Cladosporium sphaerospermum

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Classification

Full lineage of C. sphaerospermum : cellular organisms; Eukaryota; Opisthokonta; Fungi; Dikarya; Ascomycota; saccharomyceta; Pezizomycotina; leotiomyceta; dothideomyceta; Dothideomycetes; Dothideomycetidae; Capnodiales; Cladosporiaceae; Cladosporium; Cladosporium Sphaerospermum [1].

NCBI: [1]

Introduction

Cladosporium Sphaerospermum is a cosmopolitan saprobic fungus that inhabits a variety of environments. Predominantly airborne, it is found in indoor and outdoor air and sampled from not only dwelling and plants but humans also [2]. As a halotolerant microorganism, C. sphaerospermum thrives in areas of high salinity. It can also proliferate in the areas of moderate and low salinity [3]. Phylogenetic analysis of RNA suggests that C. sphaerospermum is a complex fungal species encompassing a number of different strains. Recent studies show that C. sphaerospermum, an infectious and allergenic anthropologic fungus [4], can survive and thrive in the areas of high radioactivity and can reduce levels of radiation [5]. Moreover, industrial off-gas emissions, namely aromatic hydrocarbons, ketones and some organic acids can also be degraded by C. sphaerospermum [6], rendering the fungus a potential model to study natural biofiltration mechanisms. In addition, C. sphaerospermum can possibly become a substitute for chemical fertilizers due to its ability to produce gibberellins [7], plant growth hormones that are essential for plant growth and development [8].

Genome structure

Although a number of strains of C. sphaerospermum have been discovered, only one has been sequenced. C. sphaerospermum UM843 was isolated from human blood culture and the genome was sequenced in 2012. It is in the vicinity of 31.92Mb [8]. The genome consists of a total of 10,020 genes, with approximately 94% encoding for proteins of longer than 100 amino acids. The exon frequency in the proposed model was 2.26 exons per gene [8]. Among the genes detected in the gnome were the once associated with human allergens, the genes for asenolase, aldehyde dehydrogenase, and mannitol dehydrogenase. Some of the genes found in the genome of C. sphaerospermum are linked to the resistance to the antifungal drugs fluconazole, quinidine, and fluorocytosine. The genome also includes sequences encoding for the key enzymes in the melanin biosynthesis pathway [8].

Cell structure

Thick-walled flagellate cells of this fungus form a dikaryon in which, after cytoplasmic fusion of two cells (plasmogamy), the two nuclei cohabit without fusion. Dikaryotic cells are most common for the ascogenous hyphae and the ascocarp of the fungus rendering the rest of the mycelia monokaryotic. The spores of C. sphaerospermum have different shapes and are released through an apical pore [1]. Under magnification, the fungus appears to form tree-like structures principally assembled by branching chains of dark round conidia. Although conidia are 3-4.5 μm in diameter and often single-celled, they frequently form chains by budding, leaving the youngest cell at the tip of the chain [1]. The older conidia might become oblong or shield-shaped and reach 15 μm in length. Upon budding, C. sphaerospermum conidia often undergo septation and thus might have numerous constriction scars. At 30°C, Cladosporium sphaerospermum forms 1.0 cm in diameter powdered dark grey/green colored colonies that look like domes [1].

Metabolic processes

As a saccharaomycetae, C. sphaerospermum use various metabolic enzymes to convert glucose, sucrose and starch into carbon dioxide and alcohol [6]. Some of the C. sphaerospermum strains, however, use different types of metabolic adaptations to withstand extreme environments. Halotolerant C. sphaerospermum, for example, increases activity of extracellular invertase when grown in the environment of high salinity [9]. Other e enzymes that increase activity in such environments are fructose 1,6-diphosphate aldolase, isocitrate lyase, and cytosolic malate dehydrogenase. Adaptive response of C. sphaerospermum extends to its ability to grow on toluene as a source of carbon and energy [10]. In fact, C. sphaerospermum is the first eukaryotic organism that was reported to catabolize toluene as the sole source of carbon and energy. C. sphaerospermum is also a producer of secondary metabolites. Among them are citrinin, quinolactacin A1 and A2, oxylipins [11], and melanin [12]. It is most likely that due to production of citrinin, which is a mycotoxin, some strains of C. sphaerospermum are considered plant pathogens because citrinin causes chromosome breakage, modification of amino acid uptake, inhibition of seed germination, and polyploidy in plants [13]. Quinolactacins are known tumor necrosis factor inhibitors [14]. However, the function of quinolactacins in C. sphaerospermum is not clear. Oxylipins, or oxidized fatty acids, include prostaglandins that are essential for fungal cell communication and viability [15].

a. Melanin metabolism.

