Fungi as potential tool for polluted port sediment remediation

Abstract

Contaminated sediments represent an important management problem that also concerns their remediation. Indeed, port dredging activities produce huge volumes of contaminated sediments that, in turn, require proper handling because of their quantity of inorganic and organic substances. Conventional management-remediation strategies of polluted sediment involve sediment washing, electron-chemical separation, and thermal treatment. Recently, bioremediation strategies have also been proposed as a promising answer to the problem of contaminated sediments. In this context, fungi are pioneer microorganisms known to bioconcentrate, bioaccumulate, and biostabilize heavy metals. These capabilities suggest the potential to employ indigenous fungal strains to remediate polluted port sediments. In the framework of the European Project SEDITERRA (Guidelines for the sustainable treatment of dredged sediments in the Marittimo area), the aim of this paper is to characterize the fungal communities of port sediments of Genoa and present an innovative mycoremediation protocol to evaluate the capability of indigenous fungal strains in the heavy metal remediation. In this study, Penicillium expansum Link and Paecilomyces formosus (Sakag., May. Inoue & Tada) Houbraken & Samson have been selected as fungal species for the mycoremediation treatments. The protocol requires a fungal membrane system and the results highlight efficient bioremoval of Cu and Zn from sediments.

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References

  1. Abdollahi S, Raoufi Z, Faghiri I, Savari A, Nikpour Y, Mansouri A (2013) Contamination levels and spatial distributions of heavy metals and PAHs in surface sediment of Imam Khomeini Port, Persian Gulf, Iran. Mar Pollut Bull 71:336–345

    CAS  Google Scholar 

  2. Aftab K, Akhtar K, Kausar A, Khaliq S, Nisar N, Umbreen H, Iqbal M (2017) Fungal strains isolation, identification and application for the recovery of Zn (II) ions. J Photochem Photobiol B 175:282–290

    CAS  Google Scholar 

  3. Akcil A, Erust C, Ozdemiroglu S, Fonti V, Beolchini F (2015) A review of approaches and techniques used in aquatic contaminated sediments: metal removal and stabilization by chemical and biotechnological processes. J Clean Prod 86:24–36

    CAS  Google Scholar 

  4. Bensch K, Groenewald JZ, Dijksterhuis J, Starink-Willemse M, Andersen B, Summerell BA, Shin HD, Dugan FM, Schroers HJ, Braun U, Crous PW (2010) Species and ecological diversity within the Cladosporium cladosporoides complex (Davidiellaceae, Capnoidiales). Stud Mycol 67(1):1–94

    CAS  Google Scholar 

  5. Bensch K, Braun U, Groenewald J, Crous P (2012) The genus Cladosporium. Stud Mycol 72:1–401

    CAS  Google Scholar 

  6. Bhakuni DS and Rawat DS (2006) Bioactive Marine Natural Products. Springer Science & Business Media.

  7. Bissett J (1984) A revision of the genus Trichoderma. I. Section Longibrachiatum sect. Nov. Can J Bot 62(5):924–931

    Google Scholar 

  8. Bissett J (1991a) A revision of the genus Trichoderma. II. Infrageneric classification. Can J Bot 69(11):2357–2372

    Google Scholar 

  9. Bissett J (1991b) A revision of the genus Trichoderma. III. Section Pachybasium. Can J Bot 69(11):2373–2417

    Google Scholar 

  10. Bissett J (1991c) A revision of the genus Trichoderma. IV. Additional notes on section Longibrachiatum. Can J Bot 69(11):2418–2420

    Google Scholar 

  11. Brierley CL (2010) Biohydrometallurgical prospects. Hydrometallurgy 104(3-4):324–328

    CAS  Google Scholar 

  12. Buruaem LM, Hortellani MA, Sarkis JE, Costa-Lotufo LV, Abessa DMS (2012) Contamination of port zone sediments by metals from Large Marine Ecosystems of Brazil. Mar Pollut Bull 64:479–488

    CAS  Google Scholar 

  13. Capello M, Cutroneo L, Consani S, Dinelli E, Vagge G, Carbone C (2016) Marine sediment contamination and dynamics at the mouth of a contaminated torrent: the case of the Gromolo Torrent (Sestri Levante, north-western Italy). Mar Pollut Bull 109:128–141

    CAS  Google Scholar 

  14. Caplat C, Texier H, Barillier D, Lelievre C (2015) Heavy metals mobility in harbor contaminated sediments: the case of Port-en-Bessin. Mar Pollut Bull 50:504–511

    Google Scholar 

  15. Cecchi G, Marescotti P, Di Piazza S, Zotti M (2017a) Native fungi as metal remediators: silver mycoaccumulation from metal contaminated wasterock dumps (Libiola Mine, Italy). J Environ Sci Health B 52(3):191–195

