Review

Fungi in a time of climate change — cause for concern
Untitled Mushroom by Seana Gavin.

Over the last decade, climate change has intensified, leading to altered environmental conditions, pervasively affecting our planet’s ecosystems. Destructive human activities such as large-scale deforestation and pollution that reinforce climate change, have driven many species to the brink of extinction. Animals and plants have been relatively well studied and knowledge about these organisms enable work to conserve them. The less charismatic fungi kingdom, however, has been left out of most climate change studies (Medina, Rodriguez, & Magan, 2015).Relative to the plants and animals, very little is known about the fungi and we may be losing them faster than we are learning about them (Cheek, et al., 2020).

Fungi have long captivated mankind as objects of mystic and supernatural. Before humankind had completely understood fungi and their importance in our world, we already knew to employfungi for various uses. A Neolithic corpse found preserved in glacial ice was found with a pouch carrying tinder fungus (Fomes fomentarius), that was most likely used to make fire (Peintner & Pöder, 2000). The Romans prayed to Robigus, the god of mildew, but were unfortunately not able to stop the fungal disease that led to famine and the decline of the empire (Boyd, 2005). Later in 1928, penicillin, the first antibiotic was accidental discovery from contaminant mould growing on a petri dish (Ligon, 2004). Understanding of these organisms dawned with the invention of the microscope and hence the ability to study the fungi’s microscopic spores and cells. Now, we understand that fungi are a kingdom of their own, under the supergroup Opisthokonta. They are eukaryotes that feed by digesting and absorbing organic matter (osmotrophy) and can reproduce sexually or asexually via spores. Climate change has huge ramifications for our ecosystem, affecting fungi and all organisms alike. It is important to understand how these fungi are affected by climate change and how these organisms can in turn shape the course of climate change.

Fungi are a key component of the tropical forest ecosystem.  Soil fungi communities control significant proportions of the labile nutrient which will otherwise be leeched quickly (Yang & Insam, 1991). Above ground, saprotrophic fungi also play an important role in mineralisation and nutrient cycling. Saprotrophic fungi produce a cocktail of enzymes, capable of breaking down even tough cellulosic material, making easier for other organisms to further breakdown the dead organic material (Baldrian & Valášková, 2008).Even at the atmosphere, fungi leave their mark. In tropical forests, mushrooms from the Basidiomycota phylum catapult basidiospores into the air (Hassett, Fischer, & Money, 2015). In the atmosphere, these spores allow water to accumulate on their surfaces, acting as giant cloud condensation nuclei, creating bigger droplets when smaller ones collide and combine (Hassett, Fischer & Money, 2015; Möhler et al., 2007). Given that these mushrooms depend on rain for the dispersal of their spores in the firstplace, changes in the climate to reduce rainfall could hold back growth of these fungi and worse droughts through a feedback loop (Hassett, Fischer, & Money, 2015). Worryingly, it is unclear how fungi will respond to climate change and how stable and resilient they are to abiotic changes (de Oliveira, et al., 2020).  

Fungi-animal interactions

Fungal symbiosis is not just limited to plants but are extensive in higher organisms as well. Beneficial fungal mutualisms with animals include symbioses inside the digestive systems of invertebrates and vertebrates where the fungi participate in digestion. In ruminants, such fungi may help breakdown fibre (Orpin, 1975; Bauchop, 1981).Fungi also live in our gut where they interact with other gut microfauna to metabolise sugars (Finegold, Attebery and Sutter, 1974; Hallen-Adams, et al.,2015). Gut of invertebrates such as beetles have also been found to contain Ascomycota fungi, supplying digestive enzymes that aid with digestion of plant material (Sung, Marshall, Mchugh, & Blackwell, 2003). More sinister symbioses include Aspergillus sydowii fungus attacking weak corals, causing their tissues to turn purple and die (see Fig. 1) (Smith et al., 1996; Geiser et al., 1998). The chytrid fungus, Batrachochytrium dendrobatidis use amphibians as their host, bursting from their skin during sporulation and is attributed as the main driver of amphibian decline (Bellard, Genovesi, & Jeschke, 2016). Though prevalent and tightly connected to our world and all that inhabit it, fungi have not been given much attention compared to animals and plants. Estimates suggest that there are between 2.2 and 3.8 million species of fungi in the world, which means only six percent of all fungal species have been described (Sheldrake, 2020). Understanding of these extensive fungi-animal relationships is important for the complete understanding of organisms they interact with.

