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Biodegradation of polycyclic aromatic hydrocarbons (PAHs) in a diesel oil-contaminated mangrove by plant growth-promoting rhizobacteria

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Abstract

In this study, Rhizophora mangle L. mangrove plants and plant growth-promoting bacteria were evaluated for their ability to degrade polycyclic aromatic hydrocarbons in diesel oil-contaminated sediment. The diesel-contaminated soil was sown with plant growth-promoting bacteria in the R. mangle L. rhizosphere and monitored for 120 days in a greenhouse. The plant growth-promoting bacteria Pseudomonas aeruginosa and Bacillus sp. were analyzed for their ability to degrade eight priority polycyclic aromatic hydrocarbons, achieving a removal rate for naphthalene (80%), acenaphthene (> 60%), anthracene (> 50%), benzo(a)anthracene (> 60%), benzo(a)pyrene (> 50%) and dibenzo(a,h)anthracene (> 90%) in the treatments with and without plants. R. mangle L. demonstrated a removal rate above 50% for acenaphthene and fluoranthene. The bacterial strains promoted the development of the plant propagule in 55% of sediment contaminated with diesel. Scanning electron microscopy revealed the formation of biofilms by the strains in the roots of the plants in contact with the diesel. Thus, the interaction between Rhizophora mangle L. and the bacterial strains (Bacillus sp. and P. aeruginosa) demonstrated the potential of the strains to degrade diesel and bioremediate mangroves impacted by diesel oil.

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References

  • Al-Baldawi IA, Abdullah SRS, Anuar N, Suja F, Mushrifah I (2015) Phytodegradation of total petroleum hydrocarbon (TPH) in diesel-contaminated water using Scirpus grossus. Ecol Eng 74:463–473

    Google Scholar 

  • Alongi DM (2002) Present state and future of the world’s mangrove forests. Environ Conserv 29:331–349

    Google Scholar 

  • Arslan M, Imran A, Khan QM, Afzal M (2017) Plant–bacteria partnerships for the remediation of persistent organic pollutants. Environ Sci and Pollut Res 24:4322–4336

    Google Scholar 

  • Ayed HB, Jemil N, Maalej H, Bayoudh A, Hmidet N, Nasri M (2015) Enhancement of solubilization and biodegradation of diesel oil by biosurfactant from Bacillus amyloliquefaciens An6. Int Biodeterior Biodegrad 99:8–14

    Google Scholar 

  • Bamforth SM, Singleton I (2005) Bioremediation of polycyclic aromatic hydrocarbons: current knowledge and future directions. J Chem Technol Biotechnol 80:723–736

    Google Scholar 

  • Barathi S, Vasudevan N (2001) Utilization of petroleum hydrocarbons by Pseudomonas aeruginosa isolated from a petroleum-contaminated soil. Environ Int 26:413–416

    Google Scholar 

  • Bezza FA, Chirwa EMN (2016) Biosurfactant-enhanced bioremediation of aged polycyclic aromatic hydrocarbons (PAH’s) in creosote contaminated soil. Chemosphere 144:635–644

    Google Scholar 

  • Boizard SD, Mitchell SJ (2011) Resistance of red mangrove (Rhizophora mangle L.) seedlings to deflection and extraction. Trees 25:371–381

    Google Scholar 

  • Borja A, Basset A, Bricker S, Dauvin J, Elliot M, Harrison T, Marques JC, Weisberg S, West R (2011) Classifying ecological quality and integrity of estuaries. Treat Est Coast Sci 1:125–162

    Google Scholar 

  • Cerniglia CE (1993) Biodegradation of polycyclic aromatic hydrocarbons. Curr Opin Biotechnol 4:331–338

    Google Scholar 

  • Cerqueira VS, Hollenbach EB, Maboni F, Vainstein MH, Camargo FAO, Peralba MCR, Bento FM (2011) Biodegradation potential of oily sludge by pure and mixed bacterial cultures. Bioresour Technol 102:11003–11010

    Google Scholar 

  • Chebbi A, Hentati D, Zaghden H, Baccar N, Rezgui F, Chalbi M, Sayadi S, Chamkha M (2017) Polycyclic aromatic hydrocarbon degradation and biosurfactant production by a newly isolated Pseudomonas sp. strain from used motor oil-contaminated soil. Int Biodeterior Biodegrad 122:128–140

