A Review of the Ubiquity of Ascomycetes Filamentous Fungi in Relation to Their Economic and Medical Importance

Mary Augustina Egbuta^1,2*, Mulunda Mwanza³, Olubukola Oluranti Babalola¹

¹Department of Biological Sciences, Faculty of Agriculture, Science and Technology, North-West University, Mafikeng Campus, Mmabatho, South Africa.
²Southern Cross Plant Science, Southern Cross University, Lismore Campus, Lismore, Australia.
³Department of Animal Health, Faculty of Agriculture, Science and Technology, North-West University, Mafikeng Campus, Mmabatho, South Africa.

DOI: 10.4236/aim.2016.614103                

Abstract

Filamentous fungi are found in different habitats in the environment including, air, water and soil. This group of fungi contains organisms from different classes under the sub-phylum Pezizomycotina. They occur in mixtures such that you find many genera of filamentous fungi dominating a particular habitat or substrate. The wide distribution of filamentous fungi has resulted in it being used for different purposes. This review aims to analyse the different genera of fungi species referred to as filamentous fungi and their relevance economically and medically.

Keywords

Filamentous, Fungi, Air, Soil, Water, Distribution

1. Introduction

Filamentous fungi which is a member of a large group of eukaryotes that includes some yeasts, moulds and some mushrooms, is also classified as a kingdom and separated from plants, protists, animals and bacteria. With cell walls containing chitin, a main disparity from plant cell walls which contain cellulose and bacterial cell walls, fungi are abundant in the environment and inconspicuous because of their small structures and their cryptic lifestyles on substrates they inhabit [1] . Naturally occurring in different parts of the environment and ecosystem, filamentous fungi which belong to a sub-kingdom of fungi referred to as “Dikarya” are some of the most abundant fungi known [2] .

Also referred to as molds, filamentous fungi are so called because they possess hyphae which form branches making up their mycelia, growing like threadlike structures. They are reported to occur naturally as well as contaminate different surfaces both indoors and outdoors. As a result of their vast occurrence in the environment, these types of fungi have been investigated from over the years for their positive and negative uses for mankind [3] [4] [5] [6] . Due to the ubiquitous occurrence of filamentous fungi and their applications in different sectors of mankind economy, this review aims to discuss in details the wide occurrence of filamentous fungi in our environment, describing the different genera of filamentous fungi in existence as well as analyzing the positive and negative importance of these groups of fungi to mankind.

2. Filamentous Fungi

As was mentioned in the introduction, one major characteristic contributing to classifying fungi as filamentous fungi is the ability to possess hyphae. A high number of known filamentous fungi tend to originate from the sub-Phylum “Pezizomycotina” which falls under the Phylum “Ascomycota”, also a part the sub-kingdom Dikarya [2] [7] . As indicated in the chart in Figure 1, filamentous fungi encompasses many genera of fungi including Aspergillus, Penicillium, Fusarium, Cladosporium, Emericella, Eurotium, Paecilomyces, Curvularia, etc. with Aspergillus, Penicillium, Fusarium, Alternaria and Cladosporium occurring most and more investigated than the other genera [8] . In the following sections the different genera of fungi in the group of filamentous fungi are mentioned and described taking cognisance of the most occurring and less occurring genera.

2.1. Aspergillus

A member of the Trichocomaceae family in the order Eurotiales, Aspergillus are reportedly the most abundant and widely distributed filamentous fungi globally although

Figure 1. Chart showing distribution of filamentous fungi in phylum Ascomycota ( [1] [2] [7] ).

they are more frequent in warmer regions occurring more frequently in mild zones than in warmer regions (Klich, 2002). Usually regarded as a soil fungi [9] they are a part of the filamentous fungi family, ubiquitous, cosmopolitan, found in nature and commonly isolated from soil, plant debris and indoor environment. They have the ability to grow at lower water activity and occur on storage food and feed which turn moldy. Some species of Aspergillus have been accepted to be mitosporic without any known sexual spore production while a teleomorphic state has been described for other species of Aspergillus [2] . With their characteristic dark colors, sometimes black, grey or green and in other cases white or milky colored, there are over 185 species of the genera Aspergillus in existence of which, A. fumigatus is the most commonly isolated species, followed by A. flavus and A. niger [10] . Other species of Aspergillus so far isolated, though less commonly so, include A. clavatus, A. glaucus group, A. oryzae, A. versicolor, A. nidulans, A. terreus, A. ustus, and a host of others [10] .

