoxification: a review. Environ Sci Pollut Res 24:9142–9158.  https://doi.org/10.1007/s11356-017-8462-2CrossRefGoogle Scholar
  5. Barret M, Briand M, Bonneau S et al (2015) Emergence shapes the structure of the seed microbiota. Appl Environ Microbiol 81:1257–1266.  https://doi.org/10.1128/AEM.03722-14CrossRefPubMedPubMedCentralGoogle Scholar
  6. Benson LM, Porter EK, Peterson PJ (1981) Arsenic accumulation, tolerance and genotypic variation in plants on arsenical mine wastes in S.W. England. J Plant Nutr 3:655–666.  https://doi.org/10.1080/01904168109362868CrossRefGoogle Scholar
  7. Bentley R, Chasteen TG (2002) Microbial methylation of metalloids: arsenic, antimony and bismuth. Microbiol Mol Biol Rev 66:250–271.  https://doi.org/10.1128/MMBR.66.2.250-271.2002CrossRefPubMedPubMedCentralGoogle Scholar
  8. Bleeker PM, Schat H, Vooijs R et al (2003) Mechanisms of arsenate tolerance in Cytisus striatus. New Phytol 157:33–38.  https://doi.org/10.1046/j.1469-8137.2003.00542.xCrossRefGoogle Scholar
  9. Bosch TCG, McFall-Ngai MJ (2011) Metaorganisms as the new frontier. Zoology 114:185–190.  https://doi.org/10.1016/j.zool.2011.04.001CrossRefPubMedGoogle Scholar
  10. Byrne JM, Kappler A (2017) Current and future microbiological strategies to remove As and Cd from drinking water. Microb Biotechnol 10:1098–1110.  https://doi.org/10.1111/1751-7915.12742CrossRefPubMedPubMedCentralGoogle Scholar
  11. Cha Y, Kim YM, Choi JW et al (2015) Bayesian modeling approach for characterizing groundwater arsenic contamination in the Mekong River basin. Chemosphere 143:50–56.  https://doi.org/10.1016/j.chemosphere.2015.02.045CrossRefPubMedGoogle Scholar
  12. Chen Y, Xu W, Shen H et al (2013) Engineering arsenic tolerance and hyperaccumulation in plants for phytoremediation by a PvACR3 transgenic approach. Environ Sci Technol 47:9355–9362.  https://doi.org/10.1021/es4012096CrossRefPubMedGoogle Scholar
  13. Chen J, Bhattacharjee H, Rosen BP (2015) ArsH is an organoarsenical oxidase that confers resistance to trivalent forms of the herbicide monosodium methylarsenate and the poultry growth promoter roxarsone. Mol Microbiol 96:1042–1052CrossRefGoogle Scholar
  14. Chen Y, Han YH, Cao Y et al (2017a) Arsenic transport in rice and biological solutions to reduce arsenic risk from rice. Front Plant Sci 8:268.  https://doi.org/10.3389/fpls.2017.00268CrossRefPubMedPubMedCentralGoogle Scholar
  15. Chen SC, Sun GX, Rosen BP et al (2017b) Recurrent horizontal transfer of arsenite methyltransferase genes facilitated adaptation of life to arsenic. Sci Rep 7:7741.  https://doi.org/10.1038/s41598-017-08313-2CrossRefPubMedPubMedCentralGoogle Scholar
  16. Cherian S, Weyens N, Lindberg S et al (2012) Phytoremediation of trace element–contaminated environments and the potential of endophytic bacteria for improving this process. Crit Rev Environ Sci Technol 42:2215–2260.  https://doi.org/10.1080/10643389.2011.574106CrossRefGoogle Scholar
  17. Compant S, Duffy B, Nowak J et al (2005) Use of plant growth-promoting bacteria for biocontrol of plant diseases: principles, mechanisms of action, and future prospects. Appl Environ Microbiol 71:4951–4959.  https://doi.org/10.1128/AEM.71.9.4951-4959.2005CrossRefPubMedPubMedCentralGoogle Scholar
  18. Coombs JT, Franco CMM (2003) Visualization of an endophytic Streptomyces species in wheat seed. Appl Environ Microbiol 69:4260–4262.  https://doi.org/10.1128/AEM.69.7CrossRefPubMedPubMedCentralGoogle Scholar