Melanin is one of the secondary metabolites produced by C. sphaerospermum. It provides protection from ultraviolet light and oxidizing agents, as well as facilitates fungal proliferation in the areas with high radiation levels [16]. It is, however, unlikely that melanin is metabolized by C. sphaerospermum— solely for protection, as some microorganism can survive exposure to high radiation regardless of melanization. Mechanisms of melanin synthesis in C. sphaerospermum are chemically diverse and not yet well understood. However, there is evidence that this fungus produces melanin from an endogenous substrate via a 1,8-dihydroxynaphthalene (DHN) intermediate [1]. Recent microscopic studies show that granulated melanin is localized to the cell wall where it participates in cross-linking with polysaccharides. It is likely that the internal vesicles similar to mammalian melanosomes are the sites of melanin synthesis in C. sphaerospermum. Melanin is transported to the cell wall via these vesicles [1].

b. The use of ionizing radiation.

In light of recent accidents on nuclear power plants, particularly the one on Chernobyl power plant in 1986, it has been discovered that C. sphaerospermum can withstand high levels of radiation and use it to its advantage. Production of melanin by the fungus is linked to its ability to colonize areas of high radioactive contamination (26). Moreover, in presence of radiation, C. sphaerospermum can thrive on high nutrient media as well as on the minimal nutrition media. Studies conducted with samples from Chernobyl indicate that change in electronic properties of melanin induces fungal proliferation (27). In 2007, Dadacheva et al. showed that after exposure to radiation the electronic structure of melanin changes. They also demonstrated that the ability of melanin to transfer electrons in the NADH oxidation/reduction reaction increased 4-fold [1]. The stable free radicals in melanin can interact with high-energy electrons that can damage fungal DNA. The interaction of the free radicals created by gamma radiation with the stable radicals in melanin protects DNA from radiation damage because the free radicals are prevented from entering the cell since melatonin is localized to the cell wall and extracellular space [1]. Moreover, the melanised fungal cells that were exposed to radiation levels 500 fold higher than background level grew considerably faster than nonmelanised fungus or the cells that received background level of radiation. Additional studies about the effects of radiation on C. sphaerospermum show directional growth of the fungus toward the source of radiation [1]. Thus, it is possible that C. sphaerospermum, facilitated by melanin, can capture ionizing radiation and use it for metabolic energy [1].

c. Degradation of volatile organic compounds.

Volatile organic compounds (VOC’s) degraded by melanised fungi include aromatic hydrocarbons, ketones, and organic acids. It has been discovered that C. sphaerospermum can use its metabolic machinery to degrade nine of different VOC [1]. For example, toxic for central nervous system in humans and animals, toluene can be degraded by the fungus and used as a single source of carbon and energy. In this fungus, methyl group of toluene is initially attacked to form benzoate via hydroxylation. By using NADPH and O2 to oxidize toluene, glycerol, EDTA, DTT, and PMSF, toluene monooxygenase catalases assimilation of toluene by the fungus [1]. Further hydroxylation of benzoate to 4-hydrozybenzoate leads to formation of protocatechuate as the ring fission substrate [1]. Benzene, ethylbenzene, styrene, methyl ethyl ketone methyl isobutyl ketone, and methyl propyl ketone, along with n-butyl acetate and ethyl 3-ethoxypropionate can be used by C. sphaerospermum as a sole carbon and energy source [1].

d. Gibberellins production.