2.2. Fusarium

These group of filamentous fungi widely distributed in plants, the soil and known to contain a range of plant-pathogenic fungal species have been in existence for the past two centuries as it was first introduced in 1809 [11] . They are primary plant pathogens which require high water activity for growth and are characterized by production of septate, fusiform to crescent shaped macroconidia with or without microconidia [11] [12] . Aside from their ability to act as plant pathogens, Fusarium species have been linked to wide range of diseases and infections in humans and animals [13] . Commonly occurring species of the genus Fusarium include Fusarium verticilliodes, Fusarium graminearium, Fusarium proliferatum, Fusarium sporotrichiodes, Fusarium solani, Fusarium chlamydosporum amongst others [11] .

2.3. Penicillium

Penicillium species are among the most common decomposers in nature. This genus of Ascomycetes fungi are closely related to Aspergillus species but in general are less thermo-tolerant and are most prominent ecologically in cooler areas, though they are by no means absent in the tropics [14] . Genus Penicillium is characterized by the production of conidia in a structure termed a penicillus and widely distributed in the environment posing the argument of greater economic importance between Penicillium and Aspergillus. Although it is certain that Penicillium is more diverse in terms of species and range of habitats as they have the ability to grow in almost any environment [12] . A wide range of Penicillium species occur and as such include P. citreonigum, P. polonicum, P. digitatum, P. chrysogenum, P. roqueforti, P. citrinum, P. janthinellum, P. simplicissimum, P. aurantiogriseum, P. camemberti, P. verrucosum and P. expansum amongst others [12] .

2.4. Cladosporium

This genus is a commonly isolated genus belonging to the filamentous fungi group with its species occurring both as saprophytes and as plant pathogens; and producing olive- green to brown or black colonies [12] . They occur mostly in outdoor environment and only occur indoors on moist surfaces. Cladosporium species occur as pathogens on fresh fruit with one of the species Cladosporium fulvum being a common cause of tomato leaf mold [15] . Some common Clasdosporium species include C. fulvum, C. cladosporioides, C. herbarum, C. salinae, C. spinulosum, C. fusiforme, C. arthropodii amongst over 30 known species.

2.5. Alternaria, Acremonium and Curvularia

Alternaria species are reported to be major plant pathogens causing at least 20% of agricultural spoilage [16] . A member of the Pleosporaceae family, this genus include species that are found to occur almost everywhere indoors and outdoors growing thick green, black or grey colonies. Some of the isolated Alternaria species from water, food, air and plants include A. alternata, A. molesta, A. solani, A. japonica, A. longipes, and A. infectoria.

The genus Acremonium is reported to be a large and varied genus characterized by fine and hyaline hyphae which are produced mostly by simple phialides and single-celled conidia [14] . Commonly isolated from dead plant materials and soil, this genus comprises of up to 100 species with Acremonium strictum reported as one of the most common species isolated from food.

Mostly found in tropical regions and seldom in temperate zones, the genus Curvularia is a pathogen of many plant species and soil. This genus has the ability to withstand very high temperatures up to 40˚C which is the reason for its predominance in tropical regions [12] . Curvularia species are not as numerous as the other genera of filamentous fungi group and have been mostly isolated from soil and plant tissues/seeds. Some of Curvularia species include C. clavata, C. penniseti, C. protuberata, C. trifolii, C. tuberculata, C. lunata, C. pallescens, C. ovoidea, with C. lunata and C. pallescens commonly isolated [12] .

2.6. Emericella and Eurotium

The genus Emericella was first mentioned in 1857 [17] and is a teleomorph of Aspergillus species. Described to be the sexual state of Aspergillus species and because of this closeness species of this genus are likely to be present alongside their related Aspergillus species during long term growth [18] [19] . Producing ascopores (conidia) that are brightly colored with smooth to roughened texture [2] , species of the Emericella genus grow rapidly and are common in tropical and sub-tropical regions of the world [20] . The genus includes over thirty (30) species such as Emericella olivicola, E. nidulans, E. stellamaris, E. filifera, E. quadrilineata, E. discophora, etc. [18] [19] .

Closely related to the genus Emericella and also a member of the family Trichocomaceae, the genus Eurotium is another anamorph of Aspergillus species commonly found in tropical and sub-tropical regions in the world [2] They are characterized by spherical to ellipsoidal spores that grow in chains and are rough walled. Possessing a moderately rapid growth rate, colonies of Eurotium species are usually yellow or dull green to bluish green and have the ability to grow very well even at low water activity [21] . Common Eurotium species include Eurotium amstelodami, E. herbariorium, E. repens, E. rubrum and others [21] [22] .