  19. Dastidar A, Wang Y (2009) Arsenite oxidation by batch cultures of Thiomonas arsenivorans strain b6. J Environ Eng 135:708–715.  https://doi.org/10.1061/ASCEEE.1943-7870.0000020CrossRefGoogle Scholar
  20. Ellis DR, Gumaelius L, Indriolo E et al (2006) A novel arsenate reductase from the arsenic hyperaccumulating Pteris vittata. Plant Physiol 141:1544–1554.  https://doi.org/10.1104/pp.106.084079CrossRefPubMedPubMedCentralGoogle Scholar
  21. Farooq MA, Islam F, Ali B et al (2016) Arsenic toxicity in plants: cellular and molecular mechanisms of its transport and metabolism. Environ Exp Bot 132:42–52.  https://doi.org/10.1016/j.envexpbot.2016.08.004CrossRefGoogle Scholar
  22. Ferreira A, Quecine MC, Lacava PT et al (2008) Diversity of endophytic bacteria from Eucalyptus species seed sand colonization of seedlings by Pantoea agglomerans. FEMS Microbiol Lett 287:8–14.  https://doi.org/10.1111/j.1574-6968.2008.01258.xCrossRefPubMedGoogle Scholar
  23. Franchi E, Rolli E, Marasco R et al (2016) Phytoremediation of a multi contaminated soil: mercury and arsenic phytoextraction assisted by mobilizing agent and plant growth promoting bacteria. J Soils Sediments 17:1224–1236.  https://doi.org/10.1007/s11368-015-1346-5CrossRefGoogle Scholar
  24. García-Salgado S, García-Casillas D, Quijano-Nieto MA et al (2012) Arsenic and heavy metal uptake and accumulation in native plant species from soils polluted by mining activities. Water Air Soil Pollut 223:559.  https://doi.org/10.1007/s11270-011-0882-xCrossRefGoogle Scholar
  25. Geiszinger A, Goessler W, Kosmus W (2002) Organoarsenic compounds in plants and soil on top of an ore vein. Appl Organomet Chem 16:245–249.  https://doi.org/10.1002/aoc.294CrossRefGoogle Scholar
  26. Gihring TM, Bond PL, Peters SC et al (2003) Arsenic resistance in the archaeon “Ferroplasma acidarmanus”: new insights into the structure and evolution of the ars genes. Extremophiles 7:123–130.  https://doi.org/10.1007/s00792-002-0303-6CrossRefPubMedGoogle Scholar
  27. Glassner H, Zchori-Fein E, Yaron S et al (2018) Bacterial niches inside seeds of Cucumis melo L. Plant Soil 422:101.  https://doi.org/10.1007/s11104-017-3175-3CrossRefGoogle Scholar
  28. Gutiérrez-Ginés MJ, Pastor J, Hernández AJ (2015) Heavy metals in native mediterranean grassland species growing at abandoned mine sites: ecotoxicological assessment and phytoremediation of polluted soils. In: Sherameti I, Varma A (eds) Heavy metal contamination of soils. Soil biology, vol 44. Springer, Cham, pp 159–178Google Scholar
  29. Hallmann J, Berg G, Schulz B (2006) Isolation procedures for endophytic microorganisms. In: Schulz B, Boyle C, Sieber TN (eds) Microbial root endophytes. Soil biology, vol 9. Springer, Berlin, pp 299–319CrossRefGoogle Scholar
  30. Hamamura N, Itai T, Liu Y et al (2014) Identification of anaerobic arsenite-oxidizing and arsenate-reducing bacteria associated with an alkaline saline lake in Khovsgol. Environ Microbiol Rep 6:476–448.  https://doi.org/10.1111/1758-2229.12144CrossRefPubMedGoogle Scholar
  31. Han YH, Fu JW, Chen Y et al (2016) Arsenic uptake, arsenite efflux and plant growth in hyperaccumulator Pteris vittata: role of arsenic-resistant bacteria. Chemosphere 144:1937–1942.  https://doi.org/10.1016/j.chemosphere.2015.10.096CrossRefPubMedGoogle Scholar
  32. Han YH, Liu W, Rathinasabapathi B et al (2017) Mechanisms of efficient As solubilization in soils and As accumulation by As-hyperaccumulator Pteris vittata. Environ Pollut 227:569–577.  https://doi.org/10.1016/j.envpol.2017.05.001CrossRefPubMedGoogle Scholar
