Native Endomycorrhiza With Tolerance to Heavy Metal Contamination in Organic Culture Media


Endomycorrhizal fungi are spora-carrying organisms that can survive in heavy metalcontaminated environments. The goal of this study was to investigate endomycorrhizal fungi from heavy metal-affected areas and determine an effective mix of organic culture media to increase the number and diameter of endomycorrhizal spores. In Sorowako, Indonesia, endomycorrhizal fungi were isolated from the rhizosphere of: rice husk charcoal, sand, zeolite (KM1); rice husk charcoal, sand, sawdust (KM2); rice husk charcoal, sand, cocopeat (KM3); rice husk charcoal, sand, rice soil (KM4); rice husk charcoal, sand, cold magma (KM5); rice husk charcoal, sand, cold magma (KM6); and rice husk charcoal, sand (KM7). The results of the first phase of research revealed that three endomycorrhizal genera (44.44%–75.86% Acaulospora sp, 9.52%–44.44% Gigaspora sp, and 3.38%–19.05 % Glomus sp) can adapt to and resist conditions contaminated with Hg, Cd, Ni, Pb, As, Cr, Mn, Fe, Cu, Co, and Sn, namely as a carrier medium. It was concluded that a combination of organic media was recommended, but that this must decompose first.

Keywords: Fungi, mycorrhizal, organic waste, rhizosfer

[1] Ferrol N, Tamayo E, Vargas P. The heavy metal paradox in arbuscular mycorrhizas: From mechanisms to biotechnological applications. Journal of Experimental Botany. 2016;67(22):6253–6565.

[2] Bano SA, Ashfaq D. Role of mycorrhiza to reduce heavy metal stress. Natural Science. 2013;5(12):16–20.

[3] Abu-Elsaoud AM, Nafady NA, Abdel-Azeem AM. Arbuscular mycorrhizal strategy for zinc mycoremediation and diminished translocation to shoots and grains in wheat. PLoS One. 2017;12(11):1–21.

[4] Gong X, Tian DQ. Study on the effect mechanism of arbuscular mycorrhiza on the absorption of heavy metal elements in soil by plants. IOP Conference Series: Earth And Environmental Science. 2019;267(5). 1315/267/5/052064

[5] Cely MVT, de Oliveira AG, de Freitas VF, de Luca MB, Barazetti AR, dos Santos IMO, Gionco B, Garcia GV, Prete CEC, Andrade G. Inoculant of arbuscular mycorrhizal fungi (Rhizophagus clarus) increase yield of soybean and cotton under field conditions. Frontiers. In Microbiology. 2016;7(MAY):1–9.

[6] Coelho IR, Pedone-Bonfim MVL, Silva FSB, Maia LC. Optimization of the production of mycorrhizal inoculum on substrate with organic fertilizer. Brazilian Journal of Microbiology. 2014;45(4):1173–1178.

[7] Mukhongo RW, Tumuhairwe JB, Ebanyat P, AbdelGadir AH, Thuita M, Masso C. Production and use of arbuscular mycorrhizal fungi inoculum in sub-Saharan Africa: Challenges and ways of improving. Intnational Jornal of Soil Science. 2016;11(3):108– 122.

[8] Kokkoris V, Hamel C, Hart MM. Mycorrhizal response in crop versus wild plants. PLoS One. 2019;14(8):1–16.

[9] Malusá E, Sas-Paszt L, Ciesielska J. Technologies for beneficial microorganisms inocula used as biofertilizers. Scientific World Journal. 2012.

[10] Asmelash F, Bekele T, Birhane E. The potential role of arbuscular mycorrhizal fungi in the restoration of degraded lands. Frontiers in Microbiology. 2016;7( JUL):1–15.

[11] Begum N, Qin C, Ahanger MA, Raza S, Khan MI, Ashraf M, Ahmed N, Zhang L. Role of arbuscular mycorrhizal fungi in plant growth regulation: Implications in abiotic stress tolerance. Frontiers in Plant Science. 2019;10(Sep):1–15.

[12] Medina A, Azcón R. Effectiveness of the application of arbuscular mycorrhiza fungi and organic amendments to improve soil quality and plant performance under stress conditions. Journal of Soil Science and Plant Nutrition. 2010;10(3):354–372.

[13] Krishnamoorthy R, Kim CG, Subramanian P, Kim KY, Selvakumar G, Sa TM. Arbuscular mycorrhizal fungi community structure, abundance and species richness changes in soil by different levels of heavy metal and metalloid concentration. PLoS One. 2015;10(6):1–15.

[14] Brundrett MC, Piché Y, Peterson RL. A new method for observing the morphology of vesicular–arbuscular mycorrhizae. Canadian Journal of Botany. 1984;62(10):2128– 2134.

