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Environmental Advances Toxicity of Metal Cations and Phenolic Environmental Advances 4 (2021) 100044 Contents lists available at ScienceDirect Environmental Advances journal homepage: www.elsevier.com/locate/envadv Toxicity of metal cations and phenolic compounds to the bioluminescent fungus Neonothopanus gardneri Fernanda F. Ventura a,b, Douglas M.M. Soares a, Kevin Bayle a, Anderson G. Oliveira c, Etelvino J.H. Bechara a, Renato S. Freire a, Cassius V. Stevani a,∗ a Departamento de Química Fundamental, Instituto de Química, Universidade de São Paulo, São Paulo, SP, Brazil b Fundação Jorge Duprat Figueiredo de Segurança e Medicina do Trabalho, São Paulo, SP, Brazil c Departamento de Oceanografia Física, Química e Geológica, Instituto Oceanográfico, Universidade de São Paulo, São Paulo, SP, Brazil a r t i c l e i n f o a b s t r a c t Keywords: Fungi play a key role in the soil ecosystem, where they occupy the first level of the food chain. Hence, they are Bioassay considered suitable model organisms to conduct ecotoxicological assays for the evaluation of soil condition after Basidiomycete proper soil extraction. Fungi bioluminescence-based bioassays are useful considering that their luminescence is Fungicide development an early toxicity endpoint and light emission a promptly detectable signal. In this paper, we describe a toxicolog- Soil ecotoxicology ical bioassay that relies on a 24-h variation of total light emitted by the mycelium of the bioluminescent fungus Tropical ecotoxicity Neonothopanus gardneri when exposed to a toxicant. The current bioluminescent assay, which uses a fungus of the Omphalotus lineage, fills a gap covering all the representative species of bioluminescent fungi. Among the compounds tested here, Cd(II) showed the highest toxicity, followed by 4-nitrophenol, phenol and Cu(II), respec- tively. We also found that N. gardneri presents a predictable bioluminescence and growth pattern, and is highly sensitive to these compounds. The aforementioned characteristics offer valuable advantages and make N. gardneri the ideal candidate for toxicological studies with basidiomycetes. 1. Introduction compounds are defined as priority pollutants ( Vera-Avila et al., 1996 , Igbinosa et al., 2013 ). These compounds can be decomposed by bacte- Among environmental pollutants, phenolic compounds and metal ria and fungi, although many are persistent and harmful to the environ- cations require special attention, since they occur in many different ment. products/processes and are released on a massive scale in into the The toxic effects of metals and phenolic compounds to eukary- environment, causing highly negative impacts, especially to the bio- otic organisms include their direct interaction with biomolecules and sphere ( Arjoon et al. , 2013 ; Igbinosa et al., 2013 ; Pradeep et al., 2015 ; subsequent modification, denaturation or inactivation of key enzymes Azimi et al., 2017 ; Duan et al., 2018 ; Li and Achal 2020 ; Rahman 2020 ; ( Appel 1993 ; Gadd 1993 ; Xu 1996 ; Baldrian 2003 ; Michalowicz and Roccuzzo et al., 2020 ). Several non-essential metals such as cadmium, Duda 2007 ). Moreover, these effects can trigger the uncoupling of mi- lead and mercury are highly toxic even at very low concentrations. Metal tochondrial oxidative phosphorylation, leading to the impairment of cations are present in pigments, batteries, electronic devices, amalgams, ATP biosynthesis ( Gadd 1993 ; Belgers et al., 2009 ; Stevani et al., 2013 ; fertilizers, pesticides, among many other industrialized products. They Ventura et al., 2020 ). are also released from burning fossil fuels, mining, metallurgy and other A plethora of analytical techniques is available to identify and quan- industrial activities ( Leyval et al., 1997 ; Gadd 2010 ). Metals do not tify specific pollutants, but unfortunately, these techniques do not serve degrade and can only speciate under biological or geochemical condi- to evaluate the bioavailability and/or toxicological effects of pollu- tions. Hence, they can bioaccumulate in organisms of the soil food web tants. Decomposer microorganisms such as fungi are on the first level and eventually give rise to serious ecological and possible health issues of the food chains, cycling nutrients to species at higher trophic levels ( Luoma and Rainbow 2005 , Chojnacka 2010 , Rahman 2020 ). Phenolic ( Weitz et al., 2002 ; Mendes and Stevani 2010 ; Ventura et al., 2020 ). compounds can be found in the transformation pipeline of many in- Therefore, deadly damage to fungi can affect the entire ecosystem, and dustrial products ( Santos and Linardi 2001 ; Lee et al., 2006 ). Due to hence, their potential bioanalytical role in ecotoxicology after proper their potential toxicity to microorganisms, plants and animals, phenolic extraction from soil. ∗ Corresponding