A roadmap to understanding diversity and function of coral reef-associated fungi

Abstract

Tropical coral reefs are hotspots of marine productivity, owing to the association of reef-building corals with endosymbiotic algae and metabolically diverse bacterial communities. However, the functional importance of fungi, well-known for their contribution to shaping terrestrial ecosystems and global nutrient cycles, remains underexplored on coral reefs. We here conceptualize how fungal functional traits may have facilitated the spread, diversification, and ecological adaptation of marine fungi on coral reefs. We propose that functions of reef-associated fungi may be diverse and go beyond their hitherto described roles of pathogens and bioeroders, including but not limited to reef-scale biogeochemical cycles and the structuring of coral-associated and environmental microbiomes via chemical mediation. Recent technological and conceptual advances will allow the elucidation of the physiological, ecological, and chemical contributions of understudied marine fungi to coral holobiont and reef ecosystem functioning and health and may help provide an outlook for reef management actions.

Keywords: chemical mediation; ecosystem functioning; interkingdom interactions; marine fungi; nutrient cycling; probiotics.

Figure 1.

Potential microhabitats of fungi on coral reefs. Marine fungi likely inhabit diverse microhabitats on coral reefs, such as substrates (rock, rubble, and interstitial spaces in sediments) and biofilms that have formed on reef substrates (Sampaio et al. 2007), but also the water column, where fungi may be predominantly associated with particles or planktonic organisms (Wurzbacher et al. 2010). Mucosal spaces of reef invertebrates, in particular Cnidaria, but also vertebrates such as fish could potentially attract fungi (Reisert and Fuller , Fischer et al. , Nelson et al. 2013). Furthermore, any animal epithelial or macrophyte surface (e.g. seagrasses and macroalgae) may harbor fungal communities (Kagami et al. , Ettinger and Eisen 2019). Aside from surface colonization, endolithic fungi have been reported from calcium carbonate skeletons of corals and the reef framework (Risk and Muller , Priess et al. 2000). Finally, fungi may be associated with the tissues or cells of macro-organisms (Nadal et al. , Trofa et al. 2008). The center represents different stages and/or forms of fungal cells. The outer circles represent potential microhabitats of fungi on the coral reef.

Figure 2.

Overview of fungal diversity studies in corals. (A) Geographic distribution of sampling sites and investigated coral genera (created using maps package in R). (B) Pruned phylogenetic trees displaying consistently reported fungal phyla (and classes for Ascomycetes and Basidiomycetes) across studies (NCBI taxonomy; generated using phyloT v2, Letunic 2015).

Figure 3.

Established and proposed holobiont–fungal interactions in reef-building corals. Corals are complex holobionts comprised of distinct functional compartments: the tissues (gastrodermis and ectodermis), algal endosymbionts (Symbiodiniaceae; localized in host gastrodermal cells), and the skeleton, which harbors a diverse microbiome including the filamentous alga Ostreobium. Under unperturbed conditions (left panel), coral tissues receive large amounts of organic carbon (C_org) from Symbiodiniaceae (1). Endolithic fungi coreside with the filamentous algae Ostreobium inside the coral skeleton where they form visible banding patterns (2). Endolithic fungi may “attack” Ostreobium cells but are unable to penetrate healthy host tissues, which form skeletal protuberances around fungal hyphae (Bentis et al. 2000) (3). Endolithic fungi may perform organic matter remineralization and mineral weathering, resulting in high inorganic nutrient concentrations in skeletal pore water (Risk and Muller 1983) (3). Under environmental stress (right panel), coral tissues experience a disruption of algal endosymbiont C_org translocation and subsequently expel Symbiodiniaceae, resulting in tissue paling (“coral bleaching”), altered holobiont nutrient cycling, and impaired host immunity (Rädecker et al. 2021) (4). Coral bleaching results in transparent host tissues and allows more light to penetrate into the skeleton (5), resulting in blooms of endolithic phototrophs and C_org translocation from the endoliths to the coral tissues (Fine and Loya 2002) (6). Environmental stress may increase diversity and proliferation of coral-associated fungi (Vega Thurber et al. ; Amend et al. 2012) (6), and increased skeletal erosion (Yarden et al. 2007). Thermal stress and weakening of host immune responses may result in opportunistic growth and saprobic activity of coral-associated fungi, which may be accompanied by fungal lifestyle switching (7). In a severely immunocompromised host, fungal infection of tissues and remaining algal endosymbionts may exacerbate holobiont health (Strake et al. 1988), leading to host mortality (Alker et al. 2001) (8). Arrows without dash represent established fluxes, dashed arrows represent hypothesized fluxes. Blue fluxes refer to hypothesized C_org fluxes to fungi. Black text refers to established activity and interactions. Red text refers to proposed interactions. Blue dashed arrows refer to the proposed diverting of C_org to fungi.

Figure 4.

Synthesis of known (black arrows) and proposed (red arrows) interactions and functions of fungi associated with the coral holobiont and the coral reef ecosystem. The most obvious and best-studied fungal interactions on coral reefs include putative parasitism, pathogenesis, and bioerosion. Based on fungal functions in terrestrial and other aquatic ecosystems, we propose that reef-associated fungi may further play roles in the structuring of holobiont- and reef-associated microbial communities and biogeochemical cycling.

Figure 5.

Schematic summary of key research questions and topics to improve our understanding of fungal communities and roles in coral reefs ecosystems ranked by spatial scales and biological complexity.