Figure 1. Sea fan coral (Gorgonia ventalina) infected with Aspergillus sydowii, multifocal purple annular lesions are indicative of infection (Source: Ernesto Weil).
Climate change, fungi and ecosystems

Generally, it is still uncertain how fungi will respond to climate change (Cavicchioli, et al., 2019). However, it is certain that more studies are urgently needed to understand and be equipped to mitigate possible threats to and from fungi. Fungal diseases will drastically change ecosystems if left uncontained. Traditionally, infectious diseases have not been noted as a key driver of extinction given that obligate pathogens would normally co-evolve with rather than extirpate the host they depend on for their survival (De Castro & Bolker, 2004; Smith, Sax, & Lafferty, 2006). However, fungal infections can cause mortality rates approaching 100% like in Batrochocytrium dendrobatidis with amphibians, Pseudogymnoascus destructans in bats and Ophiostoma ulmi in elm trees due to the changing ecosystem and climate change (De Castro & Bolker, 2004; Frick, et al., 2015; Garner, et al., 2009).

Climate change can lead to an increase in the emergence of fungal diseases by affecting the distribution of invertebrate vectors or leading to water or temperature stresses on plants, making them more susceptible to infection (Elad & Pertot, 2014). An unusual increase in the frequency of heavy rain would also promote the spread of fungal pathogens (Anderson, et al., 2004). Additionally, plant species grow more rapidly in warmer climates may in turn experience increase incidence of disease, since higher host density allows for increased pathogen transmission (Burdon & Chilvers, 1982). Fungi’s high reproductivity means that all individuals of the host population can be infected before the population numbers are too low to facilitate the spreading (Fischer, et al., 2012). Even if the fungal pathogen does not completely wipe out the host population, it can reduce population numbers severely, making the host population vulnerable to random or Allee effects (Stephens, Sutherland, & Freckleton, 1999). This is made worse by the fungi’s ability to survive outside their host, meaning that the fungi’s growth rate is independent of the host’s population size or density. The fungi can persist as durable spores in the environment oras a free-living saprotroph (Fischer, et al., 2012). In the ocean, Aspergillus fungi growth is also expected to increase with warming waters (Holmquist, Walker, & Stahr, 1983),further threatening the health of coral reefs.  

Fungi can also play a role in accelerating ecosystem changes started by climate change. This is exemplified in a tropical montane cloud forest, where warming has resulted in lifting of the cloud layer (Still, Foster, & Schneider, 1999; Lawton, Nair, Pielke Sr., & Welch, 2001). The warmer temperature means that the richness of soil fungi is likely to increase (Looby & Treseder, 2018). This will lead to an exponential increase in decomposition due to increased fungal activities of certain fungi (Benner, Vitousek, & Ostertag, 2010). Paired with the increased mortality of heat-sensitive flora and fauna, the break-down of organic matter can be expected to change the soil quality and increases oil respiration in the montane forest, releasing carbon in the process. Even in lowland forests, increased temperature can facilitate fungi decomposition of soil carbon (Grieve, Proctor, & Cousins, 1990), turning these ecosystems into a carbon source, thus contributing further to warming and the decline of tropical montane ecosystems.

However, not all about fungi is bad news. The fungi might also have a role to play to keep aboveground carbon where they are. When it comes to soil-living mycorrhizal fungi, their branching filament or hyphae permeate the soil and require carbon in their synthesis. These mycorrhizal fungi could therefore act as carbon sequesters, unlike most other fungi (Treseder & Holden, 2013).  Additionally, mycorrhizal fungi improve plant growth, contributing to the increase in carbon sequestration through increase in plant biomass (Malyan, et al., 2019). However, not enough is known about this phenomenon, and more studies is required to understand howto minimise loss of carbon capture by respiration to improve the carbons sequestration potential of fungi (Malyan, et al., 2019).

