Abstract
Bacterial cells dwelling in the Polycyclic Aromatic Hydrocarbons (PAH) contaminated ecosystem occur as an eco-community or biofilms having biosurfactants and exopolymeric substances (EPS) producing capacity. Bacteria have developed several mechanisms to utilize the low accessible PAH compounds by modifying their structural and physiological process. EPS provides an adsorption site for PAH binding and acts as an emulsifier, enhancing PAH uptake in bacterial cells. Biosurfactants aid in the solubilization of the low-bioavailable carbon sources by reducing the interfacial surface tension between the aqueous phase and PAH-sorbent matrix, solubilizing PAHs thus making them bioavailable. Mining of exopolysaccharides synthesizing key genes (priming Glycosyltransferase) and biosurfactant producing genes (synthetases) in PAH degrading bacteriomes established their concomitant involvement in PAH solubilization and uptake. The transcriptional and translational regulators (secondary messenger cyclic-di-GMP, quorum sensing molecules, small ribosomal RNAs, two-component signaling molecules) control the synthesis of these ‘bioavailability enhancers’ towards PAH utilization and have been elucidated explicitly in the current review.
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Abdel-Shafy HI, Mansour MSM (2016) A review on polycyclic aromatic hydrocarbons: source, environmental impact, effect on human health and remediation. Egypt J Pet 25:107–123. https://doi.org/10.1016/j.ejpe.2015.03.011
Acet Ö, Erdönmez D, Acet BÖ, Odabaşı M (2021) N-acyl homoserine lactone molecules assisted quorum sensing: effects consequences and monitoring of bacteria talking in real life. Arch Microbiol 203(7):3739–3749. https://doi.org/10.1007/s00203-021-02381-9
Adamczak M, Odzimierz Bednarski W (2000) Influence of medium composition and aeration on the synthesis of biosurfactants produced by Candida antarctica. Biotechnol Lett 22(4):313–316. https://doi.org/10.1023/A:1005634802997
Ahmad F, Zhu D, Sun J (2020) Bacterial chemotaxis: a way forward to aromatic compounds biodegradation. Environ Sci Eur 32(1):1–8. https://doi.org/10.1186/s12302-020-00329-2
Ahmad Z, Zhang X, Imran M, Zhong H, Andleeb S, Zulekha R, Liu G, Ahmad I, Coulon F (2021) Production, functional stability, and effect of rhamnolipid biosurfactant from Klebsiella sp. on phenanthrene degradation in various medium systems. Ecotoxicol Environ Saf 207:111514. https://doi.org/10.1016/j.ecoenv.2020.111514
Arciola CR, Campoccia D, Ravaioli S, Montanaro L (2015) Polysaccharide intercellular adhesin in biofilm: structural and regulatory aspects. Front Cell Infect Microbiol 5:1–10. https://doi.org/10.3389/fcimb.2015.00007
Azubuike CC, Chikere CB, Okpokwasili GC (2016) Bioremediation techniques–classification based on site of application: principles, advantages, limitations and prospects. World J Microbiol Biotechnol 32(11):1–18. https://doi.org/10.1007/s11274-016-2137-x
Barcelos MCS, Vespermann KAC, Pelissari FM, Molina G (2020) Current status of biotechnological production and applications of microbial exopolysaccharides. Crit Rev Food Sci Nutr 60(9):1475–1495. https://doi.org/10.1080/10408398.2019.1575791
Benhabib K, Faure P, Sardin M, Simonnot MO (2010) Characteristics of a solid coal tar sampled from a contaminated soil and of the organics transferred into water. Fuel 89(2):352–359. https://doi.org/10.1016/j.fuel.2009.06.009
Beolchini F, Hekeu M, Amato A, Becci A, Ribeiro AB, Mateus EP, Dell’Anno A (2021) Bioremediation of sediments contaminated with polycyclic aromatic hydrocarbons: the technological innovation patented review. Int J Environ Sci Technol 20:1–24. https://doi.org/10.1007/s13762-021-03504-x
Berlanga M, Guerrero R (2016) Living together in biofilms: the microbial cell factory and its biotechnological implications. Microb Cell Fact 15(1):1–11. https://doi.org/10.1186/s12934-016-0569-5
Bezza FA, Chirwa EMN (2015) Production and applications of lipopeptide biosurfactant for bioremediation and oil recovery by Bacillus subtilis CN2. Biochem Eng J 101:168–178. https://doi.org/10.1016/j.bej.2015.05.007
Bezza FA, Chirwa EMN (2016) Bioremediation of polycyclic aromatic hydrocarbon contaminated soil by a microbial consortium through supplementation of biosurfactant produced by Pseudomonas aeruginosa strain. Polycycl Aromat Compd 36(5):848–872. https://doi.org/10.1080/10406638.2015.1066403
Bezza FA, Chirwa EMN (2017) The role of lipopeptide biosurfactant on microbial remediation of aged polycyclic aromatic hydrocarbons (PAHs)-contaminated soil. Chem Eng J 309:563–576. https://doi.org/10.1016/j.cej.2016.10.055
Bhandari S, Poudel DK, Marahatha R, Dawadi S, Khadayat K, Phuyal S, Shrestha S, Gaire S, Basnet K, Khadka U, Parajuli N (2021) Microbial enzymes used in bioremediation. J Chem. https://doi.org/10.1155/2021/8849512
