eISSN: 2221-6197 DOI: 10.31301/2221-6197

Potential of plants and microorganisms to degrade polycyclic aromatic hydrocarbons

Year: 2018

Pages: 193-201

Number: Volume 10, issue 2

Type: scientific article

Summary:

Polycyclic aromatic hydrocarbons (PAHs) are a broad group of compounds containing two or more condensed benzene rings in the molecule and are some of the most widespread and dangerous environmental pollutants. PAHs are formed by abiogenic and anthropogenic processes, among which human activity associated with the incomplete combustion of organic raw materials (oil, coal, peat, wood, garbage, tobacco, etc.) makes the most significant contribution. PAHs can be degraded by members of almost all kingdoms of living organisms: bacteria, fungi, plants, and animals. The different chemical structures of PAHs and the variety of organisms interacting with these pollutants determine the multiplicity of metabolic pathways and intermediates formed during their biodegradation. Bacteria metabolize PAHs mostly with oxygenases. Various byproducts form that can be further transformed to water and carbon dioxide by the enzyme systems of both the same organism and other members of the biocenosis, including fungi and plants. Fungi (e.g., ascomycetes and basidiomycetes) degrade PAHs with cytochrome P-450 monooxygenases and/or laccases and peroxidases. These are enzymes of the ligninolytic complex that degrade lignin. PAHs are implicated in lignin degradation; in this case, fungi form quinones at the early stages of oxidation and are capable of complete mineralization of PAHs. Plants also have a pool of extracellular enzymes exuded into the rhizosphere. First, these are peroxidases (enzymes of stress protection), which can oxidize both native PAHs (in the presence of mediators) and PAH intermediates from bacterial and fungal decomposition. There is evidence that plants can also assimilate the carbon of the PAH molecules. The above processes were shown by us in the study of the metabolism of phenanthrene by the rhizosphere bacterium Ensifer meliloti P221 (IBPPM 383), alfalfa (Medicago sativa L.) and sorghum (Sorghum bicolor L. Moench), and the fungi Pleurotus ostreatus and Fusarium oxysporum. Studies of the degradation potential of microorganisms and plants are necessary not only for understanding natural processes but also for improving the phytoremediation technology.

 

Keywords:

biodegradation, enzymes, bacteria, plants, fungi, polycyclic aromatic hydrocarbons (PAHs)

References:

  1. Atlas R.M., Bartha R. Microbial ecology: fundamentals and applications. – Don Mills (ON): Benjamin/Cummings Publishing Company Inc. 1998. 433 p.
  2. Bezalel L., Hadar Y., Fu P.P., Freeman J.P., Cerniglia C.E. Initial oxidation products in the metabolism of pyrene, anthracene, fluorene, and dibenzothiophene by the white rot fungus Pleurotus ostreatus. Environ. Microbiol. 1996. V.62. P. 2554–2559.
  3. Baboshin M.A., Golovleva L.A. Aerobic bacterial degradation of polycyclic aromatic hydrocarbons (PAHs) and its kinetic aspects. Microbiologiya. V. 81(6). P. 639-650. (In Russian - Бабошин М.А., Головлева Л.А. Деградация полициклических ароматических углеводородов (ПАУ) аэробными бактериями и ее кинетические аспекты. Микробиология. 2012. Т. 81(6). С. 695–706.
  4. Cerniglia C.E., Sutherland J.B. Degradation of polycyclic aromatic hydrocarbons by fungi. In Handbook of Hydrocarbon and Lipid Microbiology. Eds K.N. Timmis, T.J. McGenity, J.R. van der Meer, and V.de Lorenzo. Berlin: Springer. 2010. P. 2080–2110.
  5. Chasov A.V., Alekseeva V.Ya., Kolesnikov O.P., Minibayeva F.V. Activation of extracellular peroxidase of wheat roots under the Action of xenobiotics. Biochem. Microbiol. 2010. V. 46(4). P. 431-437). (In Russian - Часов А.В., Алексеева В.Я., Колесников О.П., Минибаева Ф.В. Активация экстраклеточной пероксидазы корней пшеницы при действии ксенобитиков. Прикл. биохим. микробиол. 2010. Т. 46. С. 472-478.)
  6. Criquet S., Joner E., Leglize P., Leyval C. Anthracene and mycorrhiza affect the activity of oxidoreductases in the roots and the rhizosphere of lucerne (Medicago sativa). Biotechnol. Lett. 2000. V. 22. P. 1733-1737.
  7. Dubrovskaya E., Pozdnyakova N., Golubev S., Muratova A., Grinev V., Bondarenkova A., Turkovskaya O. Peroxidases from root exudates of Medicago sativa and Sorghum bicolor: catalytic properties and involvement in PAH degradation. Chemosphere. 2017. V. 169. P. 224–232. doi: 10.1016/j.chemosphere.2016.11.027
  8. Dubrovskaya E., Pozdnyakova N., Golubev S., Grinev V., Turkovskaya O. Peroxidases from alfalfa roots: catalytic properties and participation in degradation of polycyclic aromatic hydrocarbons. J. Plant Physiol. 2017. V. 64(2). С. 174–183. doi: 10.1134/S1021443717010058 (In Russian - Дубровская Е., Позднякова Н., Голубев С., Гринев В., Турковская О. Пероксидазы из корней люцерны: каталитические свойства и участие в деградации полициклических ароматических углеводородов. Физиология растений. 2017. Т. 64(2). С. 116–126.)
  9. Dubrovskaya E.V., Pozdnyakova N.N., Grinev V.S., Muratova A.Yu., Golubev S.N., Bondarenkova A.D., and Turkovskaya O.V. Dominant form of cationic peroxidase from sorghum roots. Rus. J. Plant Physiol. V. 63(3). P. 338–348. doi: 10.1134/S1021443716030055 (In Russian - Дубровская Е.В., Позднякова Н.Н., Гринев В.С., Муратова А.Ю., Голубев С.Н., Бондаренкова А.Д., Турковская О.В. Доминирующая форма катионной пероксидазы из корней сорго веничного. Физиология растений. 2016. Т. 63(3). С. 359–371.)
  10. Durairaj P., Hur J.‑S., Yun H. Versatile biocatalysis of fungal cytochrome P450 monooxygenases. Microb. Cell. Fact. 2016. V. 15(125). P. 2-16. DOI1186/s12934-016-0523-6
  11. Durmishidze S., Ugrehelidze D., Dzhikija A.N. Fiziologija i biohimija kul'turnyh rastenij. J. Plant. Physiol. 1974. V. 6. S. 217-221. [Physiology and biochemistry of cultivated plants]. (In Russian - Дурмишидзе С., Угрехелидзе Д., Джикия А.Н. Физиология и биохимия культурных растений. Физиология растений. 1974. Т. 6. С. 217-221.)
  12. El Amrani, Dumas A-S., Wick L.Y., Yergeau E., Berthomé R. “Omics” insights into PAH degradation toward Improved green remediation biotechnologies. Environ. Sci. Technol. 2015. V. 49(19). P. 11281–11291.