    Google Scholar 

  • Chin-A-Woeng TFC, de Priester W, van der Bij AJ, Lugtenberg BJJ (1997) Description of the colonization of a gnotobiotic tomato rhizosphere by Pseudomonas fluorescens biocontrol strain WCS365, using scanning electron microscopy. Mol Plant Microbe Interact 10:79–86

    Google Scholar 

  • Chindah AC, Braide SA, Amakiri JO, Onokurhefe J (2008) Effect of crude oil on the development of white mangrove seedlings (Avicennia germinans) in the Niger delta, Nigeria. Biologia 30:77–90

    Google Scholar 

  • Colares GB, Melo VMM (2013) Relating microbial community structure and environmental variables in mangrove sediments inside Rhizophora mangle L habitats. Appl Soil Ecol 64(171):177

    Google Scholar 

  • Danhorn T, Fuqua C (2007) Biofilm formation by plant-associated bacteria. Annu Rev Microbiol 61:401–422

    Google Scholar 

  • Das M, Das SK, Mukherjee RK (1998) Surface active properties of the culture filtrates of a Micrococcus species grown on n-alkanes and sugars. Bioresour Technol 63:231–235

    Google Scholar 

  • Desai JD, Banat IM (1997) Microbial production of surfactants and their commercial potential. Microbiol Mol Biol Rev 61:47–64

    Google Scholar 

  • Duke NC, Allen JA (2006) Rhizophora mangle, R. samoensis, R. racemosa, R. x harrisonii (Atlantic–East Pacific red mangroves). Species Profiles for Pac Isl Agrofor 1:1–18

    Google Scholar 

  • Ely CS, Smets BF (2017) Bacteria from wheat and cucurbit plant roots metabolize PAHs and aromatic root exudates: implications for rhizodegradation. Int J Phytoremed 19:877–883

    Google Scholar 

  • Farias V, Maranho LT, Vasconcelos EC, Filho MAS, Lacerda LG, Azevedo JAM, Pandey A, Soccol CR (2009) Phytodegradation potential of Erythrina crista-galli L., Fabaceae, in petroleum-contaminated soil. Appl Biochem Biotechnol 157:10–22

    Google Scholar 

  • Fernández MD, Pro J, Alonso C, Aragonese P, Tarazona JV (2011) Terrestrial microcosms in a feasibility study on the remediation of diesel-contaminated soils. Ecotoxicol Environ Saf 74:2133–2140

    Google Scholar 

  • Fiechter A (1992) Biosurfactants, moving toward industrial application. Trends Biotechnol 10:208–217

    Google Scholar 

  • Haritash AK, Kaushik CP (2009) Biodegradation aspects of polycyclic aromatic hydrocarbons (PAHs): a review. J Hazard Mater 169:1–15

    Google Scholar 

  • Haritash AK, Kaushik CP (2016) Degradation of low molecular weight polycyclic aromatic hydrocarbons by microorganisms isolated from contaminated soil. Int J Environ Sci 6:472–482

    Google Scholar 

  • Hou J, Liu W, Wang B, Wang Q, Luo Y, Franks AE (2015) PGPR enhanced phytoremediation of petroleum contaminated soil and rhizosphere microbial community response. Chemosphere 138:592–598

    Google Scholar 

  • Huang XD, El-Alawi Y, Gurska J, Glick BR, Greenberg BM (2005) A multi-process phytoremediation system for decontamination of persistent total petroleum hydrocarbons (TPHs) from soils. Microchem J 81:139–147

    Google Scholar 

  • Isaac P, Martínez FL, Bourguignon N, Sánchez LA, Ferrero MA (2015a) Improved PAHs removal performance by a defined bacterial consortium of indigenous Pseudomonas and actinobacteria from Patagonia, Argentina. Int Biodeterior Biodegrad 101:23–31

    Google Scholar 

  • Isaac P, Lozada M, Diosini HM, Estévez MC, Ferrero MA (2015b) Differential expression of the catabolic nahAc gene and its effect on PAH degradation in Pseudomonas strains isolated from contaminated Patagonian coasts. Int Biodeterior Biodegrad 105:1–6

    Google Scholar 

  • Izmalkova TY, Sazonova OI, Nagornih MO, Sokolov SL, Kosheleva IA, Boronin AM (2013) The organization of naphthalene degradation genes in Pseudomonas putida strain AK5. Res Microbiol 164:244–253

