**2.1 The role of fungi as decomposers, predators, endophytes, symbionts, parasites, plagues & pathogens**

Aquatic fungi are heterotrophs, i.e. they *sensu stricto* depend on external organic matter, which may be dead or alive. Aquatic systems harbour a wealth of organisms that can serve as suitable hosts: algae from different phyla, cyanobacteria, protists, zooplankton, fish, birds, mussels, nematodes, crayfish, mites, insects, amphibians, mammals, plants and other fungi (Sparrow, 1960; Ellis & Ellis, 1985). Fungi are omnipresent and therefore associated with almost every organism, often as parasites, sometimes as symbionts and of course as decomposers.

Parallel to fungi in soil, aquatic fungi act as prominent decomposers of POM: foremost coarse particulate organic matter (CPOM) including plant and animal debris. Filamentous growth habit is a key feature of many aquatic fungi, and this feature is responsible for their superiority to heterotrophic bacteria as pioneer colonisers. Hyphae allow fungi to actively penetrate plant tissues and tap internal nutrients. Therefore, Gessner & Van Ryckegem (2003) describe fungal hyphae as self-extending digestive tracts that have been turned inside out growing hidden inside the substrate.

The aquatic fungi which typically decompose leaf litter and wood with a hyphal network are the polyphyletic group known as "aquatic hyphomycetes". Aquatic hyphomycetes are most common in clean, well oxygenated, flowing waters (Ingold, 1975; Bärlocher, 1992), and are characterised as anamorphic fungi with tetraradiate or sigmoid conidia (asexual reproductive structures). Taxonomically, they are mainly associated with the *Ascomycota*, and only a small percentage is affiliated with the *Basidiomycota*. In contrast, aero-aquatic hyphomycetes colonise submerged plant detritus in stagnant and slow flowing waters, such as shallow ponds and water-filled depressions. Taxonomically, most aero-aquatic fungi are classified as *Ascomycota*, although four aero-aquatic species have been classified as *Basidiomycota*, and one as O*omycete* (Shearer et al., 2007). These fungi are adapted to habitats with fluctuating water levels subjected to periodic drying, low levels of dissolved oxygen, and elevated levels of sulfide. Therefore, they have buoyant conidia that are released at the water surface as water levels recede. Along with aquatic fungi, terrestrial fungi enter the aquatic realm as pioneer decomposers and endophytes of allochthonous plant debris. In the water, however, they are partially replaced by true aquatic hyphomycetes. After colonising the substrate and forming internal hyphal networks, the POM is macerated at least partly by the fungi themselves. This process is often accelerated by the feeding activity of macroinvertebrates, which find colonised leaves to be more palatable (compiled in Bärlocher, 1992; Gessner & Van Ryckegem, 2003). With the aid of an array of extracellular enzymes, aquatic fungi are able to degrade most of the polymeric substances in leaves (hemicelluloses, cellulose, starch, pectin and to some extent lignin; Krauss et al., 2011). Depending on leaf litter type and water chemistry, fungal leaf decomposition can extend over 1 to 6 months. The situation is slightly different for fungal decomposition of emergent macrophytes, because decomposition starts in standing shoots. Over 600 species of fungi have been recorded from the litter of *Phragmites australis* alone (Gessner & Van Ryckegem, 2003). Ninety four percent of these 600 species were members of *Ascomycota* and only 6%

Aquatic Fungi 231

A cornerstone of fungal lifestyle is parasitism. The life cycle of parasitic fungi is identical to that of saprophytic fungi with one exception: the host cells are still alive. Therefore, it is often impossible to separate opportunistic fungi colonizing senescent hosts from the true parasitic fungi reducing the fitness and in some cases even causing death to their previously healthy hosts. Prominent aquatic parasitic fungi belong to *Chytridiomycota* and *Oomycetes*. The host spectrum of these aquatic fungi is broad and covers every phylum including fungi itself (Sparrow, 1960; Van Donk & Bruning, 1992; Ibelings et al., 2004; Kagami et al., 2007). Encounters with fungi can be fatal to algae, particularly if their defence system is breached by the fungus. The ecological relevance of this negative interaction becomes evident when it is considered that suicide is a common defence mechanism in algae. If this controlled progress, called hypersensitivity, is initiated at the right moment during fungal infection, it results in the successful interruption of the fungal infection cycle, because the parasite's ability to reproduce via spore production is inhibited. Such "behaviour" allegorises a beneficial sanction since it protects the healthy algal population by reducing the abundance of the deadly parasite. However, if unsuccessful the parasite prevails and mass mortality of