    CAS  Google Scholar 

  16. Cecchi G, Roccotiello E, Di Piazza S, Riggi A, Mariotti MG, Zotti M (2017b) Assessment of Ni accumulation capability by fungi for a possible approach to remove metals from soils and waters. J Environ Sci Health B 52(3):166–170

    CAS  Google Scholar 

  17. Cecchi G, Marescotti P, Di Piazza S, Lucchetti G, Mariotti MG, Zotti M (2018) Gypsum biomineralization in sulphide-rich hardpans by a native Trichoderma harzianum Rifai strain. Geomicrobiol J 35(3):209–214

    CAS  Google Scholar 

  18. Coates JD, Woodward J, Allen J, Philp P, Lovley DR (1997) Anaerobic degradation of polycyclic aromatic hydrocarbons and alkanes in petroleum-contaminated marine harbor sediments. Appl Environ Microbiol 63(9):3589–3593

    CAS  Google Scholar 

  19. Crous PW, Braun U, Schubert K, Groenewald JZ (2007) Delimiting Cladosporium from morphologically similar genera. Stud Mycol 58(1):33–56

    CAS  Google Scholar 

  20. Cruz A, Anselmo AM, Suzuki S, Mendo S (2015) Tributyltin (TBT): A review on microbial resistance and degradation. Environ Sci Technol 45(9):970–1006

    CAS  Google Scholar 

  21. Cutroneo L, Massa F, Castellano M, Canepa G, Costa S, Povero P, Tucci S, Capello M (2014) Technical and public approaches to involve dredging stakeholders and citizens in the development of a port area. Environ Earth Sci 72:3159–3171

    Google Scholar 

  22. Cutroneo L, Castellano M, Carbone C, Consani S, Gaino F, Tucci S, Magrì S, Povero P, Bertolotto RM, Canepa G, Capello M (2015) Evaluation of the boundary condition influence on PAH concentrations in the water column during the sediment dredging of a port. Mar Pollut Bull 101:583–593

    CAS  Google Scholar 

  23. Cutroneo L, Carbone C, Consani S, Vagge G, Canepa G, Capello M (2017) Environmental complexity of a port: evidence from circulation of the water masses, and composition and contamination of bottom sediments. Mar Pollut Bull 119:184–194

    CAS  Google Scholar 

  24. Damare S, Singh P, Raghukumar S (2012) Biotechnology of marine fungi. Prog Mol Subcell Biol 53:277–297

    Google Scholar 

  25. Dermont G, Bergeron M, Mercier G, Richer-Lafleche M (2008) Soil washing for metal removal: a review of physical/chemical technologies and field applications. J Hazard Mater 152:1–31

    CAS  Google Scholar 

  26. Dhankhar R, Hooda A (2011) Fungal biosorption–an alternative to meet the challenges of heavy metal pollution in aqueous solutions. Environ Technol 32(5):467–491

    CAS  Google Scholar 

  27. Di Piazza S, Cecchi G, Cardinale AM, Carbone C, Mariotti MG, Giovine M, Zotti M (2017) Penicillium expansum Link strain for a biometallurgical method to recover REEs from WEEE. Waste Manag 60:596–600

    Google Scholar 

  28. Domsch KH, Gams W, Anderson TH (2007) Compendium of soil fungi, 2nd taxonomically revised edition by W." Gams. IHW, Eching.

  29. Doyle JJ, Doyle JL (1987) A rapid DNA isolation procedure for small quantities of fresh leaf tissues. Phytochem Bull 19:11–15

    Google Scholar 

  30. Falandysz J, Mędyk M, Treu R (2018) Bio-concentration potential and associations of heavy metals in Amanita muscaria (L.) Lam. from northern regions of Poland. Environ Sci Pollut Res 25:25190–25206

    CAS  Google Scholar 

  31. Fathollahzadeh H, Kaczala F, Bhatnagar A, Hogland W (2014) Speciation of metals in contaminated sediments can enhance metal mobility due to changes of bacterial diversity. Water Res 68:637–650

    Google Scholar 

  32. Fomina M, Gadd GM (2014) Biosorption: current perspectives on concept, definition and application. Bioresour Technol 160:3–14

    CAS  Google Scholar 

  33. Fonti V, Beolchini F, Rocchetti L, Dell'Anno A (2015) Bioremediation of contaminated marine sediments from Oskarshamn Harbor, Oskarshamn, Sweden. Environ Sci Pollut R 21:2455–2464

    Google Scholar 

  34. Gadd GM, Rhee YJ, Stephenson K, Wei Z (2012) Geomycology: metals, actinides and biominerals. Environ Microbiol Rep 4(3):270–296