Drastic changes in climate may kill plants that are unable to adapt, causing other perturbations within the ecosystem when plant diversity is reduced. Incidences of biotic stress from insect pests and other pathogens could also increase due to climate change (Elad & Pertot, 2014). Fungi can contribute to plant survival since it is known that plants recruit rhizosphere fungi under stress for protection (Yi, Yang, Shim, & Ryu, 2011).These fungi have smaller genomes and generation times relative to the plants (Scott et al., 2019) meaning they are capable of faster evolution than plants and rapid adaptation to climate change (Grandaubert, Dutheil, & Stukenbrock, 2019; Suryanarayanan & Shaanker, 2021). More studies are required before we can understand how the fungi responds and contributes to climate change as a whole.

Climate change, fungi and food

We have seen how fungi can be a friend of humanity but may also pose significant challenges. When it comes to food, mycotoxins or secondary metabolites produced by fungi is of concern. Mycotoxins can be toxic to us when ingested at low concentrations, posing a problem to human health when a toxic mushroom is consumed. Even if toxic mushrooms are avoided, mycotoxins can be ingested when other foods are contaminated by the mycotoxin while growing, post-harvest during storage or during transportation (Baert, et al., 2007). Known mycotoxins include aflatoxins produced by Aspergillus flavus growing on peanuts that could result in liver damage (Hedayati et al., 2007) or patulin produced by Penicillium expansum in contaminated apple juice (Marek, Annamalai, & Venkitanarayanan, 2003). Staple food crops can also be affected by fungal pathogens. Magnaporthe oryzae causes the rice blast disease which destroys 50 million tonnes of rice per annum, and is capable of host switching to wheat, posing a threat to South America’s agriculture industry (Maciel, 2011). The Cavendish banana is also poised to be wiped out by a strain of the Fusarium oxysporum fungus, which had previously wiped-out commercial Gros Michel banana farming (Hung, et al., 2018; Ploetz, 2015). Hence, climate change and the response of fungi to its effects will not only affect natural ecosystems but also agriculture and the livelihood of those who depend on it. Fungal diseases in oil palms and bananas are expected to increase with climate change, as the plants are increasingly stressed by the shifts in abiotic changes (Paterson, Sariah, & Lima, 2013).Philippines’ agriculture is already affected by mycotoxigenic fungi that reduce the quality and quantity of output, and some cases are expected to worsen with climate change (Salvacion, Pangga, & Cumagun, 2015). Stress to the food system due to climate change is going to threaten food security and worsen food inequality.

On the flip side, certain mycorrhizal fungi have also been proposed to bolster the resilience of staple food crops against climate change. Encouraging mutualistic relationships between introduced fungi and crops might confer the crops greater resilience against drought and other stressors such as the increasing salinity of crop fields due to saltwater intrusion into the water table, led by sea level rise (Liu et al.,2016; Yadav et al. 2020).

Opinion: Fungi — friend, or foe?

In facing climate change, the fungi kingdom is a double-edged sword, but it is up to us to employ fungi to help in mitigating or even fighting climate change. However, to be able to employ fungi effectively, we first need to understand them. At present, mycology is still in the dark ages — whatever we know about them is merely the tip of the iceberg.It is estimated that in the region around Singapore, 70% of the macrofungi have yet to be discovered (Lee, et al., 2021). This severe lack of understanding of fungi means that they are left out of climate modelling. It is still unclear how factoring in fungi in climate models will tip the scales. Additionally, it is also unclear how many species we are losing to habitat loss and climate change, some of which might prove to be the silver bullets we greatly need to combat climate change.

The lack of understanding of fungi is scary to me. The more we learn about fungi, the more we realise how they area part of or a symbiotic with so much of life on Earth. Many plants house fungi and have learnt to be dependent on fungi for certain nutrients. Many animals also rely on fungi for their gut health, including us humans. We do not seem to know what the effects of our changing climate will do to these fungi we rely on. The pessimist in me says that the unchecked response of fungi to climate change will accelerate the degradation of our environment beyond our imagination.

To me, climate change is largely a story of failure. It is fascinating that we may just be the only civilisation to predict extensively our own undoing, only to look on, watching it unfurl until our own demise. Our species was quick to celebrate our genius and knowledge or grasp on our environment. Only when science progressed did we understand how ignorant we were and how much damage we have caused. Afterall, the expansion into natural environments and manipulating of nature is spurred by the attitude that we are above nature, and that nature is for the service of man. When it comes to mycology, the amount we do not know is sobering. The relatively recent discovery of the ‘wood wide web’ or the underground fungal network that vastly shapes forest ecosystems is just one of the wake-up calls that mycology presented.The more we know about the systems in our planet, the more complicated we find them to be, and the more we realise we do not know. The severe lack in the knowledge of fungi should prompt us to be humble and realise that we cannot tear ourselves away from nature; we cannot be above the very thing that allows our existence.

