Chiang Mai Journal of Science

Mini Review: Wetland Associated Fungi in Coastal Freshwater Ecosystems – A Focus on Poales-Dominated Coastal Wetlands in Thailand

1. INTRODUCTION

1.1 Wetlands
     Wetlands are dynamic ecosystems that contain soil, either covered by water or saturated by water. The water level can vary depending on the season, location, and vegetation, as these factors influence soil water availability and the release of nutrients for plant uptake. Water level, quality, and water flow mainly define the inhabitants of these environments [1]. The RAMSAR Convention provides a comprehensive definition, describing wetlands as encompassing marshes, fens, peatlands, and aquatic areas, whether natural or artificial, with water that may be static or flowing, and varying in salinity from freshwater to marine environments [2]. These ecosystems cover approximately 6% of the Earth's total land area and are classified based on water flow patterns, pH, soil characteristics, nutrient availability, and geographic location.
     The RAMSAR Convention recognizes six types of wetlands: Marine, Coastal, Estuarine, Lacustrine, Riverine, and Palustrine (Marshes). Lacustrine wetlands are associated with lakes and are fed with fresh water from a lake and nearby waterways. Riverine wetlands are situated along rivers and the banks of tributaries and are often referred to as floodplains. The water level, nutrient content, and water quality fluctuate with the water level of a nearby river [3]. Marshes show a relatively high-water table, lower peat content than bogs and swamps in riverine environments. Water level in marshes shifts with the season, and vegetation adapts to synchronize with seasonal water table changes [1,2,4]. The coastal freshwater wetlands are ecosystems that comprise a combination of riverine wetlands and marshes, situated in close proximity to the coastline, and are characterized by freshwater conditions [2–4].
     Marine and estuarine wetlands are primarily located along coastal regions and comprise ecosystems such as coastal lagoons, rocky shorelines, mangrove forests, and tidal marshes. [4,5]. These environments span gradients of elevation, from shallow subtidal depths that allow light penetration for photosynthetic organisms at the bottom and benthic plants. Towards the ocean, benthic algae and seagrasses dominate the vegetation but the landward niches are inhabited by organisms that can tolerate adverse environmental conditions such as salinity, water table, and pH fluctuations [6].

1.2 Evolution of Wetland Ecosystems
     Wetland ecosystems host distinct communities of flora and fauna, shaped by interactions between biotic and abiotic factors. Co-evolution between landscape geology and related organisms could be the underlying reason for this close association between wetlands and their resident organisms [7]. Geological and paleoecological evidence suggests that wetlands originated during the mid-Paleozoic era [8].
     The development of wetland types paralleled major events in plant evolution. The origin of vascular plants, such as shrubs in the Emsian age, and large trees in the Eifelian age, which led to the development of marshes and swamps in the mid-Devonian era. They are formed by holding soil particles tightly to develop and enable plant root systems [9]. The late Cretaceous saw the origin of the order Poales. At the end of the Paleogene era, those early monocotyledonous plants diversified into families such as Cyperaceae, Juncaceae, Poaceae, and Typhaceae [10]. The physiology and anatomical features of those families facilitated their colonization of wetland habitats. Towards the end of the Oligocene epoch, marshes and swamps were colonized by grasses and grass-like plants resembling present-day flora [7,8].

1.3 Fungal Colonization of Wetlands
     Fungi may exploit available niches in developing wetlands, which offer nutrient-rich substrates, hosts, and favorable environmental conditions that support their establishment and evolution [11,12]. Fungal spores can reach wetlands through several pathways [13]. Wind disperses lightweight conidia and ascospores across long distances; some have been detected 10 km from their origin, with Fusarium graminearum spores found over 500 m above the Earth’s surface [14,15]. Water also serves as an effective dispersal vector from rivers, tributaries, rain, and ocean tides and transportation of spores into wetland environments. Water protects spores from desiccation, UV radiation, and extreme temperatures [15]. Certain fungi, like Ingoldian species, and marine fungi, have spore morphologies adapted for waterborne dispersal. For instance, Lignicola laevis is widely distributed in marine habitats, likely due to ocean currents aiding its spread [16]. Other taxa related to L. laevis have elaborately branched or appendaged spores, such as Flabellospora verticillata. Thus, fungi from upstream leaf litter or nearby vegetation can travel as propagules and colonize downstream wetlands [17].
     Fungi colonize both living and dead plant material. Wetlands often receive driftwood and herbaceous debris through water currents, supporting fungal thalli or reproductive structures [18]. Dispersal of plant propagules, such as seeds bearing endophytes, mycorrhizal fungi, or pathogens, can introduce fungi from other regions to wetlands [19]. Floating live plants can also transport fungal communities, which may establish in new wetland habitats upon settlement [16]. Animals, including humans, act as fungal dispersal agents. Biodiverse wetlands serve as feeding and breeding grounds for wildlife, and the movement of animals in and out facilitates fungal transfer. Migratory birds, for instance, have been shown to carry fungi like Cladosporium cladosporioides and Alternaria alternata between aquatic environments [20]. Human activities, including agriculture and trade can introduce new organisms to wetlands, some of which may harbor fungi that eventually become established [21].

