Metagenomic Characterization of Heavy Metal-Fungal Microbiota Interaction in Pinus brutia Needles

Authors

DOI:

https://doi.org/10.24925/turjaf.v12i9.1523-1529.6590

Keywords:

Environmental Mycology, Fungal diversity, Heavy metal pollution, Metagenomics, Samsun OIZ, Pinus brutia

Abstract

Fungi are considered an effective method as an alternative solution in the biological remediation of heavy metals. The aim of the study was to determine comparative heavy metal concentrations in Pinus brutia needles taken from Samsun Organized Industrial Zone which have been contaminated with heavy metals for a long time and Adalar Forest region, and to evaluate the fungal mycobiome that could be potential bioremediators. As a result of the study, Cu, Pb, Zn, Mn, Cr, Cd, Ni, Se, As, Li, V and Co elements were analyzed in the needle samples, and the concentrations of Ni, As, Li, V and Co among these elements remained below the detectable limits. For all other elements, the concentrations obtained in the industrial zone was higher than the concentrations obtained in the Adalar region. In addition, as a result of metagenomic analysis, Aureobasidium (27.5%), Gibberella (20.7%), Cladosporium (14%), Articulospora (5.8%), Helicoma (3.1%), Alternaria (1.7%), Hazslinszkyomyces (1.6%) and Lasiodiplodia (1%) were determined in Samsun OIZ Pinus brutia needles, respectively. Phaeococcomyces (22.8%), Hormonema (19.1%), Aureobasidium (13.8%), Cladosporium (6.5%), Alternaria (4.6%), Neosetophoma (%3.1). Rachicladosporium (3%), Ophiosphaerella (2.1%), and Phaeosclera (1.8%) were determined in the Samsun Adalar mycobiome, respectively. The results show that taxa known to be resistant to excess element concentrations are dominant in the environment. In the future, this study may serve as a reference for the development of innovative strategies for remediation of heavy metal pollution using biological resources for a sustainable and clean environment.

References

Akpasi SO, Anekwe IMS, Tetteh EK, Amune UO, Shoyiga HO, Mahlangu TP, & Kiambi SL. (2023). Mycoremediation as a Potentially Promising Technology: Current Status and Prospects-A Review. Applied Sciences, 13(8):4978. DOI: 10.3390/app13084978

Anand R, Bharadvaja N. (2022). Fungi: The Assorted Bio-Remediators. ECS Transactions, 107(1), 13903. DOI 10.1149/10701.13903ecst

Bibbins-Martinez M, Juarez-Hernandez J, Lopez-Dominguez JY, Nava-Galicia SB, Martinez-Tozcano LJ, Juarez-Atona R, ... Diaz-Godinez G. (2023). Potential application of fungal biosorption and/or bioaccumulation for the bioremediation of wastewater contamination: A review. Journal of Environmental Biology, 44(2), 135-145. DOI:10.22438/jeb/44/2/MRN-5093.

Bolyen E, Rideout JR, Dillon MR, Bokulich NA, Abnet CC, Al-Ghalith GA, … & Caporaso JG. (2019). Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nature Biotechnology, 37(8):852-857. doi:10.1038/s41587-019-02099.

Bruins MR, Kapil S, Oehme FW. (2000). “Microbial resistance to metals in the environment,” Ecotoxicology and Environmental Safety 45(3), 198-207. DOI: 10.1006/eesa.1999.1860

Callahan BJ, McMurdie PJ, Rosen MJ, Han AW, Johnson AJA, & Holmes SP. (2016). DADA2: High-resolution sample inference from Illumina amplicon data. Nature Methods, 13(7):581-583. DOI: 10.1038/nmeth.3869

Cesur A, Zeren Cetin I, Abo Aisha AES, Alrabiti OBM, Aljama AMO, Jawed AA, Cetin M, Sevik H, Ozel HB (2021) The usability of Cupressus arizonica annual rings in monitoring the changes in heavy metal concentration in air. Environmental Science and Pollution Research (Environ Sci Pout Res) 2021. DOI: 10.1007/s11356-021-13166-4;

Cuadros-Orellana S, Leite LR, Smith A, Medeiros JD, Fern Badotti AA, Fonseca PL, Vaz AB, Oliveira G, Goes-Neto A. (2013). Assessment of Fungal Diversity in the Environment using Metagenomics: a Decade in Review. Fungal Genomics and Biology Vol.3 No.2 pp.1000110, 13 pp. DOI: 0.4172/2165-8056.1000110

Çebi Kılıçoğlu M. (2023). Ağır Metal ile Kontamine Toprakta Fungal Mikrobiyomun Metagenomik Analizi. Turkish Journal of Agriculture-Food Science and Technology, 11(9), 1671-1677. DOI: 0.24925/turjaf.v11i9.1671-1677.6261

Deng Z, Cao L. (2017). “Fungal endophytes and their interactions with plants in phytoremediation: a review,” Chemosphere 168, 1100-1106. DOI: 10.1016/j.chemosphere. 2016.10.097. DOI: 10.1016/j.chemosphere.2016.10.097