  33. Hardoim PR, van Overbeek LS, Berg G et al (2015) The hidden world within plants: ecological and evolutionary considerations for defining functioning of microbial endophytes. Microbiol Mol Biol Rev 79:293–320.  https://doi.org/10.1128/MMBR.00050-14CrossRefPubMedPubMedCentralGoogle Scholar
  34. Hayat K, Menhas S, Bundschuh J et al (2017) Microbial biotechnology as an emerging industrial wastewater treatment process for arsenic mitigation: a critical review. J Clean Prod 151:427–438.  https://doi.org/10.1016/j.jclepro.2017.03.084CrossRefGoogle Scholar
  35. Indriolo E, Na GN, Ellis D et al (2010) Vacuolar arsenite transporter necessary for arsenic tolerance in the arsenic hyperaccumulating fern Pteris vittata is missing in flowering plants. Plant Cell 22:2045–2057.  https://doi.org/10.1105/tpc.109.069773CrossRefPubMedPubMedCentralGoogle Scholar
  36. Kaga H, Mano H, Tanaka F (2009) Rice seeds as sources of endophytic bacteria. Microbes Environ 24:154–162.  https://doi.org/10.1264/jsme2.ME09113CrossRefPubMedGoogle Scholar
  37. Kembel SW, O’Connor TK, Arnold HK (2014) Relationships between phyllosphere bacterial communities and plant functional traits in a neotropical forest. Proc Natl Acad Sci USA 111:13715–13720.  https://doi.org/10.1073/pnas.1216057111CrossRefPubMedGoogle Scholar
  38. Klaedtke S, Jacques MA, Raggi L et al (2015) Terroir is a key driver of seed-associated microbial assemblages. Environ Microbiol 18:1792–1804.  https://doi.org/10.1111/1462-2920.12977CrossRefPubMedGoogle Scholar
  39. Lampis S, Santi C, Ciurli A (2015) Promotion of arsenic phytoextraction efficiency in the fern Pteris vittata by the inoculation of As-resistant bacteria: a soil bioremediation perspective. Front Plant Sci 6:80.  https://doi.org/10.3389/fpls.2015.00080CrossRefPubMedPubMedCentralGoogle Scholar
  40. Lata R, Chowdhury S, Gond SK et al (2018) Induction of abiotic stress tolerance in plants by endophytic microbes. Lett Appl Microbiol 66:268–276.  https://doi.org/10.1111/lam.12855CrossRefGoogle Scholar
  41. Li W, We C, Zhang C et al (2003) A survey of arsenic species in Chinese seafood. Food Chem Toxicol 41:1103–1110.  https://doi.org/10.1016/S0278-6915(03)00063-2CrossRefPubMedGoogle Scholar
  42. Li RY, Ago Y, Liu WJ et al (2009) The rice aquaporin lsi1 mediates uptake of methylated arsenic species. Plant Physiol 150:2071–2080.  https://doi.org/10.1104/pp.109.140350CrossRefPubMedPubMedCentralGoogle Scholar
  43. Liu Y, Zuo S, Xu L et al (2012) Study on diversity of endophytic bacterial communities in seeds of hybrid maize and their parental lines. Arch Microbiol 194:1001–1012.  https://doi.org/10.1007/s00203-012-0836-8CrossRefPubMedGoogle Scholar
  44. Lyubun YL, Fritzsche A, Chernyshova MP et al (2006) Arsenic transformation by Azospirillum brasilense Sp245 in association with wheat (Triticum aestivum L.) roots. Plant Soil 286:219–227.  https://doi.org/10.1007/s11104-006-9039-xCrossRefGoogle Scholar
  45. Ma Y, Rajkumar M, Luo YM et al (2011) Inoculation of endophytic bacteria on host and non-host plants—effects on plant growth and Ni uptake. J Hazard Mater 195:230–237.  https://doi.org/10.1016/j.jhazmat.2011.08.034CrossRefPubMedGoogle Scholar
  46. Ma Y, Rajkumar M, Zhang C et al (2016) Beneficial role of bacterial endophytes in heavy metal Phytoremediation. J Environ Manag 174:14–25.  https://doi.org/10.1016/j.jenvman.2016.02.047CrossRefGoogle Scholar