In rare, but important cases, fungi cause severe damage to larger aquatic organisms. Some fungi, mainly but not exclusively *Oomycetes*, infect fishes or fish eggs (Noga, 1993; Chukanhom & Hatai, 2004) and thereby exert strong population pressure. This is of great importance for aquaculture since it necessitates antifungal treatments, but even in natural systems, fungi have the potential to severely harm the indigenous fish population. *Aphanomyces astaci* (*Oomycetales*) causing the crayfish plague has driven the European crayfish (family *Astacidea*) population to the edge of extinction (Reynolds, 1988). In contrast, *Coelomomyces* (*Blastocladiomycota*) effectively infecting several mosquito species (Sparrow, 1960) has been discussed as a biological control for malaria mosquitoes (Whisler et al., 1975). The most infamous fungal parasite is *Batrachochytrium dendrobatidis* (*Chytridiomycetales*), which contributes to worldwide extinction of several known and unknown amphibian species (Berger et al., 1998; Skerratt et al., 2007). Aquatic plants are also greatly affected by fungal parasites. A recently discovered plant parasite is *Pythium phragmites* (*Oomycetales*), obviously being an important causative agent of reed decline (Nechwatal et al., 2005). Some human pathogens may also be found amongst the aquatic fungi. Common freshwater yeasts belonging to *Candida* and *Cryptococcus* are both potentially harmful to humans (e.g. *C. albicans* and *C. tropicalis*). These fungi are frequently found along bathing sites (Vogel et al., 2007). Several typical dermatophytes and keratinophylic fungi are transferred via water and can also occur in aquatic ecosystems (Ali-Shtayeh et al., 2002). *Chytridiomycetes* and "Microsporidia", however, are rarely pathogenic and only infect immune-deficient patients. Additionally, black yeasts are on occasion salt-tolerant and thus can cause problems when

Life cycles of aquatic fungi cover a broad spectrum from very simple cell divisions to very complex cycles, crossing the terrestrial-water boundary. Starting with basal fungal lineages, Microsporidia are intracellular parasites with an extremely reduced genome (down to 2.3 Mbp, which is half the genome size of the common enterobacterium *Escherichia coli*). They are transmitted passively with non-motile spores, which have a size range of 1 - 50 µm. Endospores are chitinous and mature inside host-cells, where they are eventually released

algae results. This can lead to shifts in the algal community composition.

consuming salt preserved food (Butinar et al., 2005).

by an extrusion apparatus (summarised by Keeling & Fast, 2002).

**2.2 The life cycles of aquatic fungi** 

belonged to *Basidiomycota*. The *Ascomycota*, in turn, comprised 30% aquatic hyphomycetes (with "naked" conidia) and 22% coelomycetous anamorphs (producing conidia inside a fruiting body). Thirty species isolated from the standing dead shoots of *Juncus effusus*  (Kuehn & Suberkropp, 1998) were also mainly composed of aquatic hyphomycetes and coelomycetes. White rot *Basidiomycetes*, generally not considered being active in aquatic habitats, have also been isolated from standing dead aerial shoots in wetlands. In the case of small particles such as algae, pollen, seeds and zooplankton carcasses, decomposition is achieved by the much smaller *Oomycetes* and *Chytridiomycetes*, rather than the aquatic hyphomyctes. These organisms do not depend on macro-scale hyphal networks and are capable of very fast responses to changes in their environment. Their motile spores actively search for adequate substrates using chemotaxis. Once a suitable substrate has been reached, an appressorium is formed and the particle is invaded by tiny rhizoids tapping the internal nutrient reservoirs for production of new spores in a sporangium (either endo- or ectophytic; Sparrow, 1960; Sparrow, 1968 and references therein). Thereby, their whole life cycle can be completed in days. The short generation times and prolific spore production characterise these fungi as typical r-strategists.

Another polyphyletic group of aquatic fungi (with members of *Oomycetes, Zoopagomycotina* and *Basidiomycetes*) is specialised to hunt by using traps. These predatory fungi are often found on decomposing plant material or animal egesta. They use sticky traps, networks or slings to entrap their prey, usually amobae, rotifers, nematodes, liver flukes and small arthropods like mites. After the prey is caught, these fungi penetrate the prey's tissue and digest it from the inside. Generally, it is assumed that this behaviour supplies these fungi with additional nutrition when colonizing decomposing plant detritus. In soil, additional groups of endoparasitic fungi are found, e.g. on nematodes (Family *Hyalosporae* & *Entomophthoraceae*) which also destroy their prey from the inside (Karling, 1936; Drechsler, 1941; Peach, 1950, 1952, 1954; Sparrow, 1960; Swe et al., 2008).

