Scleroderma citrinum

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1. Classification

Higher order taxa

Eukaryota (Domain); Basidiomycota (Phylum); Agaricomycetes (Class); Boletales (Order); Sclerodermataceae (Family) [1]

NCBI: [1]

Scleroderma citrinum

2. Description and significance

Scleroderma citrinum, often referred to as “common earthball” or “pigskin poison earthball”, is a common fungal species found in the soil of temperate forests during autumn and winter [2]. The genus name Scleroderma means “hard-skin,” while the specific epithet name citrinum refers to the organism’s lemon-like yellow coloration. The exterior of the fruit body is thick with many irregular warts, and it is usually around 2-10 centimeters wide and 2-4 cm tall [2]. Although it bears a resemblance to edible earth balls, S. citrinum is considered inedible [3]. The mechanism by which symptoms, including gastrointestinal distress and irritation of the nasal cavity, arise due to spore inhalation are understudied [4].

S. citrinum is an ectomycorrhizal fungus and can alter the diversity of soil bacterial communities under some tree species, such as oak and beech, including selecting for mineral-weathering bacteria [2] [5]. S. citrinum has also been found to facilitate mycorrhization of Parapiptadenia rigida seedlings in forest nurseries [6]. Genome analysis has revealed that S. citrinum may possess alternative pathways for degrading non-plant polysaccharides as its carbon source [7]. In addition to an important ecological role, there is ongoing research to explore S. citrinum’s potential as a therapeutic agent for treating a variety of illnesses and ailments such as the Herpes simplex type I and tuberculosis [8].

3. Genome structure

The complete genome of S. citrinum has a total sequence length of 56,144,862 base pairs [9]. The fungus has 20,993 genes with a 48.6% GC content, encoding 20,995 different proteins [1]. It has been discovered that S. citrinum encodes fewer carbohydrate-active enzymes (CAZymes) for degrading plant polysaccharides and more CAZymes for synthesizing fungal cell walls than Russula griseocarbosa, another ectomycorrhizal fungus,indicating that its symbiotic lifestyle plays a role in this genomic adaptation [7] S. citrinum can encode a total of 24 lignocellulose-degrading oxidoreductases and 25 CAZymes [10]. Similarly to other ectomycorrhizal fungi, including Paxillus involutus, Paxillus rubicundulus, and many more, S. citrinum contains zero cellulose-binding molecules [10].

4. Cell structure

S. citrinum creates a mantle around colonized plant root tips, which is something commonly seen in ectomycorrhizal fungi belonging to the Scleroderma genus [11]. Both the outer layer of the mantle and the emanating hyphae have been reported to be finely rough, while the middle and inner layers contain a gelatinous matrix in which the hyphae are embedded [12]. The surface of mature rhizomorphs of ‘S. citrinum’ has also been described as inflated or swollen [13].

5. Metabolic processes

A comparison of genome sequences of S. citrinum to R. griseocarbosa revealed fewer genes coding for carbohydrate-active enzymes (CAZymes) in S. citrinum. The genome of S. citrinum consists of 253 CAZymes, including lower copy numbers of glycoside hydrolases (GH), carbohydrate esterases (CE), and polysaccharide lyases (PL) than R. griseocarbosa [7]. Lower numbers of CAZymes in S. citrinum relative to other soil-dwelling fungi indicates restricted utilization of plant cell wall polysaccharides as carbon sources, suggesting that S. citrinum has other means of degrading non-plant polysaccharides or uses other carbon sources that are not yet well understood. S. citrinum and R. griseocarbosa share a similar number of chitin synthases and β-glucanases for synthesizing fungal cell walls relative to other ectomycorrhizal fungi [7]. S. citrinum also has a greater number of CAZymes capable of degrading bacterial or animal polysaccharides than R. griseocarbosa [7].

The elemental composition of S. citrinum has been determined as: K >> Na > Ca > Mg > Fe > Mn > Zn > Cu > Se > Co > Ni > Be > Pb > Cd > As [3]. The accumulation of such metals from soil depends upon soil quality and other environmental factors, rather than the edibility of the mushroom species [3]. S. citrinum has the highest concentration of the trace metal zinc (215 mg/kg) among edible and inedible mushrooms found in South Africa [3].

S. citrinum contains three pigments: norbadione A, sclerocitrin and melanin [14] [15]. 13C spectroscopy revealed two sets of twelve signals indicating two 4-hydroxypulvinic acid residues from norbadione A, which is an unusual pulvinic acid dimer (14). Sclerocitrin was found to give S. citrinum its yellow color [14]. Melanin was found to exhibit its usual light barrier, antioxidant, and antibacterial properties, which means that S. citrinum may be a new source of natural melanin [15].