  47. Mallick I, Bhattacharyya C, Mukherji S et al (2018) Effective rhizoinoculation and biofilm formation by arsenic immobilizing halophilic plant growth promoting bacteria (PGPB) isolated from mangrove rhizosphere: a step towards arsenic rhizoremediation. Sci Total Environ 610–611:1239–1250.  https://doi.org/10.1016/j.scitotenv.2017.07.234CrossRefPubMedGoogle Scholar
  48. Mallik S, Virdi JS, Johri AK (2012) Proteomic analysis of arsenite—mediated multiple antibiotic resistance in Yersinia enterocolitica biovar 1A. J Basic Microbiol 52:306–313.  https://doi.org/10.1002/jobm.201100109CrossRefPubMedGoogle Scholar
  49. Mass MJ, Tennant A, Roop BC et al (2001) Methylated trivalent arsenic species are genotoxic. Chem Res Toxicol 14:355–361.  https://doi.org/10.1021/tx000251lCrossRefPubMedGoogle Scholar
  50. Mastretta C, Taghavi S, Van der Leie D et al (2009) Endophytic bacteria from seeds of nicotiana tabacum can reduce cadmium phytotoxicity. Int J Phytoremediation 11:251–267.  https://doi.org/10.1080/15226510802432678CrossRefGoogle Scholar
  51. Meharg AA, Jardine L (2003) Arsenite transport into paddy rice (Oryza sativa) roots. New Phytol 157:39–43.  https://doi.org/10.1046/j.1469-8137.2003.00655.xCrossRefGoogle Scholar
  52. Mesa V, Navazas A, González-Gil R et al (2017) Use of endophytic and rhizosphere bacteria to improve phytoremediation of arsenic-contaminated industrial soils by Autochthonous Betula celtiberica. Appl Environ Microbiol 83:e0341116.  https://doi.org/10.1128/AEM.03411-16CrossRefGoogle Scholar
  53. Mishra S, Mattusch J, Wennrich R (2017) Accumulation and transformation of inorganic and organic arsenic in rice and role of thiol-complexation to restrict their translocation to shoot. Sci Rep 7:40522.  https://doi.org/10.1038/srep40522CrossRefPubMedPubMedCentralGoogle Scholar
  54. Mitra E, Mattusch J, Wennrich R (2017) Accumulation and transformation of inorganic and organic arsenic in rice and role of thiol-complexation to restrict their translocation to shoot. Sci Rep 7:40522.  https://doi.org/10.1038/srep40522CrossRefGoogle Scholar
  55. Mitter B, Pfaffenbichler N, Flavell R (2017) A new approach to modify plant microbiomes and traits by introducing beneficial bacteria at flowering into progeny seeds. Front Microbiol 8:11.  https://doi.org/10.3389/fmicb.2017.00011CrossRefPubMedPubMedCentralGoogle Scholar
  56. Molina MC, González N, Bautista LF et al (2009) Isolation and genetic identification of PAH degrading bacteria from a microbial consortium. Biodegradation 20:789–800.  https://doi.org/10.1007/s10532-009-9267-xCrossRefPubMedGoogle Scholar
  57. Mosa KA, Kumar K, Chhikara S et al (2012) Members of rice plasma membrane intrinsic proteins subfamily are involved in arsenite permeability and tolerance in plants. Transgenic Res 21:1265–1277CrossRefGoogle Scholar
  58. Mukherjee G, Saha C, Naskar N et al (2018) An endophytic bacterial consortium modulates multiple strategies to improve arsenic phytoremediation efficacy in Solanum nigrum. Sci Rep 8:6979.  https://doi.org/10.1038/s41598-018-25306-xCrossRefPubMedPubMedCentralGoogle Scholar
  59. Mukhopadhyay R, Rosen BP, Phung LT et al (2002) Microbial arsenic: from geocycles to genes and enzymes. FEMS Microbiol Rev 26:311–325.  https://doi.org/10.1111/j.1574-6976.2002.tb00617.xCrossRefPubMedGoogle Scholar
  60. Nadar VS, Yoshinaga M, Pawitwar SS et al (2016) Structure of the ArsI C–As Lyase: insights into the mechanism of degradation of organoarsenical herbicides and growth promoters. J Mol Biol 428:2462–2473.  https://doi.org/10.1016/j.jmb.2016.04.022CrossRefPubMedPubMedCentralGoogle Scholar