One of the strains of C. sphaerospermum can potentially become a substitute for chemical fertilizers due to its ability to produce gibberellins, plant growth hormones that are essential for plant growth and development [1]. It has been shown that newly identified based on 18s rDNA sequence MH-6 strain of C. sphaerospermum is an endophytic fungus that produces nine different gibberellins inducing those responsible for maximal shoot elongation in plants. The mechanism by which gibberellins are produces by this fungus has yet to be elucidated. However, Hamayun et all determined that biosynthesis pathway of gibberellins in C. sphaerospermum is similar to that of F. fujicori, a known producer of gibberellins [1].

Ecology

C. sphaerospermum is a complex species that can grow in extreme and polar environments. This psychrotolerant, UV resistant, and halotolerant fungus can survive in Antarctica. It can also survive at 25-30°C in the areas where some of the strains were isolated in low salinity environments [1]. Saprobe, C. sphaerospermum also lives in symbiotic relationships with live plants. Some strains of C .sphaerospermum are able to adopt and thrive in areas exposed to high levels of ionizing radiation [1].

Pathology

C. sphaerospermum is one of the most commonly isolated airborne contaminants. Some of the strains of the fungus are not pathogenic to humans and animal; they are, however, detrimental to plants. Some of the species, for example, can cause cerebral and cutaneous phaehyphomycoses, sinusitis, and peritonitis in humans [1]. In 2003 a case was reported of a woman who developed intrabronchial lesion due to C. sphaerospermum [1]. In animals, skin and lungs are the most affected by the fungus organs. For example, exposed to the fungus mice showed systemic and subcutaneous infections and even death in immunocompromised mice [1]. C. sphaerospermum can also cause erratic behavior in red snappers following infection of the bladder and kidney [1]. Eledone cirrhosa, the lesser octopus, is also not immune to infection by this fungus [15].

Unanswered questions.

• Quinolactacin Al and quinolactacin A2 isolated from Pinicillium citrinum can inhibit acetylcholinesterase activity of which is linked to senile dementia in Alzheimer patients (45). It begs a question: can quinolactacin Al and quinolactacin A2 isolated from C. sphaerospermum also be used in studies of patients with Alzheimer disease? • Is it possible to isolate strains of C. sphaerospermum that produce quinolactacin Al and quinolactacin A2 by growing them first in radioactive environment to induce proliferation of the fungus in order to obtain high yield of the metabolites? • What effect of such metabolites will have on mammalian cells? • Prostaglandin E2 (PGE2), a hormone-like compound, is linked to smooth muscle functioning and immune response in humans (46). Since C. sphaerospermum can produce oxylipins, do any of the strains produce PGE2? If so, could the production of PGE2 by the fungus be the reason of anthropologic allergic reaction to it? • Can some strains of this fungus be used as potential fertilizers since they can produce gibberellins? If so, will using C. sphaerospermum as a fertilization element induce adverse or beneficial reaction in mammals? • Considering the ability of C. sphaerospermum to grow and capture ionizing radiation along with its metabolism of volatile organic compounds, can this fungus be used as a universal bioradioremediator?

References

[1] [Campbell, C., Johnson, E., & Warnock, D. W. (Eds.). (2013). Identification of Pathogenic Fungi (2nd Edition). Somerset, NJ, USA: John Wiley & Sons. Accessed 29 Oct. 2014, http://www.ebrary.com.]
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[8] [Polglase, J., Dix, N. and Bullock, A. (1984). Infection of skin wounds in the lesser octopus, Eledone cirrhosa, by Cladosporium sphaerospermum. Transactions of the British Mycological Society, 82(3), pp.577--580.]
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[10] [Weber, F., Hage, K. and De Bont, J. (1995). Growth of the fungus Cladosporium sphaerospermum with toluene as the sole carbon and energy source. Applied and environmental microbiology, 61(10), pp.3562--3566.]
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[21] [Hamayun M, Khan SA, Khan AL, Rehman G, Kim YH, Iqbal I, Hussain J, Sohn E.Y. and Lee I. J. (2010) Gibberellin production and plant growth promotion from pure cultures of Cladosporium sp. MH-6 isolated from Cucumber (Cucumis sativus. L). Mycologia  102:989–995.]
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Edited by [Sviatlana Rose], student of Jennifer Talbot for BI 311 General Microbiology, 2014, Boston University.