  13. Ghosal D., Ghosh S., Dutta T.K., Ahn Y. Current state of knowledge in microbial degradation of polycyclic aromatic hydrocarbons (PAHs): A Review. Microbiol. 2016. 7:1369. doi: 10.3389/fmicb.2016.01369
  14. Golovleva L.A., Kolomytseva M., Baboshin M.A., Ponomareva O.N. Rol' mikroorganizmov v transformacii ustojchivyh organicheskih polljutantov: Uchebnoe posobie. – Tula: Izd-vo TulGU, 2008. 100 s. [The role of microorganisms in the transformation of persistent organic pollutants: A Tutorial] (In Russian - Головлева Л.А., Коломыцева М.П., Бабошин М.А., Понаморева О.Н. Роль микроорганизмов в трансформации устойчивых органических поллютантов: Учебное пособие. – Тула: Изд-во ТулГУ, 2008. 100 c.)
  15. Gordeziani M.Sh., Hatisashvili G.A., Kurashvili M.V. Raspredelenie NADF-citohrom R450-reduktazy v rastitel'noj kletke. AN GSSR. 1991. T. 143. S. 321-324. [Distribution of NADP-cytochrome P450-reductase in a plant cell]. (In Russian - Гордезиани М.Ш., Хатисашвили Г.А., Курашвили М.В. Распределение НАДФ-цитохром Р450-редуктазы в растительной клетке. Сообщ. АН ГССР. 1991. Т.143. С. 321-324.)
  16. Grąz M., Jarosz-Wilkołazka A., Janusz G., Mazur A., Wielbo J., Koper P., Żebracki K., Kubik-Komarc A. Transcriptome-based analysis of the saprophytic fungus Abortiporus biennis – response to oxalic acid. Microbiol. Research. 2017. V. 199. P. 79-88. doi.org/10.1016/j.micres.2017.03.002
  17. Günther T., Sack U., Hofrichter M., Lätz M. Oxidation of PAH and PAH-derivatives by fungal and plant oxidoreductases. Basic Microbiol. 1998. V. 38(2). P. 113-122.
  18. Izmalkova T.Ju. Raznoobrazie geneticheskih sistem katabolizma naftalina shtammov fluorescirujushhih psevdomonad. ... kand. biol. nauk. Pushhino. 2004. 129 s. (In Russian) [Diversity of genetic systems of naphthalene catabolism in fluorescent pseudomonad strains]. (In Russian - Измалкова Т.Ю. Разнообразие генетических систем катаболизма нафталина штаммов флуоресцирующих псевдомонад. Дис. ... канд. биол. наук. Пущино. 2004. 129 c.)
  19. Jambon I., Thijs S., Weyens N., Vangronsveld J. Harnessing plant-bacteria-fungi interactions to improve plant growth and degradation of organic pollutants. Plant Interact. 2018. V. 13(1). P. 119-130. DOI: 10.1080/17429145.2018.1441450
  20. Kvesitadze G.I., Hatisashvili G.A., Sadunishvili T.A., Evstigneeva Z.G. Metabolizm antropogennyh toksikantov v vysshih rastenijah. : Nauka, 2005. 199 s. (In Russian) [Metabolism of anthropogenic toxicants in higher plants]. (In Russian - Квеситадзе Г.И., Хатисашвили Г.А., Садунишвили Т.А., Евстигнеева З.Г. Метаболизм антропогенных токсикантов в высших растениях. М.: Наука, 2005. 199 с.)
  21. Karich A., Ullrich R., Scheibner K., Hofrichter M. Fungal unspecific peroxygenases oxidize the majority of organic EPA priority pollutants. Microbiol. 2017. V.8:1463. doi: 10.3389/fmicb.2017.014631
  22. Kraus J.J., Munir I.Z., McEldoon J.P., Clark D.S., Dordick J.S. Oxidation of polycyclic aromatic hydrocarbons catalyzed by soybean peroxidase // Biochem. Biotechnol. 1999. V. 80. P. 221-230
  23. Li X., Lin X., Zhang J., Wu Y., Yin R., Feng Y., Wang Y.. Degradation of polycyclic aromatic hydrocarbons by crude extracts from spent mushroom substrate and its possible mechanisms. Microbiol. 2010. V. 60(5). P. 336-42. doi: 10.1007/s00284-009-9546-0
  24. Meckenstock R.U., Safinowski M., Griebler C. Anaerobic degradation of polycyclic aromatic hydrocarbons. FEMS Microbiol Ecol. V. 49(1). P. 27-36. doi: 10.1016/j.femsec.2004.02.019
  25. Muratova A., Dubrovskaya E., Golubev S., Grinev V., Chernyshova M., Turkovskaya O. The coupling of the plant and microbial catabolisms of phenanthrene in the rhizosphere of Medicago sativa. Plant Physiol. 2015. V. 188. P. 1–8. doi: 10.1016/j.jplph.2015.07.014.