Unfortunately, mycology had a shaky start right from the onset of modern biology. Right from when Linnaeus began to classify organisms into either plant or animal groups, fungi were seen as a subset of plants and even a primitive plant. Interest in these misunderstood organisms was low and they remain understudied as zoology and botany took off. Today, we continue to see the effects of the fungi’s dismissal in the early days of modern science. Fungi are rarely in the public conscience when it comes to conservation: the fungi have fallen through the cracks and stayed out of school syllabuses. When mentioned, they are often talked about as a subset of botany even though they are vastly different life forms and play very different roles in their ecosystems. A lack of fungi in education has widespread implications in the way our society views and concerns itself with these organisms, even though the fungi is a kingdom probably larger than all vertebrates and plants put together! Markedly, the logo of United Nation’s Decade on Biodiversity had included only the animals and plants (see Fig. 2), with the fungi unrepresented.Talk on conserving biodiversity cannot just include flora and fauna but should also include the mycota and microbiota. Leaving the fungi out of public awareness would inevitably lead to the lack of funding for mycology research and the stasis of mycology.

When we do talk about fungi in popular media, we often vilify them. The term ‘killer fungus’ is commonly used to describe the chytrid fungus that has damaged the amphibian population, pinning the blame on the fungus that had always persisted naturally in the environment. We often do not acknowledge that the chytrid fungus is only increasingly virulent due to anthropogenic climate change and the spread of it around the world is attributed to humanity’s expansion into the natural environment, introducing it to different parts of the globe through our trades and wars. Fungal pathogens of agriculture are also a part of the natural ecosystem, host switching to the most abundant host in their ecosystems to act as nature’s check and balance. The advent of the destructive monoculture means that there is now an abundance of hosts for the fungi, leading to their proliferation and spread. All these point to the fact that disease causing fungi are not the enemy but are signals that exploitative anthropogenic activities have driven our fragile ecosystem out of balance. Vilifying the fungi is shooting the messenger.

Since 2010, the International Society for Fungal Conservation has existed, in a bid for more nations to be onboard with protecting these important organisms. Singapore has not yet committed to the conservation of fungi. The Herbarium of the Singapore Botanic Gardens has a collection of fungi, but the collection is largely uncurated, with many materials unidentified (Lee S. , 2019). Singaporean mycologists themselves seem to be critically endangered as well. While we move ahead with the conservation and protection of flora and fauna, leaving the mycota unchecked and unprotected may decrease the effectiveness of our conservation efforts, given that the biota within our ecosystems is inextricably linked; any loss of fungi species may have widespread cascading effects on the ecosystem.

No matter how dire the situation appears, I believe we cannot afford to lose hope if we wish to stand a chance to slow down or perhaps, be able to reverse some of the effects of climate change. Singapore can make use of fungi to achieve its sustainability goals. Mushroom farming is a sustainable and relatively low-cost way of producing food. The ability to farm mushrooms indoors and in a scalable manner may be able to helpSingapore in the country’s quest for self-sufficiency and attain the “30 by 30”goal. Fungi may also be used to help restore our natural habitats. Arbuscular fungi may be used in bioremediation of degraded soils and be used for in-vitro culture of endangered plants to boost their success rates (Turnau & Haselwandter, 2002). Research in mycotechnology can help to generate solutions to climate change related problems. Singapore has the potential and resources to be a regional leader in novel and holistic climate change solutions that include fungi in the equation. Moving forward, the fungi cannot be continually left out of local climate change conversations. The understanding of fungi will have to start from schools, where students must be taught about fungi and the role they play in our ecosystem. We as individuals can do our part to be more vocal and include the fungi in climate change conversation, plans and actions. Whether or not the fungi will be our friend or our foe depends on our action (or inaction) towards climate change and our ability to restore balance to our planet’s ecosystems. This daunting task cannot be done without the understanding of the omnipresent fungi.