    Google Scholar 

  • Kechavarzi C, Pettersson K, Leeds-Harrison P, Richie L, Ledin S (2007) Root establishment of perennial ryegrass (L. perenne) in diesel contaminated subsurface soil layers. Environ Pollut 145:68–74

    Google Scholar 

  • Khan S, Afzal M, Iqbal S, Khan QM (2013) Plant–bacteria partnerships for the remediation of hydrocarbon contaminated soils. Chemosphere 90:1317–1332

    Google Scholar 

  • Kong F, Sun G, Liu Z (2018) Degradation of polycyclic aromatic hydrocarbons in soil mesocosms by microbial/plant bioaugmentation: performance and mechanism. Chemosphere 198:83–91

    Google Scholar 

  • Kuiper I, Lagendijk EL, Bloemberg GV, Lugtenberg JJ (2004) Rhizoremediation: a beneficial plant-microbe interaction. Mol Plant Microbe Interact 17:6–15

    Google Scholar 

  • Lang FS, Destain J, Delvigne F, Druart P, Ongena M, Thonart P (2016) Characterization and evaluation of the potential of a diesel-degrading bacterial consortium isolated from fresh mangrove sediment. Water Air Soil Pollut 227:58–77

    Google Scholar 

  • Lin C, Gan L, Chen ZL (2010) Biodegradation of naphthalene by strain Bacillus fusiformis (BFN). J Hazard Mater 182:771–777

    Google Scholar 

  • Maila MP, Cloete TE (2002) Germination of Lepidium sativum as a method to evaluate polycyclic aromatic hydrocarbons (PAHs) removal from contaminated soil. Int Biodeterior Biodegrad 50:107–113

    Google Scholar 

  • Moreira ITA, Oliveira OMC, Triguis JA, Santos AMP, Queiroz AFS, Martins CMS, Silva CS, Jesus RS (2011) Phytoremediation using Rhizophora mangle L. in mangrove sediments contaminated by persistent total petroleum hydrocarbons (TPH’s). Microchem J 99:376–382

    Google Scholar 

  • Mucha AP, Almeida CMR, Magalhães CM, Vasconcelos MTSD, Bordalo AA (2011) Salt marsh plant–microorganism interaction in the presence of mixed contamination. Int Biodeterior Biodegrad 65:326–333

    Google Scholar 

  • Naidoo G (2016) Mangrove propagule size and oil contamination effects: does size matter? Mar Poll Bull 110:362–370

    Google Scholar 

  • Nwinyi OC, Ajayi OO, Amund OO (2016) Degradation of polynuclear aromatic hydrocarbons by two strains of Pseudomonas. Braz J Microbiol 47:551–562

    Google Scholar 

  • Orge MDR, Porsché IJ, Costa MC, Lima JS, Soares SED, Justino R (2000) Assessment of oil refinery waste on Rhizophora mangle L. seedling growth in mangroves of Todos os Santos Bay, Bahia, Brazil. Aquat Ecosyst Health Manag 3:471–477

    Google Scholar 

  • Pathak H, Kantharia D, Malpani A, Madamwar D (2009) Naphthalene degradation by Pseudomonas spp. HOB1: in vitro studies and assessment of naphthalene degradation efficiency in simulated microcosms. J Hazard Mater 166:1466–1473

    Google Scholar 

  • Sánchez-Arias LE, Remolina DA, Alvarez-León R (2013) Evaluation of a recovery technique for mangrove soils affected by oil spills, using as indicator plantules of Rhizophora mangle L. (Rhizophoraceae). Panam J Aquat Sci 8:79–88

    Google Scholar 

  • Santos HF, Carmo FL, Paes JES, Rosado AS, Peixoto RS (2011) Bioremediation of mangroves impacted by petroleum. Water Air Soil Pollut 216:329–350

    Google Scholar 

  • Schaeffer-Novelli Y (1995) Manguezal: ecossistema entre a terra e o mar. Caribbean Ecological Research, São Paulo

    Google Scholar 

  • Sharma D, Ansari MJ, Al-Ghamdi A, Adgaba N, Khan KA, Pruthi V, Al-Waili N (2015) Biosurfactant production by Pseudomonas aeruginosa DSVP20 isolated from petroleum hydrocarbon-contaminated soil and its physicochemical characterization. Environ Sci Pollut Res 22:17636–17643