2.7. Paecilomyces

Also a member of the same family as Aspergillus, Eurotium, Emericella and Penicillium, the genus Paecilomyces is often confused with the Penicillium genus because of their close morphological resemblance [2] . Growing rapidly, some species of this genus are regarded as thermophilic organisms due to their ability to grow well at high temperatures up to 50˚C [23] . Some commonly isolated Paecilomyces species include Paecilomyces variotii [24] , P. lilacinus [23] [25] and P. fulvus [26] .

3. Distribution of Filamentous Fungi in the Environment

As a result of their ubiquitous nature, filamentous fungi are widely distributed in the environment. The vast variety of substrates on which filamentous fungi are able to grow on has also contributed to their wide distribution in the environment worldwide [27] . Although most filamentous fungi require high temperatures and high humidity like the Aspergillus species [2] which results in their species occurring mostly in hot and humid regions of the world, some fungi like the Penicillium species also have the ability to grow in temperate areas [2] causing such species to occur in colder areas of the world. In this case, filamentous fungi can be found in almost every part of the environment. In continuation of this review, we would evaluate their distribution in three habitats of the environment: air, soil and water. This is illustrated further in Table 1.

3.1. Air

Present in both outdoor and indoor air, species of the filamentous fungi family are widely distributed in air [36] [63] . They have been isolated from air samples collected from different areas such as hospitals, outdoor areas and households [37] [63] [64] . Among the many species of filamentous fungi, the Aspergillus, Penicillium and Cladosporium genera have been mostly isolated with lesser occurrence of Fusarium and other species [65] . Within the genus Aspergillus, A. flavus, A. niger and A. fumigatus are the most common species isolated from air samples collected from both indoor and outdoor areas [36] [64] [66] .

3.2. Soil

The growth pattern of filamentous fungi mycelia which is mainly hyphelial extension and branching has contributed to the potential of a wide range of filamentous fungi species to be found occurring naturally in soil from different regions of the world [67] . The occurrence of filamentous fungi such as Penicillium, Aspergillus, Trichoderma, Curvularia, Paecilomyces species, etc. have been reported in soil from semi-arid areas characterized by low rainfall [35] . The presence of a variety of filamentous fungi species

Table 1. Distribution of filamentous fungi in the environment.

have also been reported in soil from colder regions like the Antarctica by Kurek et al. [68] and Hughes et al. [69] . Although humidity is one condition which favors growth of filamentous fungi, some species of this family of fungi such as Aspergillus, Cladosporium, Penicillium and Alternaria species are able to thrive in soil from desert areas including areas that have not recorded rainfall in decades [70] .

3.3. Water

Odor and taste in water has been attributed to the presence of fungi in it [71] [72] . Fungal biomass has been reported in water systems from different parts of the world [73] [74] . A range of genera of filamentous fungi have been isolated from different sources of water. These sources include rivers, underground water, dead sea water, tap water and bottled water. Yamaguchi et al. [75] , Warris et al. [76] and Okpako et al. [77] reported isolation of Penicillium, Aspergillus, Cladosporium, Alternaria and other genera of filamentous fungi form tap water and drinking water. Occurrence of filamentous fungi genera with Penicillium, Cladosporium and Alternaria species dominating has also been isolated from bottled and processed water [77] . Filamentous fungi isolated from rivers and underground water include Penicillium species and other genera of this family [78] , also, they occur in water high in salts and minerals [79] . Amongst the commonly occurring filamentous fungi genera, Fusarium species have been seldom isolated from water [71] [76] [80] with little or nothing reported in regards to Fusarium occurrence in water.

4. Economic Importance of Filamentous Fungi

Filamentous fungi are currently being used in the manufacturing and agricultural sectors all over the world. They are a source of raw materials for food, chemical, pharmaceutical and cosmetic industries [81] [82] [83] . Apart from their positive impacts, filamentous fungi can have negative economic impacts, thus being beneficial or detrimental economically. There is therefore a need to evaluate the economic advantages and disadvantages of filamentous fungi as presented in Table 2.

