4/2/23
The blackest box
Artwork by Graeme Walker
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Hello, my dear readers. Many of you have emailed me asking when the next blog post will be posted, what topics we'll cover next, if that cliffhanger from last season will be resolved, and why I decided to partner with a new publishing company. All of those questions will not be addressed in this post because they are made up. Instead, we will pick up the shovel where we dropped it last — the black box of fine-root ecology — and traverse into an even darker territory, fungal guilds and functional traits.
Fungal guilds
Allow me to formally introduce you to a group who needs no introduction, kingdom Fungi! Fungi can fare without an intro because they're having a moment. Whether they're starring in Netflix documentaries and New York Times articles, or popping up in podcasts and your own back yard — fungi are getting around. If you bend towards the alternative crowd and aren't impressed with fungi's recent hype in popular culture, let me try to dazzle you with numbers instead. A detailed 2021 review covering fungal diversity and conservation estimated that there are currently 6.3 million to 13.2 million fungal species sharing the planet with us (but also see Larson and co's 2017 publication which estimated an astounding 165 million fungal species). Further, if some of you refuse to be numerically charmed, let me overwhelm you with MASS. The trophy for the largest living organism on earth was awarded to a species of honey fungus, Armillaria ostoyae, in 1998. This belowground behemoth covers a landmass equal to 1600 football fields in Oregon's Blue Mountains. Whatever way you tally it, both societally and biologically, fungi are a popular and expansive bunch.
To reach such levels of fame and species diversity demands a high degree of biological innovation. Fungi have evolved to set up shop, find resources, and reproduce in most habitats on Earth. This makes fungi fundamental in both human affairs and ecosystem processes. For example, fungi play pivotal roles in the biosynthesis of important drugs like antibiotics and statins. They also make their way into our food systems (in yummy forms like mushrooms and truffles and breads, and in not-so-yummy forms like the rusts and smuts that can wreak havoc on our crops). Switching gears, if we zoom out and look at things from an ecosystem perspective, fungi perform unique and vital functions in nature by decomposing the Earth's leaf litter, wood, soil organic matter, animals, and even themselves. In addition to decomposition, fungi uptake nutrients and water to utilize for their own growth as well as the growth and health of their various plant and bacterial symbionts. Fungi's roles as decomposers and symbionts therefore have significant effects on global biogeochemical cycles and the composition of plant, bacterial, and animal communities.
From the oyster mushrooms popping out of the growing kit that your aunt gifted you to the Pisolithus helping out their tree hosts in pine plantations, fungi have evolved a creative repertoire of life strategies and adaptations to all kinds of habitats. This makes kingdom Fungi an endlessly fascinating taxa, but also causes researchers to scratch their heads and hold their chins when trying to understand fungal diversity and its impacts on ecosystem processes. To prevent researchers from aggravating their scalps and permanently altering the structure of their mandibles, fungi were assigned to guilds based on the types of resources they use. This began with a Berlin researcher by the name of JHF Link who categorized endophytic fungal species in 1809. From then on, guild classifications were in mycological vogue, and other guilds were described. Below, I will cover the fungi involved in fungi-plant symbioses which include pathogenic, saprotrophic, endophytic, and mycorrhizal fungi (plus a surprise guest, the lichenized fungi, who associate with algae and/or cyanobacteria). Further, we'll cover fungal function traits, with an emphasis on mycorrhizal traits, for all of us with a keen interest in our root-associated friends.
Lexikon Blogion
Kingdom Fungi: one of the six kingdoms of life containing eukaryotic members who move via growth, and absorb nutrients by excreting enzymatic cocktails into their surrounding habitats. Members of kingdom fungi can be unicellular (e.g., yeasts), but most are multicellular and filamentous. To reproduce, fungi produce spores and undergo alternations of generations, which includes a haploid gametophyte stage and a diploid sporophyte stage. Finally, and perhaps most interestingly, fungal cell walls are constructed with a derivative of glucose called chitin (the second most abundant polysaccharide in nature!).
A. ostoyae is a pathogenic fungi that can be found in both hardwood and conifer forests. Photo by Walt Sturgeon.
Fungal guilds:
a grouping system of the kingdom fungi based on their lifestyles and modes of nutrient acquisition. Knowing the guild of a fungus will inform you of what substrates it grows on.
Each colored bar shows the proportion of species within a specific guild across fungal lineages. Figure from Zanne et al. 2020.
Pathogenic fungi
Pathogens are found throughout the fungal family tree, but most of the described species are in the subphylum Dikarya which includes the divisions Ascomycota and Basidiomycota. To be considered as an official pathogen and get your "blue check" on the Department of Agriculture's fungal databases, a fungi must a) infect host tissue, and b) induce disease or damage.