    Google Scholar 

  • Singh SN, Kumari B, Upadhyay SK, Mishra S, Kumar D (2013) Bacterial degradation of pyrene in minimal salt medium mediated by catechol dioxygenases: enzyme purification and molecular size determination. Bioresour Technol 133:293–300

    Google Scholar 

  • Tam NFY, Guo CL, Yau WY, Wong YS (2002) Preliminary study on biodegradation of phenanthrene by bacteria isolated from mangrove sediments in Hong Kong. Mar Pollut Bull 45:1–12

    Google Scholar 

  • Tomás-Gallardo L, Gómez-Álvarez H, Santero E, Floriano B (2014) Combination of degradation pathways for naphthalene utilization in Rhodococcus sp. strain TFB. Microb Biotechnol 7:100–113

    Google Scholar 

  • Trivedi S, Ansari AA (2015) Molecular mechanisms in the phytoremediation of heavy metals from coastal waters. Phytoremed Manag Environ Contam 2:219–231

    Google Scholar 

  • US Environmental Protection Agency (1984) Health Effects Assessment for Polycyclic Aromatic Hydrocarbons (PAH). Environmental Criteria and Assessment Office. EPA 540/1-86-013, Washington DC

  • US Environmental Protection Agency (US EPA) (1982) Appendix A to PART 423-126 priority pollutants

  • US Environmental Protection Agency (US EPA) (1996) EPA 3630C Silica gel cleanup. Revision 3. US EPA, Washington, DC

    Google Scholar 

  • US Environmental Protection Agency (US EPA) (2007) EPA 3550C Ultrasonic extraction. Revision 2. US EPA, Washington, DC

    Google Scholar 

  • Visser EJW, Nabben RHM, Blom CWPM, Voesenek LACJ (1997) Elongation by primary lateral roots and adventitious roots during conditions of hypoxia and high ethylene concentration. Plant Cell Environ 20:647–653

    Google Scholar 

  • Whang Z, Liu Z, Yang Y, Li T, Liu M (2012) Distribution of PAHs in tissues of wetland plants and the surrounding sediments in the Chongming wetland, Shanghai, China. Chemosphere 89:221–227

    Google Scholar 

  • Xia W, Du Z, Cui Q, Dong H, Wang F, He P, Tang Y (2014) Biosurfactant produced by novel Pseudomonas spp. WJ6 with biodegradation of n-alkanes and polycyclic aromatic hydrocarbons. J Hazard Mater 276:489–498

    Google Scholar 

  • Zhang Y, Miller RM (1994) Effect of a Pseudomonas rhamnolipids biosurfactant on cell hydrophobicity and biodegradation of octadecane. Appl Environ Microbiol 60:2101–2106

    Google Scholar 

  • Zhang X, Whang Z, Liu X, Hu X, Liang X, Hu Y (2013) Degradation of diesel pollutants in Huangpu-Yangtze River estuary wetland using plant-microbe systems. Int Biodeterior Biodegrad 76:71–75

    Google Scholar 

  • Zhuang X, Chen J, Shim H, Bai Z (2007) New advances in plant growth-promoting rhizobacteria for bioremediation. Environ Int 33:406–413

    Google Scholar 

Download references

Acknowledgements

The authors would like to thank the Coordination for the Improvement of Higher Education Personnel-CAPES for the financial support in this study.

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Authors and Affiliations

  1. Laboratório de Microbiologia Aplicada e Bioprospecção, Departamento de Biointeração, Instituto de Ciências da Saúde, Universidade Federal da Bahia (UFBA), Campus Canela, Salvador, Bahia, 40110-100, Brazil

    Carla J. S. Sampaio, Aldinéia O. Damião, Thiago C. Bahiense & Milton R. A. Roque

  2. Laboratório de Física Nuclear Aplicada, Departamento de Física da Terra e do Meio Ambiente, Instituto de Física, Universidade Federal da Bahia (UFBA), Campus Ondina, Salvador, Bahia, 40170-140, Brazil

    José R. B. de Souza

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  1. Carla J. S. Sampaio
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  2. José R. B. de Souza
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  4. Thiago C. Bahiense
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Correspondence to Milton R. A. Roque.

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Sampaio, C.J.S., de Souza, J.R.B., Damião, A.O. et al. Biodegradation of polycyclic aromatic hydrocarbons (PAHs) in a diesel oil-contaminated mangrove by plant growth-promoting rhizobacteria. 3 Biotech 9, 155 (2019). https://doi.org/10.1007/s13205-019-1686-8

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