author. E-mail address: [email protected] (C.V. Stevani). https://doi.org/10.1016/j.envadv.2021.100044 Received 17 November 2020; Received in revised form 5 February 2021; Accepted 9 March 2021 2666-7657/© 2021 The Author(s). Published by Elsevier Ltd. This is an open access article under the CC BY-NC-ND license ( http://creativecommons.org/licenses/by-nc-nd/4.0/ ) F.F. Ventura, D.M.M. Soares, K. Bayle et al. Environmental Advances 4 (2021) 100044 Fig. 1. Fourteen-day old mycelium of Neonothopanus gardneri (a), Gerronema viridilucens (b) and Mycena lucentipes (c) cultivated in the same conditions (A); the same Petri dishes in the dark (B). In conventional bioassays using basidiomycete fungi, the toxicity of changes to adapt it to N. gardneri . This is promising: other biolumines- pollutants is usually assessed based on their inhibition of mycelium cent fungi may also be used in such bioassays, following a similar proto- growth, which is determined by measuring the radial diameter or col. The toxicological bioassay with N. gardneri was performed using the mycelial biomass ( Weitz et al., 2002 ). On the other hand, biolumi- most toxic metal cations and phenolic compounds reported in the liter- nescent bioassays are based on the decrease of light emission after ature, namely cadmium, copper, phenol and 4-nitrophenol ( Weitz et al., mycelium exposure to the toxicant ( Weitz et al., 2002 ; Mendes and 2002 ; Mendes and Stevani 2010 ; Ventura et al., 2020 ). Our findings al- Stevani 2010 ; Ventura et al., 2020 ). Luminescent methodologies are low us not only to evaluate the simplicity of the bioassay methodology advantageous because the signal can be readily recorded; they are (i.e., exposure time and toxicant diluent), but also its fungus-dependent also sensitive, reproducible, less time-consuming and cost effective analytical sensitivity. ( Steinberg et al., 1995 ; Weitz et al., 2002 ; Mendes and Stevani 2010 ; Ventura et al., 2020 ). Moreover, as bioluminescence depends on molecu- 2. Material and methods lar oxygen to occur and is therefore closely linked to respiratory activity, the decrease in bioluminescence emission is a prompt and early endpoint 2.1. Chemicals and solutions that signals injuries caused by toxicants to the fungus ( Ventura et al., 2020 ). Directly or indirectly, the toxicant may act specifically or gen- Fungal culture media were prepared using food-grade agar, yeast erally upon biological membrane, receptors and enzymes, finally caus- extract (both from Sigma-Aldrich, USA) and food-grade sugarcane mo- ing light emission to decline. Potential biological targets of toxicants to lasses (55.94% sucrose, from Usina São José da Estiva, Novo Hori- fungi have been addressed by other authors ( Mendes and Stevani 2010 ; zonte, SP, Brazil). All the reagents were of ≥ 99% ACS purity grade Mendes et al., 2010 ; Ventura et al., 2020 ). The mechanism underlying and used as received. Stock solutions of phenol, 4-nitrophenol, 2- fungal bioluminescence was recently described ( Kaskova et al., 2017 ; ( N -morpholino)ethanesulfonic acid (MES) buffer, Triton X-100 (from Kotlobay et al., 2018). Sigma-Aldrich, USA), CdSO4 .8H2 O, CuSO4 .5H2 O, H2 SO4 (from Merck, All bioluminescent fungi are basidiomycetes ( Desjardin et al., 2008 ; USA), NaOH (from Synth, Brazil) and dimethyl sulfoxide (DMSO; from Stevani et al., 2013 ). Furthermore, as some bioluminescent basid- Synth, Brazil) were prepared in ultrapure deionized Milli-Q water. iomycetes are phytopathogens (e.g., Armillaria mellea and Mycena cit- ricolor ) ( Desjardin et al., 2008 ; Ventura et al., 2015 ), tailored bioas- 2.2. Equipment says within this group of fungi could be advantageous for the develop- ment of new agricultural fungicides ( Gadd 1993 ; Stevani et al., 2013 ; The materials, solutions and culture media were sterilized in an au- Ventura et al., 2020 ). It is interesting to note that toxicological data on toclave (Phoenix, model AB42) at 120 °C for 30 min and handled in white-rot basidiomycetes are still scanty, and only a few reports have a laminar flow hood (Pachane, model PCR T2.5). N. gardneri culture appeared in the literature in recent decades (Leontievsky et al., 2000; were kept in a climate chamber (Binder, model KBWF 240) at 30 °C Mendes et al., 2010 ; Mendes and Stevani 2010 ; Ventura et al., 2020 ). and 80% humidity. Distilled and ultrapure water was obtained using a In an attempt to expand the range of available bioluminescent-based Milli-Q Direct 16 water purification system (Merck-Millipore). Biolumi- fungal assays, covering different taxa in all four lineages of biolumines- nescence (BL) measurements were taken in a microplate luminometer cent fungi ( Desjardin et al., 2008 ), further experiments initiated with (Tecan, model Infinite M200) with the integration time set to
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