Freshwater Fungi as a Source of Chemical Diversity: A Review

Abstract

As their name indicates, freshwater fungi occur on submerged substrates in fresh water habitats. This review brings together the chemical diversity and biological activity of 199 of the 280 known freshwater fungal metabolites published from 1992 to 2020, representing at least seven structural classes, including polyketides, phenylpropanoids, terpenoids, meroterpenoids, alkaloids, polypeptides, and monosaccharides. In addition to describing what they are, where they are found, and what they do, we also discuss strategies for the collection, isolation, and identification of fungi from freshwater habitats, with the goal of enhancing chemists' knowledge of several mycological principles. We anticipate that this review will provide a springboard for future natural products studies from this fascinating but underexplored group of Ascomycota.

Figure 1.

The number of new freshwater ascomycetes described from freshwater habitats. Professor C.T. Ingold, the first to recognize the occurrence of a distinctive freshwater Ascomycota, published a series of papers about fungi on submerged substrates in the Lake District, England between 1951–1955.^– Note the increase since the reviews by Shearer on the freshwater ascomycetes in 1993 and 2001.^,

Figure 2.. An infographic displaying the types of freshwater fungi.

A freshwater stream is meandering through a riparian zone. Submerged dead wood and herbaceous materials, such as leaf litter, fall from these trees into the stream and are decomposed by freshwater fungi. Upon incubating submerged wood in plastic boxes with moistened paper towels, fruiting bodies of freshwater ascomycetes (sexual states; left) form on the wood. When decomposed leaf litter is cut into circles and submerged in distilled water, after a few days, Ingoldian hyphomycetes (asexual states; right) appear floating in the water. The sexual (teleomorphic) forms are more prevalent on submerged wood, while the asexual (anamorphic) forms usually occur on submerged leaf litter.

Figure 3.

Variety of ascospores and conidia of freshwater ascomycetes and hyphomycetes. Panels a-c, freshwater ascomycetes: a. Minutisphaera fimbriatispora (picture credit, C.A. Shearer), b. Luttrellia halonata (picture credit, A. Ferrer), and c. Lindgomyces ingoldianus. Panels d-f, conidia of aquatic (Ingoldian) hyphomycetes: d. Dendrospora erecta, e. Anguillospora crassa, and f. Lemonniera sp. Panels g-h, conidia of aeroaquatic hyphomycetes: g. Cancellidium applanatum (picture credit, S.E. Zelski), and h. Helicodendron sp. (picture credit, C.A. Shearer). Scale bars: a, c, f, h = 20 μm, b, d, e = 10 μm, g = 200 μm.

Figure 4.

Conidia of submerged-aquatic hyphomycetes or miscellaneous freshwater mitosporic fungi: a. Coleodictyospora sp., b. Xylomyces sp., c. Bactrodesmium abruptum, and d. Sporoschisma saccardoi. Scale bars: a-d = 10 μm (images taken from the Freshwater Ascomycetes Database: http://fungi.life.illinois.edu, maintained by C.A. Shearer and H.A. Raja).

Figure 5.

Outline of the stages of collection, transport, incubation, and isolation of freshwater ascomycetes: a. Submerged wood or herbaceous material is collected from freshwater habitats; b. The soft decorticated material is put in plastic bags with a lining of paper towels to absorb excess water. Substrates should be moist but not overly wet; c. In the lab, the substrates are rinsed with distilled water and placed in a covered plastic box with moist paper towels; d. The substrates are examined monthly for 3–6 months for sexual (asci and ascospores) or asexual (conidia) structures; e. With a pair of sterile needles, the spores (whether sexual or asexual) are gently spread on the surface of the water agar with antibiotics; f. After 24–48 h, depending on rate of germination, the spores are aseptically transferred to nutrient agar, such as potato dextrose; antibiotics are included in the media to prevent growth of bacteria, which can be prevalent in fresh water.

Figure 6.

Geographical distribution of the freshwater fungal strains sampled to study chemical diversity (n = 49). Large gaps remain in our knowledge regarding freshwater fungal chemical investigations. Notably, South America and Africa are two continents where there have been no chemical studies of freshwater fungi reported in the literature, which suggests that the vast areas of the earth remain unsampled for freshwater fungal chemical diversity.