  61. Nejad P, Johnson PA (2000) Endophytic bacteria induce growth promotion and wilt disease suppression in oilseed rape and tomato. Biol Control 18:208–215.  https://doi.org/10.1006/bcon.2000.0837CrossRefGoogle Scholar
  62. Ogra Y (2009) Toxicometallomics for research on the toxicology of exotic metalloids based on speciation studies. Anal Sci 25:1189–1195.  https://doi.org/10.2116/analsci.25.1189CrossRefPubMedGoogle Scholar
  63. Oremland RS, Stolz JF (2003) The ecology of arsenic. Science 300:939–944.  https://doi.org/10.1126/science.1081903CrossRefPubMedGoogle Scholar
  64. Páez-Espino D, Tamames J, de Lorenzo V et al (2009) Microbial responses to environmental arsenic. Biometals 22:117–130.  https://doi.org/10.1007/s10534-008-9195-yCrossRefPubMedGoogle Scholar
  65. Pawitwar SS, Nadar VS, Kandegedara A et al (2017) Biochemical characterization of ArsI: a novel C–As Lyase for degradation of environmental organoarsenicals. Environ Sci Technol 51:11115–11125. http://orcid.org/0000-0002-7243-1761CrossRefGoogle Scholar
  66. Pikovskaya RI (1948) Mobilization of phosphorus in soil in connection with vital activity of some microbial species. Mikrobiologiya 17:362–370Google Scholar
  67. Porter EK, Peterson PJ (1975) Arsenic accumulation by plants on mine waste (United Kingdom). Sci Total Environ 4:356–371CrossRefGoogle Scholar
  68. Qin J, Rosen BP, Zhang Y (2006) Arsenic detoxification and evolution of trimethylarsine gas by a microbial arsenite S-adenosylmethionine methyltransferase. Proc Natl Acad Sci U S A 103:2075–2080.  https://doi.org/10.1073/pnas.0506836103CrossRefPubMedPubMedCentralGoogle Scholar
  69. Raab A, Schat H, Meharg AA et al (2005) Uptake, translocation and transformation of arsenate and arsenite in sunflower (Helianthus annuus): formation of arsenic–phytochelatin complexes during exposure to high arsenic concentrations. New Phytol 168:551–558.  https://doi.org/10.1111/j.1469-8137.2005.01519.xCrossRefPubMedGoogle Scholar
  70. Rajkumar M, Ae N, Freitas H (2009) Endophytic bacteria and their potential to enhance heavy metal phytoextraction. Chemosphere 77:153–160.  https://doi.org/10.1016/j.chemosphere.2009.06.047CrossRefPubMedGoogle Scholar
  71. Rathinasabapathi B, Raman SB, Kertulis G et al (2006) Arsenic-resistant proteobacterium from the phyllosphere of arsenic-hyperaccumulating fern (Pteris vittata L.) reduces arsenate to arsenite. Can J Microbiol 52:695–700.  https://doi.org/10.1139/w06-017CrossRefPubMedGoogle Scholar
  72. Ratnaike RN (2003) Organic arsenic is non-toxic whereas inorganic arsenic is toxic. Acute and chronic arsenic toxicity. Postgrad Med J 79:391–396CrossRefGoogle Scholar
  73. Ritchie AW, Edmonds JS, Goessler W et al (2004) An origin for arsenobetaine involving bacterial formation of an arsenic-carbon bond. FEMS Microbiol Lett 235:95–99.  https://doi.org/10.1016/j.femsle.2004.04.016CrossRefPubMedGoogle Scholar
  74. Rosen BP (2002) Biochemistry of arsenic detoxification. FEBS Lett 529:86–92.  https://doi.org/10.1016/S0014-5793(02)03186-1CrossRefPubMedGoogle Scholar
  75. Ryan RP, Germaine K, Franks A et al (2008) Bacterial endophytes: recent developments and applications. FEMS Microbiol Let 278:1–9.  https://doi.org/10.1111/j.1574-6968.2007.00918.xCrossRefGoogle Scholar
  76. Sánchez-López AS, Pintelon I, Stevens V et al (2018a) Seed endophyte microbiome of Crotalaria pumila unpeeled: identification of plant-beneficial methylobacteria. Int J Mol Sci 19:291.  https://doi.org/10.3390/ijms19010291CrossRefPubMedCentralGoogle Scholar