Several bioactive compounds have been identified in the S. citrinum, some of which could potentially provide therapeutic benefits for diseases [8]. The triterpenoid, (20S,22S,23E)-22-O-acetyl-25-hydroxlanosta-8,23(E)-dien-3-one, has anti-HSV-1 (Herpes simplex type 1) activity [8]. The vulpinic acid, 4,4’-dimethoxyvulpinic acid (DMVA), has antitubercular (Mycobacterium tuberculosis H34Ra) activity [8]. The dibromo derivative and acetate derivative of DMVA has anti-NCI (human lung cancer cells NCI-H187) activity, in addition to antimycobacterial activity [8]. These biological constituents hold potential for pharmaceutical manufacturing of drugs to treat HSV-1, tuberculosis, and lung cancer.

Another natural product, 4,4’-dimethoxymethyl vulpinate (DMV), along with DMVA, was isolated and tested for biological activity against two plant pathogens in vitro: Phytophthora palmivora, and Colletotrichum gloeosporioides, which cause bud-rot and Anthracnose, respectively. Both DMV and DMVA exhibit a significant amount of inhibition on mycelium and conidia (spore produced asexually) production of P. palmivora and C. gloeosporioides, preventing their growth. As such, these two components of S. citrinum could play a role in treatments for plant disease [16].

6. Ecology

As an ectomycorrhizal fungus, Scleroderma citrinum is able to increase its host plant’s ability to uptake nutrients and resist abiotic stresses [17]. For example, S. citrinum is able to colonize Parapiptadenia rigida seedlings, such that the inoculation of S. citrinum spores in P. rigida seedlings at a plant nursery increases the stem diameter, fresh mass, and dry mass of P. rigida roots, which may confer a greater chance of survival after transplantation [6]. Mycorrhization by S. citrinum can also enhance the secondary metabolism of pine and eucalyptus [6]. Other plant hosts of S. citrinum include Pinus patula, Pinus sylvestris, Betula pendula, Pinus resinosa, Larix decidua, and Picea abies [12].

Oak and beech tree species also have been found to indirectly depend on S. citrinum. These tree species selected for soil bacterial communities with high mineral weathering potential. They prefer these bacteria because they contribute to nutrient mobilization and improved mineral availability enabling tree growth [5]. S. citrinum itself is not efficient in mineral weathering but is symbiotic to bacteria that are efficient in iron availability potential. The bacterial strains isolated from S. citrinum around oak and beech strands release higher proportions of iron from biotite [5]. Higher iron benefits the tree species around S. citrinum as it is an important micronutrient for metabolic processes including photosynthesis [18]. Additionally, the bacteria symbiotic to S. citrinum affect the production of protons, a mechanism responsible for mineral weathering. The acidification influences mineral stability, which benefits oak and beech species [5].

7. Toxicity & Pathology

Scleroderma citrinum has been identified as poisonous, but the details surrounding this are still unclear [3]. Spore inhalation by humans has been reported to cause various symptoms including gastrointestinal distress, rhinitis, tachycardia, unconsciousness, dyspnea, and lacrimation [4]. However, the toxic compound(s) within S. citrinum has not been isolated and identified.

8. Current Research

Recent studies conducted on S. citrinum have investigated its potential as a therapeutic agent. For example, one study found that its melanin extracts were capable of inhibiting both Enterococcus faecalis and Pseudomonas aeruginosa, two species of pathogenic bacteria [15]. An earlier study identified a few of S. citrinum’s bioactive components and determined that they could help combat Herpes simplex virus type 1, Mycobacterium tuberculosis, and lung cancer [8].

Ectomycorrhizal fungi like S. citrinum have been investigated for their resistance to heat, toxic metals, and soil pathogens [19]. It was found that S. citrinum experienced maximum growth when exposed to sucrose, while also showing signs of a decrease in pH within the span of 30-45 days [19]. As a result, this contributes to healthier soil. Plants usually thrive in soil that is slightly acidic. The results of this research helps to encourage the usage of S. citrinum in biofertilizers to stimulate plant growth [19].

9. References

[1] Scleroderma citrinum (ID 18213). National Library of Medicine (US), National Center for Biotechnology Information; 2004 - [cited 2020 Oct 12.]

[2] Uroz, S., & Oger, P. (2017). Caballeronia Mineralivorans Sp. Nov., Isolated from Oak-Scleroderma Citrinum Mycorrhizosphere. Systematic and Applied Microbiology, 40(6): 345-51.