Bhatt P, Verma A, Gangola S, Bhandari G, Chen S (2021) Microbial glycoconjugates in organic pollutant bioremediation: recent advances and applications. Microb Cell Fact 20(1):1–18. https://doi.org/10.1186/s12934-021-01556-9
Calvo C, Ferrer MR, Martinez-Checa F, Béjar V, Quesada E (1995) Some rheological properties of the extracellular polysaccharide produced by Volcaniella eurihalina F2–7. Appl Biochem Biotechnol 55(1):45–54. https://doi.org/10.1007/BF02788747
Carolin CF, Kumar PS, Ngueagni PT (2021) A review on new aspects of lipopeptide biosurfactant: types, production, properties and its application in the bioremediation process. J Hazard Mater 407:124827. https://doi.org/10.1016/j.jhazmat.2020.124827
Chakraborty J, Das S (2014) Characterization and cadmium-resistant gene expression of biofilm-forming marine bacterium Pseudomonas aeruginosa JP-11. Environ Sci Pollut Res 21(24):14188–14201. https://doi.org/10.1007/s11356-014-3308-7
Challis GL, Naismith JH (2004) Structural aspects of non-ribosomal peptide biosynthesis. Curr Opin Struct Biol 14(6):748–756. https://doi.org/10.1016/j.sbi.2004.10.005
Chambers JR, Sauer K (2013) Small RNAs and their role in biofilm formation. Trends Microbiol 21(1):39–49. https://doi.org/10.1016/j.tim.2012.10.008
Chanasit W, Gonzaga ZJC, Rehm BHA (2020) Analysis of the alginate O-acetylation machinery in Pseudomonas aeruginosa. Appl Microbiol Biotechnol 104(5):2179–2191. https://doi.org/10.1007/s00253-019-10310-6
Chandler JR, Duerkop BA, Hinz A, West TE, Herman JP, Churchill ME, Skerrett SJ, Greenberg EP (2009) Mutational analysis of Burkholderia thailandensis quorum sensing and self-aggregation. J Bacteriol 191(19):5901–5909. https://doi.org/10.1128/JB.00591-09
Chandran P, Das N (2011) Degradation of diesel oil by immobilized Candida tropicalis and biofilm formed on gravels. Biodegradation 22:1181–1189. https://doi.org/10.1007/s10532-011-9473-1
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 22:128–140. https://doi.org/10.1016/j.ibiod.2017.05.006
Chen W, Kong Y, Li J, Sun Y, Min J, Hu X (2020) Enhanced biodegradation of crude oil by constructed bacterial consortium comprising salt-tolerant petroleum degraders and biosurfactant producers. Int Biodeterior Biodegrad 154:105047. https://doi.org/10.1016/j.ibiod.2020.105047
Chirwa EMN, Lutsinge-Nembudani TB, Fayemiwo OM, Bezza FA (2021) Biosurfactant assisted degradation of high molecular weight polycyclic aromatic hydrocarbons by mixed cultures from a car service oil dump from Pretoria central business district (South Africa). J Clean Prod 290:125183. https://doi.org/10.1016/j.jclepro.2020.125183
Colvin KM, Alnabelseya N, Baker P, Whitney JC, Howell PL, Parsek MR (2013) PelA deacetylase activity is required for pel polysaccharide synthesis in pseudomonas aeruginosa. J Bacteriol 195(10):2329–2339. https://doi.org/10.1128/JB.02150-12
Costa OYA, Raaijmakers JM, Kuramae EE (2018) Microbial extracellular polymeric substances: ecological function and impact on soil aggregation. Front Microbiol 9:1636. https://doi.org/10.3389/fmicb.2018.01636
da Silva JA, Cardoso LG, de Jesus AD, Gomes GV, Oliveira MB, de Souza CO, Druzian JI (2018) Xanthan Gum Production by Xanthomonas campestris pv. campestris IBSBF 1866 and 1867 from Lignocellulosic Agroindustrial Wastes. Appl Biochem Biotechnol 186(3):750–763. https://doi.org/10.1007/s12010-018-2765-8
Das P, Mukherjee S, Sen R (2008) Genetic regulations of the biosynthesis of microbial surfactants: an overview. Biotechnol Genet Eng Rev 25(1):165–186. https://doi.org/10.5661/bger-25-165
de Gannes V, Hickey WJ (2017) Genetic adaptations of bacteria for metabolism of polycyclic aromatic hydrocarbons. In: Microbial ecotoxicology , Springer: Cham pp 133–164
de Oliveira JD, Carvalho LS, Gomes AM, Queiroz LR, Magalhães BS, Parachin NS (2016) Genetic basis for hyper production of hyaluronic acid in natural and engineered microorganisms. Microb Cell Fact 15(1):1–9. https://doi.org/10.1186/s12934-016-0517-4
Deng Z, Jiang Y, Chen K, Li J, Zheng C, Gao F, Liu X (2020) One biosurfactant-producing bacteria Achromobacter sp. A-8 and its potential use in microbial enhanced oil recovery and bioremediation. Front Microbiol 11:247. https://doi.org/10.3389/fmicb.2020.00247
Dignac MF, Urbain V, Rybacki D et al (1998) Chemical description of extracellular polymers: Implication on activated sludge floc structure. Water Sci Technol 38(8–9):45–53. https://doi.org/10.1016/S0273-1223(98)00676-3
Dogsa I, Brloznik M, Stopar D, Mandic-Mulec I (2013) Exopolymer diversity and the role of Levan in Bacillus subtilis biofilms. PLoS ONE 8(4):e62044. https://doi.org/10.1371/journal.pone.0062044