  77. Sánchez-López AS, Thijs S, Beckers B et al (2018b) Community structure and diversity of endophytic bacteria in seeds of three consecutive generations of Crotalaria pumila growing on metal mine residues. Plant Soil 422:51.  https://doi.org/10.1007/s11104-017-3176-2CrossRefGoogle Scholar
  78. Selvankumar T, Radhika R, Mythili R et al (2017) Isolation, identification and characterization of arsenic transforming exogenous endophytic Citrobacter sp. RPT from roots of Pteris vittata. Biotech 7:264.  https://doi.org/10.1007/s13205-017-0901-8CrossRefGoogle Scholar
  79. Sheoran N, Nadakkakath AV, Munjal V et al (2015) Genetic analysis of plant endophytic Pseudomonas putida BP25 and chemo-profiling of its antimicrobial volatile organic compounds. Microbiol Res 173:66–78.  https://doi.org/10.1016/j.micres.2015.02.001CrossRefPubMedGoogle Scholar
  80. Shi YW, Yang H, Zhang T (2014) Illumina-based analysis of endophytic bacterial diversity and space-time dynamics in sugar beet on the north slope of Tianshan mountain. Appl Microbiol Biotechnol 98:6375–6638.  https://doi.org/10.1007/s00253-014-5720-9CrossRefPubMedGoogle Scholar
  81. Siciliano SD, Fortin N, Mihoc A et al (2001) Selection of specific endophytic bacterial genotypes by plants in response to soil contamination. Appl Environ Microbiol 67:2469–2475.  https://doi.org/10.1128/AEM.67.6.2469–2475.200CrossRefPubMedPubMedCentralGoogle Scholar
  82. Silver S, Phung LT (2005) Genes and enzymes involved in bacterial oxidation and reduction of inorganic arsenic. Appl Environ Microbiol 71:599–608.  https://doi.org/10.1128/AEM.71.2.599–608.2005CrossRefPubMedPubMedCentralGoogle Scholar
  83. Srivastava N (2016) Role of phytochelatins in phytoremediation of heavy metals contaminated soils. In: Ansari A, Gill S, Gill R, Lanza G, Newman L (eds) Phytoremediation. Springer, Cham, pp 393–419CrossRefGoogle Scholar
  84. Sun W, Xionga Z, Chua L et al (2018) Bacterial communities of three plant species from Pb-Zn contaminated sites and plant-growth promotional benefits of endophytic Microbacterium sp. (strain BXGe71). J Hazard Mater.  https://doi.org/10.1016/j.jhazmat.2018.02.003
  85. Thijs S, Sillen W, Rineau F et al (2016) Towards an enhanced understanding of plant–microbiome interactions to improve phytoremediation: engineering the metaorganism. Front Microbiol 107:1–15.  https://doi.org/10.3389/fmicb.2016.00341CrossRefGoogle Scholar
  86. Titah HS, Abdullah SRS, Anuar N et al (2011) Isolation and screening of arsenic resistant rhizobacteria of Ludwigia octovalvis. Afr J Biotechnol 10:18695–18703.  https://doi.org/10.5897/AJB11.2740CrossRefGoogle Scholar
  87. Tiwari S, Sarangi K, Thul ST (2016) Identification of arsenic resistant endophytic bacteria from Pteris vittata roots and characterization for arsenic remediation application. J Environ Manag 180:359–365.  https://doi.org/10.1016/j.jenvman.2016.05.029CrossRefGoogle Scholar
  88. Torres SK, Campos VL, León CG et al (2012) Biosynthesis of selenium nanoparticles by Pantoea agglomerans and their antioxidant activity. J Nanopart Res 14:1236.  https://doi.org/10.1007/s11051-012-1236-3CrossRefGoogle Scholar
  89. Tripathi RD, Srivastava S, Mishra S, Singh N, Tuli R, Gupta DK, Maathuis FJ (2007) Arsenic hazards: strategies for tolerance and remediation by plants. Trends Biotechnol 25(4):158–165CrossRefGoogle Scholar
  90. Truyens S, Jambon I, Croes S et al (2014) The effect of long-term Cd and Ni exposure on seed endophytes of Agrostis capillaris and their potential application in phytoremediation of metal-contaminated soils. Int J Phytoremediation 16:643–659.  https://doi.org/10.1080/15226514.2013.837027CrossRefPubMedGoogle Scholar