[15] Walker C, Mize CW, McNabb HS. Populations of endogonaceous fungi at two locations in central Iowa. Canadian Journal of Botany. 1982;60(12):2518–2529.

[16] Akib MA. Prosedur rancangan percobaan: Aplication of the model in different environmental conditions. 2nd ed. . Parepare: Lampena Intimedia; 2019.

[17] Hossain MA, Piyatida P, da Silva JAT, Fujita M. Molecular mechanism of heavy metal
toxicity and tolerance in plants: Central role of glutathione in detoxification of reactive
oxygen species and methylglyoxal and in heavy metal chelation. Journal of Botany.

[18] Jaishankar M, Tseten T, Anbalagan N, Mathew BB, Beeregowda KN. Toxicity,
mechanism and health effects of some heavy metals. Interdisciplinary Toxicology.

[19] Briffa J, Sinagra E, Blundell R. Heavy metal pollution in the environment
and their toxicological effects on humans. Heliyon. 2020;6(9):e04691-e04717.

[20] Bellini E, Betti C, di Toppi LS. Responses to cadmium in early-diverging streptophytes
(charophytes and bryophytes): Current views and potential applications. Plants.

[21] Yan A, Wang Y, Tan SN, Yusof ML, Ghosh S, Chen Z. Phytoremediation: A promising
approach for revegetation of heavy metal-polluted land. Frontiers in Plant Science.

[22] Hadianur H, Syafruddin S, Kesumawati E. Pengaruh jenis fungi mikoriza arbuscular
terhadap pertumbuhan dan hasil tanaman tomat (Lycopersicum esculentum Mill).
Jurnal Agrista, Universitas Syiah Kuala. 2016;20(3):126–134.

[23] Vieira LC, da Silva DKA, Escobar IEC, da Silva JM, de Moura IA, Oehl F, da Silva
GA. Changes in an arbuscular mycorrhizal fungi community along an environmental
gradient. Plants. 2020;9(1):1–16.

[24] Ismael HR, Honore IK, Abaka AS, Philippe K, Clautilde M. Diversity of arbuscular
mycorrhizal fungi (AMF) associated with cotton (Gossypium hirsutum L.) growing
in the far-north region of Cameroon. African Journal of Microbiology Research.

[25] Berruti A, Lumini E, Balestrini R, Bianciotto V. Arbuscular mycorrhizal fungi as
natural biofertilizers: Let’s benefit from past successes. Frontiers in Microbiology.
2016;6( Jan):1–13.

[26] Songachan LS, Kayang H. Diversity of arbuscular mycorrhizal fungi associated with Flemingia vestita Benth. ex Baker. Mycology. 2013;4(2):85–95.

[27] Wang M, Jiang P. Colonization and diversity of AM fungi by morphological analysis
on medicinal plants in Southeast China. The Scientific World Journal. 2015:2015,ID
753842, 1-7.

[28] Dodd JC, Boddington CL, Rodriguez A, Carmen G-C, Mansur I. Mycelium of
arbuscular mycorrhizal fungi (AMF) from different genera: Form, function and
detection. Plant Soil. 2000;226:131–151.

[29] Costa FA, Haddad LSA, Kasuya MC, Oton WC, Costa MD, Borges AC. Cultura in vitro
de Gigaspora decipiens e Glomus clarum em raízes transformadas de cenoura:Influência da temperatura e pH. Acta Scientiarm. Agronomy. 2013;35(3):315–323.

[30] Castillo CG, Borie F, Oehl F, Sieverding E. Arbuscular mycorrhizal fungi
biodiversity: Prospecting in southern-central zone of Chile. A review. Journal of
Soil Science and Plant Nutrition. 2016;16(2):400–422.

[31] do Carmo DL, de Lima LB, Silva CA. Soil fertility and electrical conductivity affected
by organic waste rates and nutrient inputs davi lopes. Revista Brasileira de Ciencia
do Solo. 2016;40(1–17).

[32] Saidi D. Importance and role of cation exchange capacity on the physicals properties
of the cheliff saline soils (Algeria). Procedia Engineering. 2012;33(2011):435–449.

[33] Yunan D, Xianliang Q, Xiaochen W. Study on cation exchange capacity of agricultural
soils. IOP Conference Series: Materials Science and Engineering. 2018;392(4):1-5

[34] Febriani W, Riniarti M, Surnayanti. The aplication of various planting media and spore
inoculums to improve ectomycorrhizal colonization and growth of Shorea javanica.
Jurnal Sylva Lestari. 2017;5(3):87–94.

[35] Mujica MI, Saez N, Cisternas M, Manzano M, Armesto JJ, Pérez F. Relationship between soil nutrients and mycorrhizal associations of two bipinnula
species (Orchidaceae) from central Chile. Annals of Botany. 2016;118(1):149–158.