1.4 Wetlands and Evolution of Fungi
     Fungi evolved alongside plants and wetlands, diversifying as decomposers, symbionts, and pathogens. True fungi with chitinous cell walls originated around 760 million years ago, and molecular clock estimates place the divergence of Ascomycota at 500–650 million years ago [22].
     Aero-aquatic fungi are a significant group in wetlands and aquatic habitats. These saprobes decompose submerged plant litter and produce conidia with adaptations for dispersal through air in freshwater environments. Although polyphyletic, their conidial forms evolved independently across evolutionary distinct lineages in response to aquatic conditions and selection pressures, a case of convergent evolution, as seen in Spirosphaera, Tricladium and Varicosporium [22–26]. Genera like Helicodendron and Pseudaegerita produce both large macroconidia and small microconidia. While microconidia rarely germinate, they are considered the true conidia, whereas macroconidia likely evolved as aquatic propagules [23,24]. The emergence of wetlands created new ecological opportunities, driving fungal adaptations and contributing to the structure and diversity of wetland fungal communities [22,24].

1.5 Wetlands in Thailand
     Thailand, a tropical Asian nation, hosts diverse flora and fauna, with wetlands playing a crucial role in supporting biodiversity and offering economic benefits such as eco-tourism and aquaculture [25]. The country's wetlands, comprising marine wetlands, marshes, estuaries, and mangrove swamps that cover about 36,600 km², or 7.5% of land area [27,28]. Important areas include: Thale Noi Non, Don Hoi Lot, the Mekong River, and coastal zones: Khao Sam Roi Yot and Pran Buri estuary [28]. However, these ecosystems face significant threats from resource overexploitation, including logging, land conversion for shrimp farming, poaching, and unsustainable agriculture, leading to the loss of nearly 2,000 km² of mangroves between 1961 and 1996 [29].
     Preserving and studying Thailand’s wetlands is essential not only for wildlife conservation but also for advancing our understanding of wetland-associated microbial diversity. Focused research on wetland fungi can clarify taxonomic relationships and community structures, contributing to a more comprehensive picture of the region’s microbial ecology.

2. FUNGUS-LIKE TAXA FOUND IN WETLANDS

2.1 Zoosporic Fungi and Chytridiomycota
     Wetlands are ecologically diverse habitats offering a wide range of niches for fungal colonization, supporting nearly all major fungal groups and fungus-like organisms [8]. These include zoosporic fungi (Myxomycota, and Oomycota), as well as higher fungi such as Ascomycota, Glomeromycota, Basidiomycota and Zygomycota which process multicellular organization and lack flagellated propagules [30]. Lichens, though present in wetlands and closely related life form to fungi, are not addressed in this review. [31].
     Zoosporic fungi are characterized by their motile, flagellated zoospores [32]. Chytridiomycota, one of the principal zoosporic fungal phyla along with Oomycota, is considered the oldest lineage of true fungi. Though unicellular, chytrids possess true fungal traits and are globally distributed [33–35]. In wetlands, they function primarily as parasites or saprobes, thriving in challenging conditions and tolerating broad pH ranges [36,37]. Saprobic chytrids have been recorded on decaying plant materials, including submerged wood, algae, and herbaceous tissues [30]. For examples Phlyctochytrium planicorne found to exist on filaments of green algae, and Micromyces sp. reported on shrimp chitin [33].