    CAS  Google Scholar 

  35. Garcia-Orellana J, Cañas L, Masqué P, Obrador B, Olid C, Pretus J (2011) Chronological reconstruction of metal contamination in the Port of Maó (Minorca, Spain). Mar Pollut Bull 62:1632–1640

    CAS  Google Scholar 

  36. Gardes M, Bruns TD (1993) ITS primers with enhanced specificity for basidiomycetes application to the identification of mycorrhizae and rusts. Mol Ecol 2(2):113–118

    CAS  Google Scholar 

  37. Glass NL, Donaldson GC (1995) Development of primer sets designed for used with the PCR to amplify conserved genes from filamentous ascomycetes. Appl Environ Microbiol 61(4):1323–1330

    CAS  Google Scholar 

  38. Goltapeh EM, Danesh YR, Varma A (2013) (Eds.). Fungi as bioremediators (Vol. 32). Springer Science & Business Media.

  39. Greco G, Cecchi G, Di Piazza S, Cutroneo L, Capello M, Zotti M (2018) Fungal characterisation of a contaminated marine environment: the case of the Port of Genoa (North-Western Italy). Webbia 73(1):97–106

    Google Scholar 

  40. Howe P, Watts P (2005) Tin and inorganic tin compounds. Concise International Chemical Assessment Document 65. World Health Organization, pp. 81.

  41. Iannelli R, Bianchi V, Macci C, Peruzzi E, Chiellini C, Petroni G, Masciandaro G (2012) Assessment of pollution impact on biological activity and structure of seabed bacterial communities in the Port of Livorno (Italy). Sci Total Environ 426:56–64

    CAS  Google Scholar 

  42. Italian Ministerial Decree 56 of 14 April 2009. Criteri tecnici per il monitoraggio dei corpi idrici – Articolo 75, Dlgs 152/2006.

  43. Johnson DB (2013) Development and application of biotechnologies in the metal mining industry. Environ Sci Pollut R 20:7768–7776

    Google Scholar 

  44. Klich MA (2002) Identification of common Aspergillus species, Utrecht, Netherlands: Centraalbureau voor Schimmelcultures 116 pp..

  45. Kohlmeyer J, Kohlmeyer E (1979) Marine Mycology: The Higher Fungi. Academic Press, New York, p 690

    Google Scholar 

  46. Li WW, Yu HQ (2015) Stimulating sediment bioremediation with benthic microbial fuel cells. Biotechnol Adv 33:1–12

    Google Scholar 

  47. Li M, Tian X, Liu RZ, Chen WL, Cai P, Rong XM, Dai K, Huang QY (2014) Combined application of rice straw and fungus Penicillium Chrysogenum to remediate heavy-metal-contaminated. Soil Sediment Contam 23(3):328–338

    CAS  Google Scholar 

  48. Malik A (2004) Metal bioremediation through growing cells. Environ Int 30(2):261–278

    CAS  Google Scholar 

  49. Mulligan CN, Yong RN, Gibbs BF (2001) An evaluation of technologies for the heavy metal remediation of dredged sediments. J Hazard Mater 85:145–163

    CAS  Google Scholar 

  50. OSPAR Commission (2014) OSPAR Guidelines for the Management of Dredged Material at Sea. Draft Summary Record - EIHA, Annex 7, pp. 34. https://dredging.org/media/ceda/org/documents/guidance/ospar/ospar-dredged-materialguidelines_for%20london-2014.pdf

  51. Peng J-F, Song Y-H, Yuan P, Cui X-Y, Qiu G-L (2009) The remediation of heavy metals contaminated sediment. J Hazard Mater 161:633–640

    CAS  Google Scholar 

  52. Pitt JL (1979) The genus Penicillium and its teleomorphic states Eupenicillium and Talaromyces. Academic Press, New York, 634 pp..

  53. Ram C (1968) Timber-attacking fungi from the State of Maranhao, Brazil. Some new species of Paecilomyces and its perfect stage Byssochlamys Westl. VIII. Nova Hedwigia 16:305–314

    Google Scholar 

  54. Raper KB, Fennel DI (1965) The genus Aspergillus. The Williams & Wilkins Co., Baltimore, 686 pp..

  55. Rifai MA (1969) A revision of the genus Trichoderma. Mycol Pap 166:1–56

    Google Scholar 

  56. Roccotiello E, Marescotti P, Di Piazza S, Cecchi G, Mariotti MG, Zotti M (2015) Biodiversity in metal contaminated sites—problem and perspective—a case study. In: Lo YH, Blanco JA, Roy S (eds) Biodiversity in Ecosystems—Linking Structure and Function. InTech, Rijeka, pp 581–600

    Google Scholar 

  57. Ruiz CE, Schroeder PR (2007) Capping Design Approaches for Contaminated Sediments and Dredging Residuals: Engineered Reduction in Bioavailability. Fifth LACCEI International Latin American and Caribbean Conference for Engineering and Technology (LACCEI’2007), “Developing Entrepreneurial Engineers for the Sustainable Growth of Latin America and the Caribbean: Education, Innovation, Technology and Practice”. 29 May – 1 June 2007, Tampico, México.