Dusane DH, Zinjarde SS, Venugopalan VP, Mclean RJ, Weber MM, Rahman PK (2010) Quorum sensing: implications on Rhamnolipid biosurfactant production. Biotechnol Genet Eng Rev 27(1):159–184. https://doi.org/10.1080/02648725.2010.10648149
El-Maradny A, El-Sherbiny MM, Ghandourah M, Bashir ME, Orif M (2021) PAH bioaccumulation in two polluted sites along the eastern coast of the Red Sea, Saudi Arabia. Int J Environ Sci Technol 18(6):1335–1348. https://doi.org/10.1007/s13762-020-02929-0
Esmaeel Q, Pupin M, Kieu NP, Chataigné G, Béchet M, Deravel J, Krier F, Höfte M, Jacques P, Leclère V (2016) Burkholderia genome mining for nonribosomal peptide synthetases reveals a great potential for novel siderophores and lipopeptides synthesis. Microbiology Open 5(3):512–526. https://doi.org/10.1002/mbo3.347
Evans E, Brown MRW, Gilbert P (1994) Iron chelator, exopolysaccharide and protease production in Staphylococcus epidermidis: a comparative study of the effects of specific growth rate in biofilm and planktonic culture. Microbiology 140(1):153–157. https://doi.org/10.1099/13500872-140-1-153
Falaleeva M, Zurek OW, Watkins RL, Reed RW, Ali H, Sumby P, Voyich JM, Korotkova N (2014) Transcription of the Streptococcus pyogenes hyaluronic acid capsule biosynthesis operon is regulated by previously unknown upstream elements. Infect Immun 82(12):5293–5307. https://doi.org/10.1128/IAI.02035-14
Fata Moradali M, Rehm BHA (2021) Microbial cell factories for biomanufacturing of polysaccharides. Biopolym Biomed Biotechnol Appl. https://doi.org/10.1002/9783527818310.ch3
Federle MJ, Scott JR (2002) Identification of binding sites for the group A streptococcal global regulator CovR. Mol Microbiol 43(5):1161–1172. https://doi.org/10.1046/j.1365-2958.2002.02810.x
Flemming HC (1993) Biofilms and environmental protection. Water Sci Technol 27(7–8):1–10. https://doi.org/10.2166/wst.1993.0528
Flemming HC, Wingender J, Szewzyk U, Steinberg P, Rice SA, Kjelleberg S (2016) Biofilms: an emergent form of bacterial life. Nat Rev Microbiol 14(9):563–575. https://doi.org/10.1038/nrmicro.2016.94
Freitas F, Alves VD, Reis MAM (2011) Advances in bacterial exopolysaccharides: from production to biotechnological applications. Trends Biotechnol 29(8):388–398. https://doi.org/10.1016/j.tibtech.2011.03.008
García-Delgado C, Fresno T, Rodríguez-Santamaría JJ, Diaz E, Mohedano AF, Moreno-Jimenez E (2019) Co-application of activated carbon and compost to contaminated soils toxic elements mobility and PAH degradation and availability. Int J Environ Sci Technol 16(2):1057–1068. https://doi.org/10.1007/s13762-018-1751-6
Ghaz-Jahanian MA, Khodaparastan F, Berenjian A, Jafarizadeh-Malmiri H (2013) Influence of small RNAs on biofilm formation process in bacteria. Mol Biotechnol 55(3):288–297. https://doi.org/10.1007/s12033-013-9700-6
Ghosal D, Ghosh S, Dutta TK, Ahn Y (2016) Current state of knowledge in microbial degradation of polycyclic aromatic hydrocarbons (PAHs): a review. Front Microbiol. https://doi.org/10.3389/fmicb.2016.01369
Ghosh S, Qureshi A, Purohit HJ (2017) Enhanced expression of catechol 1,2 dioxygenase gene in biofilm forming Pseudomonas mendocina EGD-AQ5 under increasing benzoate stress. Int Biodeterior Biodegrad 118:57–65. https://doi.org/10.1016/j.ibiod.2017.01.019
Gran-Scheuch A, Fuentes E, Bravo DM, Jiménez JC, Pérez-Donoso JM (2017) Isolation and characterization of phenanthrene degrading bacteria from diesel fuel-contaminated Antarctic soils. Front Microbiol. https://doi.org/10.3389/fmicb.2017.01634
Green ER, Mecsas J (2016) Bacterial secretion systems: an overview. Microbiol Spectr 4(1):4–1. https://doi.org/10.1128/microbiolspec.vmbf-0012-2015
Guo G, Tian F, Ding K, Wang L, Liu T, Yang F (2017) Effect of a bacterial consortium on the degradation of polycyclic aromatic hydrocarbons and bacterial community composition in Chinese soils. Int Biodeterior Biodegrad 123:56–62. https://doi.org/10.1016/j.ibiod.2017.04.022
Gupta B, Puri S, Thakur IS, Kaur J (2020) Enhanced pyrene degradation by a biosurfactant producing Acinetobacter baumannii BJ5: growth kinetics, toxicity and substrate inhibition studies. Environ Technol Innov 19:100804. https://doi.org/10.1016/j.eti.2020.100804
Gutierrez T, Berry D, Yang T, Mishamandani S, McKay L, Teske A, Aitken MD (2013) Role of bacterial exopolysaccharides (EPS) in the fate of the oil released during the deepwater horizon oil spill. PLoS ONE 8(6):e67717. https://doi.org/10.1371/journal.pone.0067717
Hall-Stoodley L, Costerton JW, Stoodley P (2004) Bacterial biofilms: from the natural environment to infectious diseases. Nat Rev Microbiol 2(2):95–108. https://doi.org/10.1038/nrmicro821
Haritash AK, Kaushik CP (2009) Biodegradation aspects of polycyclic aromatic hydrocarbons (PAHs): a review. J Hazard Mater 169(1–3):1–15. https://doi.org/10.1016/j.jhazmat.2009.03.137