The words "infect," "disease," and "damage," tend to paint a dismal picture, but pathogenic fungi serve as important regulators of biodiversity in our ecosystems. For example, fungal pathogens can prevent the dominance of competitive tree species and increase the biodiversity in some forests. In contrast, the subdivisions Pucciniomycotina (rust fungi) and Ustilaginomycotina (smut fungi) within Basidiomycota tend to love our monocropping systems, so us humans have to find inventive ways of keeping them at bay.
To make a living off of dead and dying host tissue, fungal pathogens utilize a unique suite of enzymes, morphologies, and methods for overcoming host resistance. To describe these different traits and methods, researchers further categorize fungal pathogens into three types: necrotrophs, biotrophs, and hemibiotrophs. As it turns out, most currently described pathogens seem to go the necrotrophic route. This prevalency towards necrotrophy is supported by a strong arsenal of enzymes (e.g., carbohydrate-active enzymes) that break down complex compounds found in plant cell walls.
Ganoderma is a wide-spread fungal genus containing around 80 species of pathogenic-saprotrophic fungi. Some identifiable features include the pores on the underside of their caps (instead of gills), their shelf or bracket-like growth form, and their occurrence on dead or dying trees.
Necrotrophs: fungi that kill host tissue before nutrient absorption. To me, this seems like quite the empathetic approach.
Biotrophs: fungi and bacteria that require living plant tissue to acquire nutrients and reproduce. However, context can alter the status of biotrophic relationships. Some conditions can cause fungal or plant partners to shift their cooperative attitudes towards a more selfish strategy. If things get really bad, some symbioses end in divorce, or even a slanderous tell-all book.
Hemibiotrophs: fungi that function as both biotrophs and necrotrophs, absorbing nutrients from living and dying tissue as their host takes its last breaths. Once their host is officially KO'ed, hemibiotrophs will transition to a necrotrophic arsenal of enzymes and finish up the job (this is an oversimplification for comedic effect, but the process described above is hopefully somewhat correct).
Saprotrophic fungi
Akin to their pathogenic cousins described above, saprotrophic fungi are widely dispersed amongst the fungal family tree. In fact, various unsolved murder cases have been solved by saprotrophs submitting their DNA to companies like 9andMe, which has allowed police to track down pathogenic relatives who've left their DNA at crime scenes. Just kidding, this is all nonsence. However, according to the Evans et al., Agaricus bisporous has 9 chromosomes, so if there was in fact a company mapping fungal ancestry, it's only reasonable that it would be named "9andMe." Anyway, to make it as a saprotroph, one must live a life decomposing wood, leaf litter, soil organic matter, or the necromass of other fungi. Some may not consider this a glorious life, but we'd all be buried without them.
Much like researchers group pathogenic fungi into categories to understand their lifecycles and absorption strategies, saprotrophic fungi are distinguished by the types of substrates they grow on. Substrates like soil, leaf litter, and wood, all contain unique communities of saprotrophs that are able to enzymatically (and in some cases, non-enzymatically) digest their tissues. Soil saprotrophs are found in all major lineages, whereas leaf litter and wood decaying saprotrophs are more closely related and a little more specialized. For example, wood decaying fungi are found in the same popular fungal divisions mentioned above (Ascomycota and Basidiomycota), and categorized based on their rot strategy. White rot fungi can degrade both lignin (i.e., compound in bark) and plant cell walls, whereas brown rot fungi leave the lignin behind. These rot strategies have important implications on how organic materials are cycled through our ecosystems.
The above figure shows the different residues left behind by brown and white rot saprotrophic fungi: a) brown rot residue, b) brown rot fungus Fomitopsis pinicola, c) white rot residue, and d) white rot fungus Fomes fomentarius. Remembering the difference between these two rot strategies can be a little tricky, but if you see brown then you know that lignin was left behind, if you see white, then lignin was decomposed. Figure from Krah et al. 2018.
Endophytic fungi
Remember our friendly biotrophs mentioned above? Well, say hello to perhaps the most widespread fungal biotroph in the game, endophytic fungi! Endophytes are mostly within the Ascomycota division and are found in association with all living land plants. Inside living plant tissues both above- and belowground, endophytes hang around peacefully without causing disease. Other than their location on the fungal family tree, there isn't much else I can confidently share with you about this fungal group. Endophytes are a mysterious bunch, and much about their lifecycles and functions remain unknown.