2.2 Oomycota
     Oomycota resemble true fungi in forming mycelium-like thalli and digesting substrates extracellularly, but they differ significantly in structure and genetics. Their coenocytic hyphae contains diploid nuclei and have cell walls composed of β-glucans and cellulose [38]. Primarily saprophytes and pathogens of plants, animals, and fungi, Oomycota inhabit diverse ecosystems including freshwater, marine, and terrestrial habitats [39]. In Korea, species such as Pythium diclinum, P. heterothallicum, P. inflatum, P. intermedium, and P. oopapillum were isolated from sediments and decaying plant matter in freshwater systems [39]. Studies in the Arctic ocean revealed that Oomycota account for about 6% of the eukaryotic microbial community, with diatom parasites like Olpidiopsis drebesii dominant in saline environments. Additionally, Pythiogeton species have been implicated in the die-back of Phragmites australis [41]. These findings highlight the ecological range and widespread occurrence of Oomycota in aquatic systems, including wetlands.

3. HIGHER FUNGI FOUND IN WETLANDS

3.1 Glomeromycota
     Glomeromycetes are true fungi residing in the rhizosphere, forming endomycorrhizal (Arbuscular Mycorrhizal Fungi: AMF) associations within plant root cells [30,42]. Characterized by aseptate hyphae and large multinucleate spores, they lack observed sexual reproduction and are difficult to culture, making metagenomics the primary approach for study. Although data on AMF in wetlands are limited, their presence underscores their ecological significance [43].
     In Thailand’s coastal freshwater wetlands, Typha species dominate, creating monocultures that influence AMF diversity. Studies on Phragmites australis in wetlands identified Glomus species, especially G. mosseae and G. fasciculatum, as dominant [44]. Coastal wetland conditions, such as flooding and hypoxia, impact AMF community structures. Santillán-Manjarrez et al. [45] reported population decline of AMF under anoxic stress. Meanwhile, Silvani et al. [46] identified 14 AMF species from Glomeraceae and Claroideoglomeraceae in similarly extreme environments using both molecular and morphological approaches. Given the fluctuating hydrology, oxygen limitation, and Poales-dominated vegetation of wetlands in Thailand, AMF in these ecosystems likely exhibit dynamic and stress-adapted population structures, warranting further investigation.

3.2 Yeasts
     Yeasts are a group of unicellular fungi that inhabit various habitats including aquatic ecosystems, including wetlands. Yeast stages are found in both Ascomycota and Basidiomycota. The vegetative cells of most yeasts are obovoid, ellipsoid, or spherical in shape; they are occasionally known to produce pseudohyphae depending on environmental conditions, while Mrakia aquatica forms tetraradiate propagules in nature [46]. Candida albicans, Mrakia aquatica, Papiliotrema laurentii, and Saccharomyces cerevisiae are among the most commonly reported yeast species from freshwater ecosystems, with Saccharomycetales being the most dominant order [25,48–50].
     Yeasts in aquatic ecosystems predominantly propagate asexually via budding, although sexual structures have occasionally been reported in Saccharomyces species [51]. In freshwater environments, yeasts are known to function as decomposers (e.g., Saccharomyces cerevisiae, and Mrakia aquatica), endophytic organisms (e.g., Rhodotorula), and as pathogenic organisms associated with aquatic fauna such as Candida species, Debaryomyces hansenii, and Metschnikowia bicuspidata) [49,52,53]. Although most yeast studies in freshwater environments have focused on sediments and aquatic fauna, in-depth taxonomic investigations of yeasts associated with freshwater wetlands remain limited. Therefore, a polyphasic taxonomic approach is recommended to better understand the yeast diversity in these habitats.

3.3 Ascomycota
     Ascomycota is the most abundant and diverse fungal phylum that showcase cosmopolitan distribution across ecosystems. A large proportion of fungi in wetlands are occupied by this group, and function as saprobes, endophytes, and pathogens in these environments. They are well-studied due to their ecological significance and their reproductive strategies including producing either asci-bearing sexual morphs or conidial asexual morphs, and the contribution to maintain ecosystem balance [25,30].
     Four major Ascomycota classes are commonly associated with plants and plant-derived substrates in aquatic habitats include Dothideomycetes, Eurotiomycetes, Leotiomycetes, and Sordariomycetes [49]. Dothideomycetes, the largest class, are defined by their diverse ascomata and bitunicate asci with fissitunicate dehiscence. Sordariomycetes, the second largest, are characterized by perithecial ascomata and inoperculate unitunicate asci. Eurotiomycetes are mostly represented by asexual forms, with cleistothecial ascomata and primitive asci reported in their sexual morphs. Leotiomycetes produce apothecial or cleistothecial ascomata. These classes are well represented in aquatic environments, including wetlands, and are frequently associated with Poales vegetation (Figure 1) [50,54–57].