Domka AM, Rozpaądek P, Turnau K. (2019). “Are fungal endophytes merely mycorrhizal copycats? The role of fungal endophytes in the adaptation of plants to metal toxicity,” Frontiers in Microbiology, 10, 371. DOI: 10.3389/fmicb.2019.00371

Ghoma WEO, Şevik H, Işınkaralar K. (2023). Comparison of the rate of certain trace metals accumulation in indoor plants for smoking and non-smoking areas. Environmental Science and Pollution Research, 1-9. DOI: 10.1007/s11356-023-27790-9

Işınkaralar K, Koç I, Erdem R, Şevik H (2022) Atmospheric Cd, Cr, and Zn Deposition in Several Landscape Plants in Mersin, Türkiye, Water, Air, & Soil Pollution, DOI: 10.1007/s11270-022-05607-8

Işınkaralar K, Işınkaralar O, Koç İ, Özel HB, Şevik H. (2023). Assessing the possibility of airborne bismuth accumulation and spatial distribution in an urban area by tree bark: A case study in Düzce, Türkiye. Biomass Conversion and Biorefinery, 1-12.

İstanbullu SN, Şevik H, Işınkaralar K, Işınkaralar O. (2023). Spatial distribution of heavy metal contamination in road dust samples from an urban environment in Samsun, Türkiye. Bulletin of Environmental Contamination and Toxicology, 110(4):78. DOI: 10.1007/s00128-023-03720-w

Jha S, Kulkarni P, Sharma A. (2022). Heavy Metal Tolerance and Toxicity Studies on Indigenous Microflora and its Application for Bioremediation.Spectrum of Emerging Sciences,2(2), 10-16. DOI: 10.55878/SES2022-2-2-3

Karaçocuk T, Şevik H, Işınkaralar K, Türkyılmaz A, Çetin M. (2022). “The change of Cr and Mn concentrations in selected plants in Samsun city center depending on traffic density,” Landscape and Ecological Engineering, 1-9. DOI: 10.1007/s11355-021-00483-6

Kaul, S., Gupta, S., Ahmed, M., & Dhar, M. K. (2012). Endophytic fungi from medicinal plants: a treasure hunt for bioactive metabolites. Phytochemistry reviews, 11, 487-505. DOI 10.1007/s11101-012-9260-6

Key, K., Kulaç, Ş., Koç, İ. Sevik, H. (2023). Proof of concept to characterize historical heavy-metal concentrations in atmosphere in North Türkiye: determining the variations of Ni, Co, and Mn concentrations in 180-year-old Corylus colurna L. (Turkish hazelnut) annual rings. Acta Physiol Plant 45, 120 (2023). https://doi.org/10.1007/s11738-023-03608-6

Khan AR, Waqas M, Ullah I, Khan AL, Khan MA, Lee IJ, Shin JH. (2017). “Culturable endophytic fungal diversity in the cadmium hyperaccumulator Solanum nigrum L. and their role in enhancing phytoremediation,” Environmental and Experimental Botany 135, 126-135. DOI: 10.1016/j.envexpbot.2016.03.005

Koç I, Çobanoğlu H, Cantürk U, Key K, Kulaç S, Şevik H. (2023). Change of Cr concentration from past to present in areas with elevated air pollution. International Journal of Environmental Science and Technology, 1-12. DOI: 10.1007/s13762-023-05239-3

Kumar V, Dwivedi SK. (2021). Mycoremediation of heavy metals: processes, mechanisms, and affecting factors. Environmental Science and Pollution Research, 28(9):10375-10412. DOI: 10.1007/s11356-020-11491-8

Kuzmina N, Menshchikov S, Mohnachev P, Zavyalov K, Petrova I, Ozel HB, ... & Sevik H. (2023). Change of aluminum concentrations in specific plants by species, organ, washing, and traffic density. BioResources, 18(1):792. DOI: 10.15376/biores.18.1.792-803

Li HY, Li DW, He CM, Zhou ZP, Mei T, Xu HM. (2012). “Diversity and heavy metal tolerance of endophytic fungi from six dominant plant species in a Pb–Zn mine wasteland in China,” Fungal Ecology 5(3), 309-315. DOI: 10.1016/j.funeco.2011.06.002

Lindblom SD, Wangeline AL, Valdez Barillas JR, Devilbiss B, Fakra SC, Pilon-Smits EA. (2018). “Fungal endophyte Alternaria tenuissima can affect growth and selenium accumulation in its hyperaccumulator host Astragalus bisulcatus,” Frontiers in Plant Science, 9, 1213. DOI: 10.3389/fpls.2018.01213

Miersch J, Tschimedbalshir M, Barlocher F, Grams Y, Pierau B, Schierhorn A, Krauss GJ. (2001). Heavy metals and thiol compounds in Mucor racemosus and Articulospora tetracladia. Mycological Research, 105(7), 883-889. DOI: 10.1017/S095375620100404X