Holding true with all of the previously covered fungal trophic groups, endophytic fungi are further separated into distinct groups. Rather than grouping based on nutrient absorption strategies or substrate preferences, endophytes are categorized by the way they spread to different hosts. Endophytes can spread vertically by taking a ride on seeds from parent plants, or horizontally by "jumping" to other plants in the surrounding environment. Vertically transmitted endophytes are all within the Clavicipitaceous group and associate with grasses. The horizontally transmitted endophytes, some of which are in the previously mentioned Ascomycota and Basidiomycota divisions, associate with a broad range of angiosperm and gymnosperm species. Both types can facilitate host-plant growth, tolerance to environmental stressors like drought and herbivory, and alter soil community composition.
Figures showing different growth forms of endophytic fungal mycelia between and within plant cells, and the different functional classes of endophytes proposed by Rodriguez et al. 2009. Class 1 includes those Clavicipitacious members that I mentioned earlier, whereas classes 2-4 are all nonclavicipitatious. Classes exhibit various levels of plant colonization, diversity, and benefits to their plant partners. Figure from Kusari and Spiteller 2012.
Lichenized fungi
If you're dying to see fungi in person this very second, go outside to your nearest undisturbed surface (a tree, a rock, the bumper of the car your neighbor has been working on in his driveway for the past 12 years) and feast your eyes on the quiet and confident lichen! Lichenized fungal species are mostly within the Ascomycota division, but they can also be found in Basidiomycota and Glomeromycota. Back in the early days (before the 1860's) lichen were thought to be a singular organism. It wasn't until 1867 that a Swiss botanist named Simon Schwendener made the seemingly outrageous claim that lichen were in fact a symbiosis between fungi and algae/cyanobacteria. Now we know for a fact that when you see that lichen on your neighbor's car bumber, what you are actually seeing is a fungi absorbing water and nutrients from the air and exchanging those resources for sugar from its photosynthetic partner.
Because of the complexities of the lichen symbiosis that can be seen in the figure to the right, further categorization of the fungi in this group is a bit trickier than what we saw in the previous fungal guilds. With that being said, researchers have done a lot of work to examine the morphologies of lichen, what substrates they grow on, and to identify the photobionts (i.e., the algae and cyanobacteria) in the symbiosis. Regarding morphology, microscopic analysis shows unique characteristics of the lichen body, or the thallus. Lichen also vary in color and the structure of their rhizines, which are root-like structures that can attach to trees, rocks, and other surfaces. As far as substrate preferences go, just like our saprotrophs, lichenized fungi can specialize on different substrates and in various microhabitats. To help them adapt to specific substrates and microhabitats, lichenized fungi can associate with distinct photosymbionts that are best adapted to a given environment (Del Campo et al., 2013).
Above I introduced lichen as quiet and confident, and that's because even though they look unassuming, they play extremely important roles in many ecosystems. In some biomes, like alpine and arctic tundras, lichens can be the dominant form of vegetation. They are an important food source for reindeer, caribou, deer, and other smaller mammals. Lichen can also fix nitrogen in low-nutrient habitats and sequester heavy metals in polluted areas.
Lexikon Blogion
Photobionts: the photosynthetic symbiont found in lichen. Photobionts are typically green algae (85%), but can also be cyanobacteria (10%), or an individual lichen can host multiple photobionts (as can be seen in the figure below from Morillas et al. 2022).
Thalli: the vegetative growth, or "body" of the lichen that is formed by the fungal partner. Another figure from Morillas shows the multiple fungal layers that make up the thallus: the upper cortex that protects the photobiont, the medulla and lower cortex that are found underneath the photobiont, and the rhizines, which are described approximately two centimeters below this line of text.
Rhizines: don't let their rhiz fool you, rhizines are not true roots, but instead fungal filaments that are specialized to attach lichens to surfaces. Much like the rhizoids found on mosses and liverworts, our current understanding suggests that rhizines don't perform nutrient or water uptake, but instead serve as anchors growing into substrate.
The figure to the left shows lichen thalli along with different photobiont pairings. Lichens a and b have a single algal layer. Lichen c shows a tripartite symbiosis between fungi, algae, and cyanobacteria. Finally, the lichen in d shows a symbiosis between fungi and cyanobacteria where the cyanobacteria is dispersed throughout the medulla.