  91. Truyens S, Weyens N, Cuypers A (2015) Bacterial seed endophytes: genera, vertical transmission and interaction with plants. Environ Microbiol Rep 7:40–50.  https://doi.org/10.1111/1758-2229.12181CrossRefGoogle Scholar
  92. Tsai SL, Singh S, Chen W (2009) Arsenic metabolism by microbes in nature and the impact on arsenic remediation. Curr Opin Biotechnol 20:659–667.  https://doi.org/10.1016/j.copbio.2009.09.013CrossRefPubMedGoogle Scholar
  93. Utturkar SM, Cude WN, Robeson MS et al (2006) Enrichment of root endophytic bacteria from Populus deltoides and single-cell-genomics analysis. Appl Environ Microbiol 82:5698–5708.  https://doi.org/10.1128/AEM.01285-16CrossRefGoogle Scholar
  94. Verma SK, Kingsley K, Irizarry I, Bergen M, Kharwar RN, White JF Jr (2017) Seed-vectored endophytic bacteria modulate development of rice seedlings. J Appl Microbiol 122(6):1680–1691CrossRefGoogle Scholar
  95. Verma SK, White JF (2017) Indigenous endophytic seed bacteria promote seedling development and defend against fungal disease in browntop millet (Urochloa ramosa L.). J Appl Microbiol 124:764–778.  https://doi.org/10.1111/jam.13673CrossRefGoogle Scholar
  96. White JF, Torres MA (2010) Is plant endophyte-mediated defensive mutualism the result of oxidative stress protection? Physiol Plant 138:440–446.  https://doi.org/10.1111/j.1399-3054.2009.01332.xCrossRefPubMedGoogle Scholar
  97. White JF, Kingsley KI, Kowalski KP et al (2018a) Disease protection and allelopathic interactions of seed-transmitted endophytic pseudomonads of invasive reed grass. Plant Soil 422:195–208.  https://doi.org/10.1007/s11104-016-3169-6CrossRefGoogle Scholar
  98. White J, Kingsley K, Verma S et al (2018b) Rhizophagy cycle: an oxidative process in plants for nutrient extraction from symbiotic microbes. Microorganisms 6:95.  https://doi.org/10.3390/microorganisms6030095
  99. Xu JY, Han YH, Chen Y et al (2016) Arsenic transformation and plant growth promotion characteristics of As-resistant endophytic bacteria from As hyperaccumulator Pteris vittata. Chemosphere 144:1233–1240.  https://doi.org/10.1016/j.chemosphere.2015.09.102CrossRefPubMedGoogle Scholar
  100. Zecchin S, Corisi A, Martin M et al (2017) Rhizospheric iron and arsenic bacteria affected by water regime: implications for metalloid uptake by rice. Soil Biol Biochem 106:129–137.  https://doi.org/10.1016/j.soilbio.2016.12.021CrossRefGoogle Scholar
  101. Zhao R, Zhao M, Wang H et al (2006) Arsenic speciation in moso bamboo shoot – a terrestrial plant that contains organoarsenic species. Sci Total Environ 371:293–303.  https://doi.org/10.1016/j.scitotenv.2006.03.019CrossRefPubMedGoogle Scholar
  102. 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.  https://doi.org/10.1146/annurev-arplant-042809-112152CrossRefGoogle Scholar
  103. Zhu LJ, Guan DX, Luo J et al (2014) Characterization of arsenic-resistant endophytic bacteria from hyperaccumulators Pteris vittata and Pteris multifida. Chemosphere 113:9–16.  https://doi.org/10.1016/j.chemosphere.2014.03.081CrossRefPubMedGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • María del Carmen Molina
    • 1
    • 2
    Email author
  • James Francis WhiteJr
    • 2
  • Kathryn L. Kingsley
    • 2
  • Natalia González-Benítez
    • 1
  1. 1.Area de Biodiversidad y Conservación, Departamento de Biología, Geología, Física y Química InorgánicaUniversidad Rey Juan CarlosMadridSpain
  2. 2.Department of Plant BiologyRutgers UniversityNew BrunswickUSA

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