Hawkins JP, Geddes BA, Oresnik IJ (2017) Succinoglycan production contributes to acidic ph tolerance in sinorhizobium meliloti Rm1021. Mol Plant-Microbe Interact 30(12):1009–1019. https://doi.org/10.1094/MPMI-07-17-0176-R
Hay ID, Wang Y, Moradali MF, Rehman ZU, Rehm BH (2014) Genetics and regulation of bacterial alginate production. Environ Microbiol 16(10):2997–3011. https://doi.org/10.1111/1462-2920.12389
Hengge R (2009) Principles of c-di-GMP signalling in bacteria. Nat Rev Microbiol 7:263–273. https://doi.org/10.1038/nrmicro2109
Hua X, Wu Z, Zhang H, Lu D, Wang M, Liu Y, Liu Z (2010) Degradation of hexadecane by Enterobacter cloacae strain TU that secretes an exopolysaccharide as a bioemulsifier. Chemosphere 80(8):951–956. https://doi.org/10.1016/j.chemosphere.2010.05.002
Hussain A, Zia KM, Tabasum S, Noreen A, Ali M, Iqbal R, Zuber M (2017) Blends and composites of exopolysaccharides; properties and applications: a review. Int J Biol Macromol 94:10–27. https://doi.org/10.1016/j.ijbiomac.2016.09.104
Ibrahim HMM (2018) Characterization of biosurfactants produced by novel strains of Ochrobactrum anthropi HM-1 and Citrobacter freundii HM-2 from used engine oil-contaminated soil. Egypt J Pet 27(1):21–29. https://doi.org/10.1016/j.ejpe.2016.12.005
Ibrar M, Zhang H (2020) Construction of a hydrocarbon-degrading consortium and characterization of two new lipopeptides biosurfactants. Sci Total Environ 714:136400. https://doi.org/10.1016/j.scitotenv.2019.136400
Ilori MO, Amobi CJ, Odocha AC (2005) Factors affecting biosurfactant production by oil degrading Aeromonas spp. isolated from a tropical environment. Chemosphere 61(7):985–992. https://doi.org/10.1016/j.chemosphere.2005.03.066
Janczarek M (2011) Environmental signals and regulatory pathways that influence exopolysaccharide production in rhizobia. Int J Mol Sci 12(11):7898–7933. https://doi.org/10.3390/ijms12117898
Jeckelmann JM, Erni B (2019) Carbohydrate transport by group translocation: the bacterial phosphoenolpyruvate: sugar phosphotransferase system. In: Kuhn A (ed) Bacterial cell walls and membranes. Subcellular biochemistry, vol 92. Springer, Cham, pp 223–274
Jimoh AA, Lin J (2019) Biosurfactant: a new frontier for greener technology and environmental sustainability. Ecotoxicol Environ Saf 184:109607. https://doi.org/10.1016/j.ecoenv.2019.109607
Jindal N, Singh Khattar J (2018) Microbial polysaccharides in food industry. In Biopolymers for food design, Academic Press, pp 95–123
Johnsen AR, Karlson U (2004) Evaluation of bacterial strategies to promote the bioavailability of polycyclic aromatic hydrocarbons. Appl Microbiol Biotechnol 63(4):452–459. https://doi.org/10.1007/s00253-003-1265-z
Johnsen AR, Wick LY, Harms H (2005) Principles of microbial PAH-degradation in soil. Environ Pollut 133(1):71–84. https://doi.org/10.1016/j.envpol.2004.04.015
Jorfi S, Rezaee A, Jaafarzadeh NA, Esrafili A, Akbari H, Moheb Ali GA (2014) Bioremediation of pyrene-contaminated soils using biosurfactant. Jentashapir J Heal Res. https://doi.org/10.17795/jjhr-23228
Kaczorek E, Pacholak A, Zdarta A, Smułek W (2018) The impact of biosurfactants on microbial cell properties leading to hydrocarbon bioavailability increase. Colloids Interfaces 2(3):35. https://doi.org/10.3390/colloids2030035
Karlapudi AP, Venkateswarulu TC, Tammineedi J, Kanumuri L, Ravuru L, Dirisala V, Kodali VP (2018) Role of biosurfactants in bioremediation of oil pollution-a review. Petroleum 4:241–249. https://doi.org/10.1016/j.petlm.2018.03.007
Kaur V, Bera MB, Panesar PS, Kumar H, Kennedy JF (2014) Welan gum: microbial production, characterization, and applications. Int J Biol Macromol 65:454–461. https://doi.org/10.1016/j.ijbiomac.2014.01.061
Ke CY, Lu GM, Li YB, Sun WJ, Zhang QZ, Zhang XL (2018) A pilot study on large-scale microbial enhanced oil recovery (MEOR) in Baolige Oilfield. Int Biodeterior Biodegrad 127:247–253. https://doi.org/10.1016/j.ibiod.2017.12.009
Kim YH, Freeman JP, Moody JD, Engesser KH, Cerniglia CE (2005) Effects of pH on the degradation of phenanthrene and pyrene by Mycobacterium vanbaalenii PYR-1. Appl Microbiol Biotechnol 67(2):275–285. https://doi.org/10.1007/s00253-004-1796-y
Kotoky R, Singha LP, Pandey P (2017) Draft genome sequence of polyaromatic hydrocarbon-degrading bacterium Bacillus subtilis SR1, which has plant growth-promoting attributes. Genome Announc 5(41):e01339-17. https://doi.org/10.1128/genomeA.01339-17
Kotoky R, Singha LP, Pandey P (2017) Draft genome sequence of heavy metal-resistant soil bacterium Serratia marcescens S2I7, which has the ability to degrade polyaromatic hydrocarbons. Genome Announc 5(48):e01338-17. https://doi.org/10.1128/genomeA.01338-17
Krell T, Lacal J, Reyes-Darias JA, Jimenez-Sanchez C, Sungthong R, Ortega-Calvo JJ (2013) Bioavailability of pollutants and chemotaxis. Curr Opin Biotechnol 24(3):451–456. https://doi.org/10.1016/j.copbio.2012.08.011