Mowll JL, Gadd GM. (1984). “Cadmium uptake by Aureobasidium pullulans,” Microbiology 130(2), 279-284. DOI: 10.1099/00221287-130-2-279

Refaey M, Abdel-Azeem AM, Abo Nahas HH, Abdel-Azeem MA, El-Saharty AA. (2021). Role of Fungi in Bioremediation of Soil Contaminated with Heavy Metals. In Industrially Important Fungi for Sustainable Development: Volume 1: Biodiversity and Ecological Perspectives (pp. 509-540). Cham: Springer International Publishing. DOI: 10.1007/978-3-030-67561-5-16

Rai, N., Kumari Keshri, P., Verma, A., Kamble, S. C., Mishra, P., Barik, S., …Gautam, V. (2021). Plant associated fungal endophytes as a source of natural bioactive compounds. Mycology, 12(3), 139-159. dOI:10.1080/2F21501203.2020.1870579

Sanusi AI. (2016). Heavy metal profile of Oreochromis niloticus harvested from e-waste polluted vials and associated Fungi. Advances in Microbiology, 6(8), 555-565. DOI: 10.4236/aim.2016.68056

Seshikala D, Charya MS. (2012). Effect of pH on chromium biosorption. Int J Pharma Bio Sci,2, 298-302.

Singh V, Singh MP, Mishra V. (2020). Bioremediation of toxic metal ions from coal washery effluent Desalin. Water Treat, 197: 300-318. DOI: 10.5004/dwt.2020.25996

Singh V, Singh J, & Mishra V. (2021). Development of a cost-effective, recyclable and viable metal ion doped adsorbent for simultaneous adsorption and reduction of toxic Cr (VI) ions. Journal of Environmental Chemical Engineering, 9(2): 105124. DOI: 10.1016/j.jece.2021.105124

Sulhan OF, Sevik H, Isinkaralar K. (2023). “Assessment of Cr and Zn deposition on Picea pungens Engelm. in urban air of Ankara, Turkiye,” Environment, Development and Sustainability 25(5), 4365-4384. DOI: 10.1007/s10668-022-02647-2

Tu C, Liu Y, Wei J, Li L, Scheckel KG, & Luo Y. (2018). Characterization and mechanism of copper biosorption by a highly copper-resistant fungal strain isolated from copper-polluted acidic orchard soil. Environmental Science and Pollution Research, 25: 24965-24974.

Türkkan M, Çebi Kılıcoglu M, Erper I. (2020). “Characterization and pathogenicity of Rhizoctonia isolates collected from Brassica oleracea var. acephala in Ordu, Türkiye,” Phytoparasitica, 48(2), 273-286. DOI: 10.1007/s12600-020-00793-9

Türkyılmaz A, Sevik H, Cetin M. (2018). The use of perennial needles as bio-monitors for recently accumulated heavy metals. Landsc Ecol Eng 14 (1):115–120. DOI: 10.1007/s11355-017-0335-9

Vaid N, Sudan J, Dave S, Mangla H, Pathak H. (2022). “Insight into microbes and plants ability for bioremediation of heavy metals,” Current Microbiology 79(5), 141. DOI: 10.1007/s00284-022-02829-1

Wang M, Xu Z, Dong B, Zeng Y, Chen S, Zhang Y, ... & Pei X. (2022). An efficient manganese-oxidizing fungus Cladosporium halotolerans strain XM01: Mn (II) oxidization and Cd adsorption behavior. Chemosphere, 287:132026.

White TJ, Bruns T, Lee SJWT, & Taylor J. (1990). Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. PCR Protocols: A Guide to Methods and Applications, 18(1):315-322.

Yayla EE, Şevik H, Işınkaralar K. (2022). Detection of landscape species as a low-cost biomonitoring study: Cr, Mn, and Zn pollution in an urban air quality. Environmental Monitoring and Assessment, 194(10), 1-10. DOI: 10.1007/s10661-022-10356-6

Zhang J, Fan X, Wang X, Tang Y, Zhang H, Yuan Z, ... & Li T. (2022). Bioremediation of a saline-alkali soil polluted with Zn using ryegrass associated with Fusarium incarnatum. Environmental Pollution, 312:119929. DOI: 10.1016/j.envpol.2022.119929

Zheng J, Xie X, Li C, Wang H, Yu Y, Huang B. (2023). Regulation mechanism of plant response to heavy metal stress mediated by endophytic fungi,” International Journal of Phytoremediation 1-18. DOI: 10.1080/15226514.2023.2176466

Published

16.09.2024

How to Cite

Çebi Kılıçoğlu, M. (2024). Metagenomic Characterization of Heavy Metal-Fungal Microbiota Interaction in Pinus brutia Needles. Turkish Journal of Agriculture - Food Science and Technology, 12(9), 1523–1529. https://doi.org/10.24925/turjaf.v12i9.1523-1529.6590

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Research Paper