[3] Uroz, S., & Oger, P. (2017). Rasalanavho, M., Moodley, R., & Jonnalagadda, S. B. (2019). Elemental distribution including toxic elements in edible and inedible wild growing mushrooms from south Africa. Environmental Science and Pollution Research International, 26(8): 7913-7925.

[4] Uroz, S., & Oger, P. (2017). Berg, M.W., Shaw, M., & Cochran, K. W. (2006). Theory-plus years of mushroom poisoning: summary of the approximately 2,000 reports in the NAMA case registry. McIlvainea, 16(2): 47-68.

[5] Calvaruso, C., Turpault, M. P., Leclerc, E., Ranger, J., Garbaye, J., Uroz, S., & Frey-Klett, P. (2010). Influence on forest trees on the distribution of mineral weathering-associated bacterial communities of the Scleroderma citrinum mycorrhizosphere. Applied and Environmental Microbiology, 76(14): 4780-4787.

[6] Steffen G.P..K., R.B. Steffen, R.M. de Morais, C.W. Saldanha, J. Maldaner, T.M. Loiola. (2017). Parapiptadenia rigida mycorrhization with spores of Scleroderma citrinum. CERNE, 23(2): 241-248.

[7] Yu, F., Song, J., Liang, J., Wang, S., & Lu, J. (2020). Whole genome sequencing and genome annotation of the wild edible mushroom, Russula griseocarnosa. Genomics, 112(1): 603-614.

[8] Kanokmedhakul S., K. Kanokmedhakul, T. Prajuabsuk, K. Soytong, P. Kongsaeree, A. Suksamrarn. (2003). A bioactive triterpenoid and vulpinic acid derivatives from the mushroom Scleroderma citrinum. Planta Medica, 69(6): 568-571.

[9] Scleroderma citrinum Foug A v1.0. Bethesda (MD): National Library of Medicine (US), National Center for Biotechnology Information; 2004 - [cited 2020 Oct 15.]

[10] Kohler, A., Kuo, A., Nagy, L. et al. (2015).Convergent losses of decay mechanisms and rapid turnover of symbiosis genes in mycorrhizal mutualists. Nat Genet, 47: 410–415.

[11] Richter, D. L. & Bruhn, J. N. (1986). Pure culture synthesis of Pinus resinosa ectomycorrhizae with Scleroderma aurantium. Mycologia, 78: 139–142.

[12] Mrak, T., Kühdirk, K., Grebenc, T., Štraus, I., Münzenberger, B., Kraigher, H. (2017). Scleroderma areolatum ectomycorrhizal on Fagus sylvatica L. Mycorrhiza, 27(3): 283-293.

[13] Mohan, V., Natarajan, K., Ingleby, K. (1993). Anatomical studies on ectomycorrhizas. Mycorrhiza, 3:51-56.

[14] Winner, M., Giménez, A., Schmidt, H., Sontag, B., Steffan, B., & Steglich, W. (2004). Unusual pulvinic acid dimers from the common fungi Scleroderma citrinum (common earthball) and Chalciporus piperatus (peppery bolete). Angewandte Chemie International Edition, 43: 1883-1886.

[15] Lopusiewicz, L. (2018). Scleroderma citrinum melanin: isolation, purification, spectroscopic studies with characterization of antioxidant, antibacterial and light barrier properties. World Scientific News: An international Scientific Journal, 94(2): 115-130.

[16] Soytong, K., Sibounnavong, P., Kanokmedhakul, K., Kanokmedhakul, S. (2014). Biological active compounds of Scleroderma citrinum that inhibit plant pathogenic fungi. International Journal of Agricultural Technology, 10(1): 79-86.

[17] Cardoso Filho, J. A., Pascholati, S.F., Sabrinho, R.R. (2016). Mycorrhizal association and their role in plant disease protection.In: Hakeem, K.R., & M.S. Akhar (Eds). Plant, Soil and Microbes, v2: Mechanisms and Molecular Interactions. Springer. P. 95-143.

[18] Rout, G. R., Sahoo, S. (2015). Role of iron in plant growth and metabolism. Reviews in Agricultural Science, 3: 1-24.

[19] Hemalatha, S., Mohan, V., & Sujatha, K. (2011). Effect of carbon sources on the growth of ectomycorrhizal fungi. Research J. Science and Tech, 3(1): 44-48.

Edited by Cheryl Zhang, Gaelle Gourdet, Audrey Tran, Amalia Peña Perez, Joshua Tagoe, students of Jennifer Bhatnagar for BI 311 General Microbiology, 2020, Boston University.