Kumar AS, Mody K, Jha B (2007) Bacterial exopolysaccharides - a perception. J Basic Microbiol 47(2):103–117. https://doi.org/10.1002/jobm.200610203
Kuppusamy S, Thavamani P, Megharaj M, Naidu R (2016) Biodegradation of polycyclic aromatic hydrocarbons (PAHs) by novel bacterial consortia tolerant to diverse physical settings - assessments in liquid- and slurry-phase systems. Int Biodeterior Biodegrad 108:149–157. https://doi.org/10.1016/j.ibiod.2015.12.013
Kuppusamy S, Thavamani P, Venkateswarlu K, Lee YB, Naidu R, Megharaj M (2017) Remediation approaches for polycyclic aromatic hydrocarbons (PAHs) contaminated soils: technological constraints, emerging trends and future directions. Chemosphere 168:944–968. https://doi.org/10.1016/j.chemosphere.2016.10.115
Lai IC, Lee CL, Ko FC, Lin JC, Huang HC (2015) Persistent organic pollutants in tropical coastal and offshore environment: part A—atmospheric polycyclic aromatic hydrocarbons. Int J Environ Sci Technol 12(3):1075–86. https://doi.org/10.1007/s13762-013-0482-y
Leech C, Tighe MK, Pereg L, Winter G, McMillan M, Esmaeili A, Wilson SC (2020) Bioaccessibility constrains the co-composting bioremediation of field aged PAH contaminated soils. Int Biodeterior Biodegrad 149:104922. https://doi.org/10.1016/j.ibiod.2020.104922
Li S, Pi Y, Bao M, Zhang C, Zhao D, Li Y, Sun P, Lu J (2015) Effect of rhamnolipid biosurfactant on solubilization of polycyclic aromatic hydrocarbons. Mar Pollut Bull 101(1):219–225. https://doi.org/10.1016/j.marpolbul.2015.09.059
Li J, Wang Y, Zhou W, Chen W, Deng M, Zhou S (2020) Characterization of a new biosurfactant produced by an effective pyrene-degrading Achromobacter species strain AC15. Int Biodeterior Biodegrad 152:104959. https://doi.org/10.1016/j.ibiod.2020.104959
Liu G, Zhong H, Yang X, Liu Y, Shao B, Liu Z (2018) Advances in applications of rhamnolipids biosurfactant in environmental remediation: a review. Biotechnol Bioeng 115(4):796–814. https://doi.org/10.1002/bit.26517
Lu XY, Zhang T, Fang HHP (2011) Bacteria-mediated PAH degradation in soil and sediment. Appl Microbiol Biotechnol 89(5):1357–1371. https://doi.org/10.1007/s00253-010-3072-7
Lu H, Wang W, Li F, Zhu L (2019) Mixed-surfactant-enhanced phytoremediation of PAHs in soil: bioavailability of PAHs and responses of microbial community structure. Sci Total Environ 653:658–666. https://doi.org/10.1016/j.scitotenv.2018.10.385
Luo L, Lin S, Huang H, Zhang S (2012) Relationships between aging of PAHs and soil properties. Environ Pollut 170:177–182. https://doi.org/10.1016/j.envpol.2012.07.003
Mahto KU, Das S (2020) Whole genome characterization and phenanthrene catabolic pathway of a biofilm forming marine bacterium Pseudomonas aeruginosa PFL-P1. Ecotoxicol Environ Saf 206:111087. https://doi.org/10.1016/j.ecoenv.2020.111087
Majdalani N, Gottesman S (2005) The Rcs phosphorelay: a complex signal transduction system. Annu Rev Microbiol 59:379–405. https://doi.org/10.1146/annurev.micro.59.050405.101230
Mangwani N, Kumari S, Das S (2015) Involvement of quorum sensing genes in biofilm development and degradation of polycyclic aromatic hydrocarbons by a marine bacterium Pseudomonas aeruginosa N6P6. Appl Microbiol Biotechnol 99(23):10283–10297. https://doi.org/10.1007/s00253-015-6868-7
Mangwani N, Shukla SK, Kumari S, Das S, Rao TS (2016) Effect of biofilm parameters and extracellular polymeric substance composition on polycyclic aromatic hydrocarbon degradation. RSC Adv 6(62):57540–57551. https://doi.org/10.1039/c6ra12824f
Matsuyama BY, Krasteva PV, Baraquet C, Harwood CS, Sondermann H, Navarro MV (2016) Mechanistic insights into c-di-GMP-dependent control of the biofilm regulator FleQ from Pseudomonas aeruginosa. Proc Natl Acad Sci 113(2):E209–E218. https://doi.org/10.1073/pnas.1523148113
McKew BA, Coulon F, Osborn AM, Timmis KN, McGenity TJ (2007) Determining the identity and roles of oil-metabolizing marine bacteria from the Thames estuary, UK. Environ Microbiol 9(1):165–176. https://doi.org/10.1111/j.1462-2920.2006.01125.x
Mishra M, Singh SK, Kumar A (2021) Environmental factors affecting the bioremediation potential of microbes. In: Microbe mediated remediation of environmental contaminants. Woodhead Publishing, pp 47–58
Mishra A, Jha B (2013) Microbial exopolysacchrides. In: Rosenberg E, DeLong EF, Thompson F, Lory S, Stackebrandt E (eds) The Prokaryotes: applied bacteriology and biotechnology, 4th edn. Springer, Berlin, pp 179–192
Moayed HK, Panahi M, Ghazizade MJ, Abedi Z, Ghaffarzadeh H (2021) Removal of PAH compounds from refinery industrial sludge as hazardous environmental contaminants through anaerobic digestion. Int J Environ Sci Technol 18(6):1617–1626. https://doi.org/10.1007/s13762-020-02904-9