[36] Nouri E, Breuillin-Sessoms F, Feller U, Reinhardt D. Phosphorus and nitrogen
regulate arbuscular mycorrhizal symbiosis in Petunia hybrida. PLoS One. 2014;9(3):

[37] Prasad K, Aggarwal A, Yadav K, Tanwar A. Impact of different levels of
superphosphate using arbuscular mycorrhizal fungi and Pseudomonas fluorescens
on Chrysanthemum indicum L. Journal of Soil Science and Plant Nutrition.

[38] Beltrano J, Ruscitti M, Arango MC, Ronco M. Effects of arbuscular mycorrhiza
inoculation on plant growth, biological and physiological parameters and mineral
nutrition in pepper grown under different salinity and p levels. Journal of
Soil Science and Plant Nutrition. 2013;13(1):123–141.

[39] Balzergue C, Chabaud M, Barker DG, Bécard G, Rochange SF. High phosphate
reduces host ability to develop arbuscular mycorrhizal symbiosis without affecting
root calcium spiking responses to the fungus. Frontiers Plant Science. 2013;4(Oct):1–

[40] Yulius F, Towaha J, Sasmita RRKD. Plant water compost usage as a carrier of
mycorrhizal inoculant from bushy pepper cultivation in the post-tin mining soil.
Industrial Crops Research Journal. 2013;19(1):15–22.

[41] Setiadi AA, Purwantisari S. Viability and number of mycorrhizae product of Ngudi
makmur farmer group in Kataan Village Ngadirejo Temanggung. Jurnal Biologi
Tropika. 2019;2(2):80–84.

[42] Gleixner G. Soil organic matter dynamics: A biological perspective derived from the
use of compound-specific isotopes studies. Ecological Research. 2013;28(5):683–

[43] Jacoby R, Peukert M, Succurro A, Koprivova A, Kopriva S. The role of soil
microorganisms in plant mineral nutrition - Current knowledge and future directions.
Frontiers in Plant Science. 2017;8(Sep):1–19.

[44] Novak E, de Carvalho LA, Santiago EF, Tomazi M. Changes in the soil structure and
organic matter dynamics under different plant covers. Cerne. 2019;25(2):230–239.

[45] Nunes JR, Miras JR, Piñeiro AL, Loures L, Gil C, Coelho J, Loures A. Concentrations
of available heavy metals in Mediterranean agricultural soils and their relation
with some soil selected properties: A case study in typical Mediterranean soils.
Sustainability. 2014;6(12):9124–9138.

[46] Kim SJ, Eo JK, Lee EH, Park H, Eom AH. Effects of arbuscular mycorrhizal
fungi and soil conditions on crop plant growth. Mycobiology. 2017;45(1):20–24.

[47] Goetten LC, Moretto G, Stürmer SL. Influence of arbuscular mycorrhizal fungi
inoculum produced on-farm and phosphorus on growth and nutrition of native
woody plant species from Brazil. Acta Botanica Brasilica. 2016;30(1):9–16.

[48] IJdo M, Cranenbrouck S, Declerck S. Methods for large-scale production of AM fungi:
Past, present, and future. Mycorrhiza. 2011;21(1):1–16.

[49] Chen M, Arato M, Borghi L, Nouri E, Reinhardt D. Beneficial services of arbuscular
mycorrhizal fungi – From ecology to application. Frontiers in Plant Science.

[50] Hao Z, Xie W, Chen B. Arbuscular mycorrhizal symbiosis affects plant
immunity to viral infection and accumulation. Viruses. 2019;11(6):1–12.

[51] Ohtomo R, Kobae Y, Morimoto S, Oka N. Infection unit density as an index of infection
potential of arbuscular mycorrhizal fungi. Microbes and Environmets. 2018;33(1):34–

[52] Garg N, Aggarwal N. Effect of mycorrhizal inoculations on heavy metal uptake
and stress alleviation of Cajanus cajan (L.) Millsp. genotypes grown in cadmium and lead contaminated soils. Plant Growth Regulation. 2012;66(1):9–26.

[53] Johri AK, Oelmüller R, Dua M , Yadav V, Kumar M, Tuteja N, Varma A, Bonfante P,
Persson BL, Stroud RM. Fungal association and utilization of phosphate by plants:
Success, limitations, and future prospects. Frontiers in. Microbiology. 2015;6(Oct):1–

[54] Wipf D, Krajinski F, van Tuinen D, Recorbet G, Courty PE. Trading on the
arbuscular mycorrhiza market: From arbuscules to common mycorrhizal networks.
New Phytologist. 2019;223(3):1127–1142.