  58. Samson RA, Houbraken J, Varga J, Frisvad JC (2009) Polyphasic taxonomy of the heat resistant ascomycete genus Byssochlamys and its Paecilomyces anamorphs. Persoonia 22:14–27

    CAS  Google Scholar 

  59. Samson RA, Houbraken J, Rane U, Frisvad JC, Andersen B (2010) Food and indoor fungi. CBS Laboratory Manual Series 2. 390 p. ISBN: 978-90-70351-82-3.

  60. Samson SA, Varga J, Frisvad JC (2011) Taxonomic studies on the genus Aspergillus. Stud Mycol 69:1–97

    Google Scholar 

  61. Svobodová K, Novotný Č (2018) Bioreactors based on immobilized fungi: bioremediation under non-sterile conditions. Appl Microbiol Biotechnol 102:39–46

    Google Scholar 

  62. Tabak HH, Lens P, Hullebusch ED, Dejonghe W (2008) Developments in bioremediation of soils and sediments polluted with metals and radionuclides. Microbial processes and mechanisms affecting bioremediation of metal contamination and influencing metal toxicity and transport. Rev Environ Sci Biotechnol 4:115–156

    Google Scholar 

  63. Tavakoly Sany SB, Salleh A, Rezayi M, Saadati N, Narimany L, Tehrani GM (2013) Distribution and contamination of heavy metal in the coastal sediments of port Klang, Selangor, Malaysia. Water Air Soil Pollut 224(4):1–18

    CAS  Google Scholar 

  64. U.S. EPA (1996) Method 3050B: Acid Digestion of Sediments, Sludges, and Soils. Revision 2. Washington, DC, pp. 12.

  65. U.S. EPA. (2014) Method 6010D (SW-846): Inductively Coupled Plasma-Atomic Emission Spectrometry. Revision 4. Washington, DC, pp. 35.

  66. Vagge G, Cutroneo L, Castellano M, Canepa G, Bertolotto RM, Capello M (2018) The effects of dredging and environmental conditions on concentrations of polycyclic aromatic hydrocarbons in the water column. Mar Pollut Bull 135:704–713

    CAS  Google Scholar 

  67. Walker TR, MacAskill D, Weaver P (2013a) Environmental recovery in Sidney Harbour, Nova Scotia: evidence of natural and anthropogenic sediment capping. Mar Pollut Bull 74:446–452

    CAS  Google Scholar 

  68. Walker TR, MacLean B, Appleton R, McMillan S, Miles M (2013b) Cost-effective sediment dredge disposal options for small craft harbours in Canada. Remediat J 23(4):123–140

    Google Scholar 

  69. Wang JN, Li A, Yang JX, Wang JH, Guo JB, Ma F, Shi SN, Zhang S, Ren NQ (2013) Mycelial pellet as the biomass carrier for semi-continuous production of bioflocculant. RSC Adv 3:18414–18423

    CAS  Google Scholar 

  70. Wang L, Chen L, Tsang DCW, Li J-S, Baek K, Hou D, Ding S, Poon C-S (2018) Recycling dredged sediment into fill materials, partition blocks, and paving blocks: technical and economic assessment. J Clean Prod 199:69–76. https://doi.org/10.1016/j.jclepro.2018.07.165

    CAS  Article  Google Scholar 

  71. White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: PCR protocols: a guide to methods and applications, pp 315–322

    Google Scholar 

  72. Zotti M, Di Piazza S, Roccotiello E, Lucchetti G, Mariotti MG, Marescotti P (2014) Microfungi in highly copper-contaminated soils from an abandoned Fe–Cu sulphide mine: growth responses, tolerance and bioaccumulation. Chemosphere 117:471–476

    CAS  Google Scholar 

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Funding

The present study was funded by the European Interreg Italy-France 2014-2020 Maritime Project SEDITERRA “Guidelines for the sustainable treatment of dredged sediments in the Marittimo area” (CUP I42F17000010006).

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Cecchi, G., Vagge, G., Cutroneo, L. et al. Fungi as potential tool for polluted port sediment remediation. Environ Sci Pollut Res 26, 35602–35609 (2019). https://doi.org/10.1007/s11356-019-04844-5

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Keywords

  • Dredged sediment
  • Fungi
  • Contaminants
  • Mycoremediation
  • Heavy metals
  • Bioaccumulation