  26. Muratova A., Pozdnyakova N., Makarov O., Baboshin M., Baskunov B, Myasoedova N., Golovleva L., Turkovskaya O. Degradation of phenanthrene by the rhizobacterium Ensifer meliloti. Biodegradation. 2014. V. 25(6). P. 787-795. doi: 10.1007/s10532-014-9699-9
  27. Muratova A.Yu., Golubev S.N., Dubrovskaya E.V., Pozdnyakova N.N., Panchenko L.V., Pleshakova E.V., Chernyshova M.P., Turkovskaya O.V. Remediating abilities of different plant species grown in diesel-fuel-contaminated leached chernozem. Soil Ecol. 2012. V. 56. P. 51-57.
  28. Nikitina O.V. Vnekletochnye oksidoreduktazy ligninoliticheskogo kompleksa bazidial'nogo griba Trametes pubescens (Schumach.) Pilat. … dis. kand. biol. nauk. Moskva. 2006. 24 s. [Extracellular oxidoreductases of the ligninolytic complex of the basidiomycete Trametes pubescens (Schumach.) Pilat]. (In Russian - Никитина О.В. Внеклеточные оксидоредуктазы лигнинолитического комплекса базидиального гриба Trametes pubescens (Schumach.) Pilat. Автореф. … дис. канд. биол. наук. Москва. 2006. 24 c.)
  29. Pozdnyakova N.N., Balandina S.A., Dubrovskaya E.V., Golubev C.N., Turkovskaya O.V. Ligninolytic basidiomycetes as promising organisms for the mycoremediation of PAH-contaminated environments. IOP Conf. Series: Earth and Environmental Science. 2017. 107:012071 doi :10.1088/1755-1315/107/1/012071
  30. Pozdnyakova N.N., Chernyshova M.P., Grinev V.S., Landesman E.O., Koroleva O.V., Turkovskaya O.V. Degradation of Fluorene and Fluoranthene by the Basidiomycete Pleurotus ostreatus. Appl. Biochem. Microbiol. 2016. V. 52(6). P. 621–628. DOI: 10.1134/S0003683816060132 (In Russian - Позднякова Н.Н., Чернышова М.П., Гринёв В.С., Ландесман Е.О., Королёва О.В., Турковская О.В. Деградация флуорена и флуорантена базидиомицетом Pleurotus ostreatus. Прикл. биохим. микробиол. 2016. Т. 52(6). С. 590-598.)
  31. Pozdnyakova N.N., Chernyshova M.P., Grinev V.S., Landesman E.O., Koroleva O.V., Turkovskaya O.V. Degradation of Fluorene and Fluoranthene by the Basidiomycete Pleurotus ostreatus. Appl. Biochem. Microbiol. 2016. V. 52(6). P. 621–628. DOI: 10.1134/S0003683816060132 (In Russian - Позднякова Н.Н., Чернышова М.П., Гринёв В.С., Ландесман Е.О., Королёва О.В., Турковская О.В. Деградация флуорена и флуорантена базидиомицетом Pleurotus ostreatus. Прикл. биохим. микробиол. 2016. Т. 52(6). С. 590-598.)
  32. Pozdnyakova N.N., Nikiforova S.V., Turkovskaya O.V. Influence of PAHs on ligninolytic enzymes of the fungus Pleurotus ostreatus Cent. Eur. J. Biol. 2010. V. 5(1). P. 83-94.
  33. Pozdnyakova N.N., Rodakiewicz-Nowak J., Turkovskaya O.V., Haber J. Oxidative degradation of polyaromatic hydrocarbons catalysed by blue laccase from Pleurotus ostreatus D1 in the presence of synthetic mediators. Enzyme Microb. Technol. 2006. V. 39(6). P.1242-1249
  34. Rovinskij F.Ja., Teplickaja T.A., Alekseeva T.A. Fonovyj monitoring policiklicheskih aromaticheskih uglevodorodov. : Gidrometioizdat, 1988. 224 s. [Background monitoring of polycyclic aromatic hydrocarbons]. (In Russian - Ровинский Ф.Я., Теплицкая Т.А., Алексеева Т.А. Фоновый мониторинг полициклических ароматических углеводородов. Л.: Гидрометиоиздат, 1988. 224 с.
  35. Seo J.S., Keum Y.S. Li Q.X. Bacterial degradation of aromatic compounds. J. Environ. Res. Public Health. 2009. V.6. P.278-309. doi:10.3390/ijerph6010278
  36. Tortella G.R., Diez M.C., Duran N. Fungal diversity and use in decomposition of environmental pollutants. Rev. Microbiol. 2005. V. 31. P. 197–212. doi: 10.1080/10408410500304066
  37. Wu Y-R., Luo Z-H., Vrijmoed L.L.P. Biodegradation of anthracene and benz[a]anthracene by two Fusarium solani strains isolated from mangrove sediments. Bioresource Technology. 2010. V. 101. P. 9666–9672.
Download pdf
up
eISSN: 2221-6197 DOI: 10.31301/2221-6197