An additional strategy of fungi with presumably long annual life cycles, is to grow inside living plants without affecting the host's viability. Yet, it is unclear whether the host plant benefits from these "endophytes" or if the relationship between plant and fungi is solely based on commensalism. Obviously, when the host plant enters senescence, all internal fungi have a great advantage over the secondary colonising fungi since the primary rule of "first come, first serve" is of major importance for growth and reproductive success.

An important group of endophytic fungi, which is clearly beneficial for the plant, consists of mycorrhiza forming symbionts present in the roots of several aquatic macrophytes. Many mycorrhiza forming symbionts belong to a phylum of the "lower fungi" called *Glomeromycota*. Certain orders of the *Glomeromycota* are obligate root symbionts characterized by a vesicular arbuscular mycorrhiza (VAM) that supply their hosts with nutrients. In return, the host plant provides the fungus with sugars rich in energy, amongst other things. VAM fungi were formerly believed to be purely terrestrial, but today it is known that they are particularly important in nutrient poor clear waters. For example, in oligotrophic waters, VAM fungi allow macrophytes to grow under nutrient limiting conditions by supplying the plant with solid-phase bound nutrients (Baar et al., 2011).

Freshwater algae, e.g. *Dunaliella* and the autotrophic protozoan *Euglena* can establish a mutual relationship with the fungus *Bispora* or the yeast *Cryptococcus,* respectively (Gimmler, 2001). Moreover, fungi belonging to the *Kickxellomycotina* are endosymbionts of invertebrates, especially of aquatic arthropods and - together with specialised protozoans are summarised under the term trichomycetes (Lichtwardt, 2004; Hibbett et al., 2007).

belonged to *Basidiomycota*. The *Ascomycota*, in turn, comprised 30% aquatic hyphomycetes (with "naked" conidia) and 22% coelomycetous anamorphs (producing conidia inside a fruiting body). Thirty species isolated from the standing dead shoots of *Juncus effusus*  (Kuehn & Suberkropp, 1998) were also mainly composed of aquatic hyphomycetes and coelomycetes. White rot *Basidiomycetes*, generally not considered being active in aquatic habitats, have also been isolated from standing dead aerial shoots in wetlands. In the case of small particles such as algae, pollen, seeds and zooplankton carcasses, decomposition is achieved by the much smaller *Oomycetes* and *Chytridiomycetes*, rather than the aquatic hyphomyctes. These organisms do not depend on macro-scale hyphal networks and are capable of very fast responses to changes in their environment. Their motile spores actively search for adequate substrates using chemotaxis. Once a suitable substrate has been reached, an appressorium is formed and the particle is invaded by tiny rhizoids tapping the internal nutrient reservoirs for production of new spores in a sporangium (either endo- or ectophytic; Sparrow, 1960; Sparrow, 1968 and references therein). Thereby, their whole life cycle can be completed in days. The short generation times and prolific spore production

Another polyphyletic group of aquatic fungi (with members of *Oomycetes, Zoopagomycotina* and *Basidiomycetes*) is specialised to hunt by using traps. These predatory fungi are often found on decomposing plant material or animal egesta. They use sticky traps, networks or slings to entrap their prey, usually amobae, rotifers, nematodes, liver flukes and small arthropods like mites. After the prey is caught, these fungi penetrate the prey's tissue and digest it from the inside. Generally, it is assumed that this behaviour supplies these fungi with additional nutrition when colonizing decomposing plant detritus. In soil, additional groups of endoparasitic fungi are found, e.g. on nematodes (Family *Hyalosporae* & *Entomophthoraceae*) which also destroy their prey from the inside (Karling, 1936; Drechsler,

An additional strategy of fungi with presumably long annual life cycles, is to grow inside living plants without affecting the host's viability. Yet, it is unclear whether the host plant benefits from these "endophytes" or if the relationship between plant and fungi is solely based on commensalism. Obviously, when the host plant enters senescence, all internal fungi have a great advantage over the secondary colonising fungi since the primary rule of