More TT, Yadav JSS, Yan S, Tyagi RD, Surampalli RY (2014) Extracellular polymeric substances of bacteria and their potential environmental applications. J Environ Manage 144:1–25. https://doi.org/10.1016/j.jenvman.2014.05.010
Morgan JLW, McNamara JT, Zimmer J (2014) Mechanism of activation of bacterial cellulose synthase by cyclic di-GMP. Nat Struct Mol Biol 21(5):489–496. https://doi.org/10.1038/nsmb.2803
Moscovici M (2015) Present and future medical applications of microbial exopolysaccharides. Front Microbiol 6:1–11. https://doi.org/10.3389/fmicb.2015.01012
Nazirkar A, Wagh M, Qureshi A, Bodade R, Kutty R (2020) Development of tracking tool for p-nitrophenol monooxygenase genes from soil augmented with p-Nitrophenol degrading isolates: Bacillus Pseudomonas and Arthrobacter. Bioremediat J 24(1):71–79. https://doi.org/10.1080/10889868.2019.1672620
NCBI Resource Coordinators (2018) Database resources of the National Center for Biotechnology Information. Nucleic Acids Res 46(D1):D8–D13. https://doi.org/10.1093/nar/gkx1095
Nickzad A, Lépine F, Déziel E (2015) Quorum sensing controls swarming motility of Burkholderia glumae through regulation of rhamnolipids. PLoS ONE 10(6):e0128509. https://doi.org/10.1371/journal.pone.0128509
Oliveira JS, Araujo W, Lopes Sales AI, Brito Guerra AD, Silva Araújo SC, de Vasconcelos AT, Agnez-Lima LF, Freitas AT (2015) BioSurfDB: knowledge and algorithms to support biosurfactants and biodegradation studies. Database. https://doi.org/10.1093/database/bav033
Ossai IC, Ahmed A, Hassan A, Hamid FS (2020) Remediation of soil and water contaminated with petroleum hydrocarbon: a review. Environ Technol Innov 17:100526. https://doi.org/10.1016/j.eti.2019.100526
O’Toole G, Kaplan HB, Kolter R (2000) Biofilm formation as microbial development. Annu Rev Microbiol 54(1):49–79. https://doi.org/10.1146/annurev.micro.54.1.49
Patel AB, Shaikh S, Jain KR, Desai C, Madamwar D (2020) Polycyclic aromatic hydrocarbons: sources, toxicity, and remediation approaches. Front Microbiol. https://doi.org/10.3389/fmicb.2020.562813
Peng X, Yuan X, Liu H, Zeng GM, Chen XH (2015) Degradation of polycyclic aromatic hydrocarbons (PAHs) by Laccase in rhamnolipid reversed micellar system. Appl Biochem Biotechnol 176(1):45–55. https://doi.org/10.1007/s12010-015-1508-3
Perfumo A, Smyth T, Marchant R, Banat I (2010) Production and roles of biosurfactants and bioemulsifiers in accessing hydrophobic substrates. In: Timmis KN (ed) Handbook of hydrocarbon and lipid microbiology. Springer, Berlin, pp 1501–1512
Purohit HJ, Kapley A, Khardenavis A, Qureshi A, Dafale NA (2016) Insights in waste management bioprocesses using genomic tools. Adv Appl Microbiol 97:121–170. https://doi.org/10.1016/bs.aambs.2016.09.002
Qureshi A, Verma V, Kapley A, Purohit HJ (2007) Degradation of 4-nitroaniline by Stenotrophomonas strain HPC 135. Int Biodeterior Biodegrad 60(4):215–218. https://doi.org/10.1016/j.ibiod.2007.03.004
Qureshi A, Mohan M, Kanade GS, Kapley A, Purohit HJ (2009) In situ bioremediation of organochlorine-pesticide-contaminated microcosm soil and evaluation by gene probe. Pest Manag Sci Former Pestic Sci 65(7):798–804. https://doi.org/10.1002/ps.1757
Rambeloarisoa E, Rontani JF, Giusti G, Duvnjak Z, Bertrand JC (1984) Degradation of crude oil by a mixed population of bacteria isolated from sea-surface foams. Mar Biol 83(1):69–81. https://doi.org/10.1007/BF00393087
Reddy MS, Naresh B, Leela T, Prashanthi M, Madhusudhan NC, Dhanasri G, Devi P (2010) Biodegradation of phenanthrene with biosurfactant production by a new strain of Brevibacillus sp. Bioresour Technol 101(20):7980–7983. https://doi.org/10.1016/j.biortech.2010.04.054
Ren X, Zeng G, Tang L, Wang J, Wan J, Liu Y, Yu J, Yi H, Ye S, Deng R (2018) Sorption, transport and biodegradation – an insight into bioavailability of persistent organic pollutants in soil. Sci Total Environ 610:1154–1163. https://doi.org/10.1016/j.scitotenv.2017.08.089
Roca C, Alves VD, Freitas F, Reis MAM (2015) Exopolysaccharides enriched in rare sugars: bacterial sources, production, and applications. Front Microbiol 6:288. https://doi.org/10.3389/fmicb.2015.00288
Romeo T, Vakulskas CA, Babitzke P (2013) Post-transcriptional regulation on a global scale: form and function of Csr/Rsm systems. Environ Microbiol 15(2):313–324. https://doi.org/10.1111/j.1462-2920.2012.02794.x
Römling U, Galperin MY (2015) Bacterial cellulose biosynthesis: diversity of operons, subunits, products, and functions. Trends Microbiol 23(9):545–557. https://doi.org/10.1016/j.tim.2015.05.005
Rosenberg E, Ron EZ (1997) Bioemulsans: microbial polymeric emulsifiers. Curr Opin Biotechnol 8(3):313–316. https://doi.org/10.1016/S0958-1669(97)80009-2
Ruffing AM, Chen RR (2012) Transcriptome profiling of a curdlan-producing Agrobacterium reveals conserved regulatory mechanisms of exopolysaccharide biosynthesis. Microb Cell Fact 11(1):1–13. https://doi.org/10.1186/1475-2859-11-17