4.1. Agriculture

Filamentous fungi have been implemented as bioremediation agents [96] [97] , degrading the contents of high chemically contaminated soil and thereby reducing toxicity of the soil. Species such as A. flavus and Paecilomyces farinosus have the ability to degrade Benzo [a] pyrene in soil (Romero et al. [84] , whereas, Fusarium species can also bio-re- mediate soils high in polycyclic aromatic hydrocarbons [98] . The discovery of filamentous fungi activity in bioremediation of soil has prompted more studies of other naturally occurring soil filamentous fungi for bioremediation properties. One example of such is a study by Kurniati et al. [85] whereby filamentous fungi were investigated for reducing mercury in soil. These micro-organisms have also made positive impacts in their use as biocontrol agents against microbes and harmful compounds in plants and crops [89] [90] [99] . The potential of using filamentous fungi in biofuel production

Table 2. Economic applications of filamentous fungi.

has been investigated by Zheng et al. [100] and found to be feasible.

Some genera of filamentous fungi are reported in association with plant diseases and food spoilage in agriculture, contaminating crops at different stages of production [101] . Aspergillus species such as A. niger, A. flavus, A. fumigatus, A. alliaceus, A. carbonarius and A. ochraceus, as well as Fusarium, Penicillium and Alternaria genera are some examples that cause infections and contamination in plants and plant products respectively [26] [101] [102] . Fungal Infection/ contamination of food crops and food products results to a reduced nutritional value and quality of food crops [102] as well as subsequent economical losses [103] .

4.2. Manufacturing Industry

In the paper manufacturing industry, filamentous fungi are implemented in the manufacture of high quality paper suitable for writing and printing [104] , with reports that fungal mycelium make up about 10% of good paper quality content. The use of filamentous fungi in industries to compost industrial waste has also been reported by Mohammad et al. [105] indicating the contribution of these micro-organisms in disposal of waste generated from processing palm produce.

4.3. Food Industry

As a source of different enzymes [106] [107] [108] , filamentous fungi are currently being used in different areas of the food manufacturing industry [2] . The activity of filamentous fungi during fermentation has contributed to its use in food manufacturing. An example of such is the use of A. niger for fermentation to produce citric acid [109] [110] , which is one of the main sources of industrially produced citric acid. Also, the ability of filamentous fungi to produce enzymes, vitamins, lipids, proteins, flavors and other valuable compounds which are implemented in food production [111] .

4.4. Pharmaceutical/Medical

Chemical compounds produced by filamentous fungi are important to the medical and pharmaceutical industry. This importance can be beneficial or detrimental properties of the compounds and their effects on both humans and animals. Filamentous fungi produce different metabolites that have proven to have different inhibitory effects in metabolic pathways. An example of such compounds are the statins which include lovastatin produced by A. terreus [112] , mevastatin produced by P. citrinum [113] and pravastatin produced by P. chrysogenum [114] . The function of statins is to inhibit the enzyme hydroxymethyl glutaryl-Coenzyme A (HMG-CoA) reductase which is the first enzyme in cholesterol biosynthesis [113] , thereby lowering blood cholesterol levels in individuals who have high cholesterol levels. Some other filamentous fungus (Fusarium oxysporum) have been investigated and found to produce Cyclosporin-A(an immunosuppressant) currently used in the treatment of cancer, organ transplant patients and in the treatment of auto-immune diseases including AIDS [115] .

The ability of filamentous fungi to inhibit microbial growth has also been investigated. He et al. [116] found that filamentous fungi species could produce pyrrocidines A and B, which are effective antibiotics against gram-positive bacteria including resistant strains. Echinocandins produced by Aspergillus species have been reported by Goswami et al. [117] to inhibit an enzyme that facilitates fungal cell wall formation in fungal species. Other anti-microbial activities of filamentous fungi reported include inhibition of Escherichia coli, Staphylococcus aureus and Candida albicans [118] and anti-oxidant activities [119] . Filamentous fungi biofilm are currently used as biocatalysts for the production of human drug metabolites since they have been proven to have longer effective time [120] . This is a process required for drug development which contributes to assessing toxicity of a drug in pharmacokinetic studies.

5. Conclusion

This review has reported that the distribution of filamentous fungi in our environment is an obvious fact that cannot be disputed. The eventual result of this distribution is the implementation of filamentous fungi by mankind in different industries. Considering the pros and cons of filamentous fungi discussed in this review, it is evident that filamentous fungi can be both beneficial and detrimental to the human race. In that regard, more research is encouraged to exploit the positive uses of these groups of diverse organisms as well as carry out studies to investigate ways of reducing their harmful effects.

Acknowledgements

The authors wish to appreciate North-West University for providing the academic environment to prepare this review and the National Research Foundation (NRF), for providing funding for the study.

Conflict of Interest

The authors hereby declare that there are no conflicts of interest.

Conflicts of Interest

The authors declare no conflicts of interest.

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