An important group of endophytic fungi, which is clearly beneficial for the plant, consists of mycorrhiza forming symbionts present in the roots of several aquatic macrophytes. Many mycorrhiza forming symbionts belong to a phylum of the "lower fungi" called *Glomeromycota*. Certain orders of the *Glomeromycota* are obligate root symbionts characterized by a vesicular arbuscular mycorrhiza (VAM) that supply their hosts with nutrients. In return, the host plant provides the fungus with sugars rich in energy, amongst other things. VAM fungi were formerly believed to be purely terrestrial, but today it is known that they are particularly important in nutrient poor clear waters. For example, in oligotrophic waters, VAM fungi allow macrophytes to grow under nutrient limiting conditions by supplying the plant with solid-phase bound nutrients (Baar et al., 2011). Freshwater algae, e.g. *Dunaliella* and the autotrophic protozoan *Euglena* can establish a mutual relationship with the fungus *Bispora* or the yeast *Cryptococcus,* respectively (Gimmler, 2001). Moreover, fungi belonging to the *Kickxellomycotina* are endosymbionts of invertebrates, especially of aquatic arthropods and - together with specialised protozoans are summarised under the term trichomycetes (Lichtwardt, 2004; Hibbett et al., 2007).

"first come, first serve" is of major importance for growth and reproductive success.

characterise these fungi as typical r-strategists.

1941; Peach, 1950, 1952, 1954; Sparrow, 1960; Swe et al., 2008).

A cornerstone of fungal lifestyle is parasitism. The life cycle of parasitic fungi is identical to that of saprophytic fungi with one exception: the host cells are still alive. Therefore, it is often impossible to separate opportunistic fungi colonizing senescent hosts from the true parasitic fungi reducing the fitness and in some cases even causing death to their previously healthy hosts. Prominent aquatic parasitic fungi belong to *Chytridiomycota* and *Oomycetes*. The host spectrum of these aquatic fungi is broad and covers every phylum including fungi itself (Sparrow, 1960; Van Donk & Bruning, 1992; Ibelings et al., 2004; Kagami et al., 2007). Encounters with fungi can be fatal to algae, particularly if their defence system is breached by the fungus. The ecological relevance of this negative interaction becomes evident when it is considered that suicide is a common defence mechanism in algae. If this controlled progress, called hypersensitivity, is initiated at the right moment during fungal infection, it results in the successful interruption of the fungal infection cycle, because the parasite's ability to reproduce via spore production is inhibited. Such "behaviour" allegorises a beneficial sanction since it protects the healthy algal population by reducing the abundance of the deadly parasite. However, if unsuccessful the parasite prevails and mass mortality of algae results. This can lead to shifts in the algal community composition.

In rare, but important cases, fungi cause severe damage to larger aquatic organisms. Some fungi, mainly but not exclusively *Oomycetes*, infect fishes or fish eggs (Noga, 1993; Chukanhom & Hatai, 2004) and thereby exert strong population pressure. This is of great importance for aquaculture since it necessitates antifungal treatments, but even in natural systems, fungi have the potential to severely harm the indigenous fish population. *Aphanomyces astaci* (*Oomycetales*) causing the crayfish plague has driven the European crayfish (family *Astacidea*) population to the edge of extinction (Reynolds, 1988). In contrast, *Coelomomyces* (*Blastocladiomycota*) effectively infecting several mosquito species (Sparrow, 1960) has been discussed as a biological control for malaria mosquitoes (Whisler et al., 1975). The most infamous fungal parasite is *Batrachochytrium dendrobatidis* (*Chytridiomycetales*), which contributes to worldwide extinction of several known and unknown amphibian species (Berger et al., 1998; Skerratt et al., 2007). Aquatic plants are also greatly affected by fungal parasites. A recently discovered plant parasite is *Pythium phragmites* (*Oomycetales*), obviously being an important causative agent of reed decline (Nechwatal et al., 2005).

Some human pathogens may also be found amongst the aquatic fungi. Common freshwater yeasts belonging to *Candida* and *Cryptococcus* are both potentially harmful to humans (e.g. *C. albicans* and *C. tropicalis*). These fungi are frequently found along bathing sites (Vogel et al., 2007). Several typical dermatophytes and keratinophylic fungi are transferred via water and can also occur in aquatic ecosystems (Ali-Shtayeh et al., 2002). *Chytridiomycetes* and "Microsporidia", however, are rarely pathogenic and only infect immune-deficient patients. Additionally, black yeasts are on occasion salt-tolerant and thus can cause problems when consuming salt preserved food (Butinar et al., 2005).