Sagarkar S, Bhardwaj P, Yadav TC, Qureshi A, Khardenavis A, Purohit HJ, Kapley A (2014) Draft genome sequence of atrazine-utilizing bacteria isolated from Indian agricultural soil. Genome Announc 2(1):e01149-e1213. https://doi.org/10.1128/genomeA.01149-13
Salama Y, Chennaoui M, Sylla A et al (2016) Characterization, structure, and function of extracellular polymeric substances (EPS) of microbial biofilm in biological wastewater treatment systems: a review. Desalin Water Treat 57(35):16220–16237. https://doi.org/10.1080/19443994.2015.1077739
Sałek K, Euston SR (2019) Sustainable microbial biosurfactants and bioemulsifiers for commercial exploitation. Process Biochem 85:143–155. https://doi.org/10.1016/j.procbio.2019.06.027
Schmid J, Sieber V, Rehm B (2015) Bacterial exopolysaccharides: biosynthesis pathways and engineering strategies. Front Microbiol 6:496. https://doi.org/10.3389/fmicb.2015.00496
Scott PM, Erickson KM, Troutman JM (2019) Identification of the functional roles of six key proteins in the biosynthesis of Enterobacteriaceae colanic acid. Biochemistry 58(13):1818–1830. https://doi.org/10.1021/acs.biochem.9b00040
Semple KT, Doick KJ, Wick LY, Harms H (2007) Microbial interactions with organic contaminants in soil: definitions, processes and measurement. Environ Pollut 150(1):166–176. https://doi.org/10.1016/j.envpol.2007.07.023
Sharma A, Singh SB, Sharma R, Chaudhary P, Pandey AK, Ansari R, Vasudevan V, Arora A, Singh S, Saha S, Nain L (2016) Enhanced biodegradation of PAHs by microbial consortium with different amendment and their fate in in-situ condition. J Environ Manage 181:728–736. https://doi.org/10.1016/j.jenvman.2016.08.024
Shekhar S, Sundaramanickam A, Balasubramanian T (2015) Biosurfactant producing microbes and their potential applications: a review. Crit Rev Environ Sci Technol 45(14):1522–1554. https://doi.org/10.1080/10643389.2014.955631
Shoaib M, Shehzad A, Omar M, Rakha A, Raza H, Sharif HR, Shakeel A, Ansari A, Niazi S (2016) Inulin: properties, health benefits and food applications. Carbohydr Polym 147:444–454. https://doi.org/10.1016/j.carbpol.2016.04.020
Shukla A, Mehta K, Parmar J, Pandya J, Saraf M (2019) Depicting the exemplary knowledge of microbial exopolysaccharides in a nutshell. Eur Polym J 119:298–310. https://doi.org/10.1016/j.eurpolymj.2019.07.044
Shukla SK, Mangwani N, Rao TS, Das S (2014) Biofilm-mediated bioremediation of polycyclic aromatic hydrocarbons. In: Microbial biodegradation and bioremediation. Elsevier Inc, pp 203–232
Singh SK, Haritash AK (2019) Polycyclic aromatic hydrocarbons: soil pollution and remediation. Int J Environ Sci Technol 16(10):6489–6512. https://doi.org/10.1007/s13762-019-02414-3
Soberón-Chávez G, González-Valdez A, Soto-Aceves MP, Cocotl-Yañez M (2021) Rhamnolipids produced by Pseudomonas: from molecular genetics to the market. Microb Biotechnol 14(1):136–146. https://doi.org/10.1111/1751-7915.13700
Sobrero PM, Valverde C (2020) Comparative genomics and evolutionary analysis of RNA-binding proteins of the CsrA family in the Genus Pseudomonas. Front Mol Biosci. https://doi.org/10.3389/fmolb.2020.00127
Sobrinho HB, Luna JM, Rufino RD, Porto AL, Sarubbo LA (2014) Biosurfactants: classification, properties and environmental applications. Biotechnology 11(14):1–29. https://doi.org/10.3390/ijms150712523
Sousa SA, Feliciano JR, Pinheiro PF, Leitão JH (2013) Biochemical and functional studies on the Burkholderia cepacia complex bceN gene, encoding a GDP-D-mannose 4, 6-dehydratase. PloS One 8(2):e56902. https://doi.org/10.1371/journal.pone.0056902
Souza EC, Vessoni-Penna TC, de Souza Oliveira RP (2014) Biosurfactant-enhanced hydrocarbon bioremediation: an overview. Int Biodeterior Biodegrad 89:88–94. https://doi.org/10.1016/j.ibiod.2014.01.007
Sun L, Zang SY, Sun HJ (2014) Sources and history of PAHs in lake sediments from oil-producing and industrial areas, northeast China. Int J Environ Sci Technol 11(7):2051–2060. https://doi.org/10.1007/s13762-013-0396-8
Tabassum N, Asaduzzaman SA, Ullah AA (2021) Genetic and biochemical aspects of quorum sensing in the bacterial lifestyle and pathogenesis. Life Res 4(2):14. https://doi.org/10.12032/life2021-0401-0331
Tikariha H, Pal RR, Qureshi A, Kapley A, Purohit HJ (2016) In silico analysis for prediction of degradative capacity of Pseudomonas putida SF1. Gene 591(2):382–392. https://doi.org/10.1016/j.gene.2016.06.028
Tribedi P, Sil AK (2014) Cell surface hydrophobicity: a key component in the degradation of polyethylene succinate by Pseudomonas sp. AKS2. J Appl Microbiol 116(2):295–303. https://doi.org/10.1111/jam.12375
Tripathi V, Gaur VK, Dhiman N, Gautam K, Manickam N (2020) Characterization and properties of the biosurfactant produced by PAH-degrading bacteria isolated from contaminated oily sludge environment. Environ Sci Pollut Res 27(22):27268–27278. https://doi.org/10.1007/s11356-019-05591-3
Turakhia MH, Characklis WG (1989) Activity of Pseudomonas aeruginosa in biofilms: effect of calcium effect of calcium. Biotechnol Bioeng 33(4):406–414. https://doi.org/10.1002/bit.260330405
Van Kranenburg R, Vos HR, Van Swam II, Kleerebezem M, De Vos WM (1999) Functional analysis of glycosyltransferase genes from Lactococcus lactis and other gram-positive cocci: complementation, expression, and diversity. J Bacteriol 181(20):6347–6353. https://doi.org/10.1128/jb.181.20.6347-6353.1999
Varjani SJ, Upasani VN (2017) A new look on factors affecting microbial degradation of petroleum hydrocarbon pollutants. Int Biodeterior Biodegrad 120:71–83. https://doi.org/10.1016/j.ibiod.2017.02.006
Wang H, Jiang R, Kong D, Liu Z, Wu X, Xu J, Li Y (2020) Transmembrane transport of polycyclic aromatic hydrocarbons by bacteria and functional regulation of membrane proteins. Front Environ Sci Eng 14(1):1–21. https://doi.org/10.1007/s11783-019-1188-2
Whitfield C (2006) Biosynthesis and assembly of capsular polysaccharides in Escherichia coli. Annu Rev Biochem 75:39–68. https://doi.org/10.1146/annurev.biochem.75.103004.142545
Wolska KI, Grudniak AM, Rudnicka Z, Markowska K (2016) Genetic control of bacterial biofilms. J Appl Genet 57(2):225–238. https://doi.org/10.1007/s13353-015-0309-2
Xia W, Du Z, Cui Q, Dong H, Wang F, He P, Tang Y (2014) Biosurfactant produced by novel Pseudomonas sp. WJ6 with biodegradation of n-alkanes and polycyclic aromatic hydrocarbons. J Hazard Mater 276:489–498. https://doi.org/10.1016/j.jhazmat.2014.05.062
Xiao-Hong PE, Xin-Hua ZH, Shi-Mei WA, Yu-Suo LI, Li-Xiang ZH (2010) Effects of a biosurfactant and a synthetic surfactant on phenanthrene degradation by a Sphingomonas strain. Pedosphere 20(6):771–779
Yan S, Wu G (2020) Uptake of polycyclic aromatic hydrocarbons across bacterial membrane. Adv Microbiol 10(7):331–348. https://doi.org/10.4236/aim.2020.107024
Yesankar PJ, Qureshi A, Purohit HJ (2022) Biofilm-mediated biodegradation of hydrophobic organic compounds in the presence of metals as co-contaminants. In: Microbial biodegradation and bioremediation, 2nd edn. Elsevier, pp. 441–460
Yin Y, Hu Y, Xiong F (2013) Biosorption properties of Cd(II), Pb(II), and Cu(II) of extracellular polymeric substances (EPS) extracted from Aspergillus fumigatus and determined by polarographic method. Environ Monit Assess 185(8):6713–6718. https://doi.org/10.1007/s10661-013-3059-9
Yu S, Wei Q, Zhao T, Guo Y, Ma LZ (2016) A survival strategy for Pseudomonas aeruginosa that uses exopolysaccharides to sequester and store iron to stimulate psl-dependent biofilm formation. Appl Environ Microbiol 82(21):6403–6413. https://doi.org/10.1128/AEM.01307-16
Zhang Y, Wang F, Bian Y, Kengara FO, Gu C, Zhao Q, Jiang X (2012) Enhanced desorption of humin-bound phenanthrene by attached phenanthrene-degrading bacteria. Bioresour Technol 123:92–97. https://doi.org/10.1016/j.biortech.2012.07.093
Zhang D, Zhu L, Li F (2013) Influences and mechanisms of surfactants on pyrene biodegradation based on interactions of surfactant with a Klebsiella oxytoca strain. Bioresour Technol 142:454–461. https://doi.org/10.1016/j.biortech.2013.05.077
Zhang Y, Wang F, Zhu X, Zeng J, Zhao Q, Jiang X (2015) Extracellular polymeric substances govern the development of biofilm and mass transfer of polycyclic aromatic hydrocarbons for improved biodegradation. Bioresour Technol 193:274–280. https://doi.org/10.1016/j.biortech.2015.06.110
Zhang M, Shen X, Zhang H, Cai F, Chen W, Gao Q, Ortega-Calvo JJ, Tao S, Wang X (2016) Bioavailability of phenanthrene and nitrobenzene sorbed on carbonaceous materials. Carbon 110:404–413. https://doi.org/10.1016/j.carbon.2016.09.044
Acknowledgements
The authors acknowledge CSIR-NEERI, Nagpur for providing the necessary infrastructure facilities. Prerna J Yesankar would like to thank the Academy of Scientific and Innovative Research (AcSIR) to provide a platform to pursue scientific research and Department of Biotechnology (DBT), Government of India, to grant financial support (DBT/JRF/BET-16/I/2016/AL/72) for doctoral work. The manuscript was checked for plagiarism using i-Thenticate software at the NEERI Knowledge Resource Centre (KRC No- NEERI/KRC/2021/JUNE/EBGD/3).
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Yesankar, P.J., Pal, M., Patil, A. et al. Microbial exopolymeric substances and biosurfactants as ‘bioavailability enhancers’ for polycyclic aromatic hydrocarbons biodegradation. Int. J. Environ. Sci. Technol. 20, 5823–5844 (2023). https://doi.org/10.1007/s13762-022-04068-0
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DOI: https://doi.org/10.1007/s13762-022-04068-0