Mycorrhizal fungi
We have finally reached my preferred fungal guild, the mycorrhizal fungi. Don't let my bias influence you, all of these guilds are equally important in the functioning of our ecosystems and for the entertainment of odd people like us who enjoy learning about them. Back to the fungi, mycorrhizal fungi are a diverse bunch that can be found in the Ascomycota, Basidiomycota, and Mucoromycota divisions. To further orient you, the ectomycorrhizal fungal type that forms associations with many dominant forest tree species (and produces tasty mushrooms!) are found in Ascomycota and Basidiomycota. Whereas the arbuscular mycorrhizal fungal type that associates with 80% of all vascular land plants are found within Mucoromycota in the subdivisions Glomeromycotina and Mucoromycotina. There are 10+ more types of root-associated fungi, but I will save that topic for another post. Fungi in the mycorrhizal guild make their living by trading nutrients, water, and great conversation, for sugar and a couch to sleep on (i.e., root living space) from their plant symbionts. This symbiotic strategy seems to work well for both partners, and that is one of the reasons why this fungal guild is so diverse.
As I not-so-subtly alluded to above, there are various types of mycorrhizal fungi and these types are distinguished by the species of fungus involved in the symbiosis (i.e., their phylogeny) AND the type of structural interface they form with roots (i.e., their interior or exterior design strategies). Along with the different family crests and architectural tastes that mycorrhizal fungi bring to the table, they also differ among traits, which we'll be covering in a later section of this installment. In the mean time, if you need a refresher on the differences between ecto- and arbuscular mycorrhizal fungi or mycorrhizal nutrient economies, check out these previous blog posts.
The above images show oak roots associated with a variety of mycorrhizal fungal partners. Photo cred goes to Root Lab team members: Claire, who just had a birthday and bakes a great olive oil and lemon cake, and Bill, who is currently reading the tale of a western robber named Black Bart.
Guild shifting: a fungal identity crisis
Before moving on to the topic of functional traits, it's important to let you know that everything you just read about fungal guild categorization is a lie. Just kidding, I would consider it more of a ... not-full truth? The thing is, scientists love to categorize. Categorizing is a pragmatic way to understand the world. In an ecological context, it allows us to understand why organisms and communities respond to certain environmental conditions, disturbances, and other organisms. However, because an unconceivable number of environmental conditions + disturbances + other organisms occur in nature, and because kingdom fungi is so diverse, it's hard to place fungal species into definitive guilds.
For all of the guilds covered above, there are certain environmental contexts and host-related interactions that may encourage a shift in a fungi's occupation. For example, the tranquil co-existence between an endophytic fungi and their host may turn parasitic if the host begins to decline in health because of some other factor. In some cases, something as small as the host no longer laughing at the endophyte's jokes can turn a relationship sour. In line with this heartbreaking tale of scorned roommates, mycorrhizal fungi may also shift towards parasitic relations with their hosts if nutrient conditions change and it's more beneficial to store nutrients or use it for their own growth. If you are interested in learning more about guild flexibility (also referred to as “dual niche” and “multifunctional” fungi) check out Selosse et al.’s 2018 commentary on the subject. The authors do a great job in encouraging mycologists and ecologists to think beyond their specialty fields when researching fungi, and also provide a helpful review of experiments showing the multifunctionality of many fungal taxa.
When narrowing the focus to ectomycorrhizal fungal species, guild assignment can get even trickier. Comparatively, it's much easier to rock a rhyme that's right on time (song reference for all of you people who listen to songs out there). The trickiness arises from the diversity in the ectomycorrhizal fungal group and its evolutionary origins from various saprotrophic lineages (80+). Because of this diversity in species and phylogeny, ectomycorrhizal fungi seem to exist on a biotrophy-saprotrophy continuum where some species maintain more saprotrophic traits from their ancestors and are able to obtain carbohydrates both with- and without a plant host (Koide et al. 2008). The existence of this spectrum doesn't discount the fact that some fungal species, to our knowledge, are purely ectomycorrhizal or purely saprotrophic. However, it opens the door for more nuance, and emphasizes the importance in considering the flexibility in some fungal species' trophic habits.
Fungal functional traits
Similar to what was emphasized in my previous post covering root functional traits, fungal functional traits are important for helping us understand not only fungal biology and ecology, but also their impacts on individual hosts and whole-ecosystem processes. Fungal traits determine what environments fungi are able to inhabit, what substrates or hosts they get their resources from, what unique structures and tissues they produce, and their reproductive strategies. For plant hosts, fungal traits can influence growth, stress tolerance, seedling establishment, and community composition. Finally, fungal traits influence whole ecosystem processes, mostly through the production of mycelia, mineralization and immobilization of soil nutrients, and their impacts on plant community composition and production. Since we gravitate towards roots here in the mysterious underground, below we'll cover some important mycorrhizal functional traits of the two main types (ectomycorrhizal and arbuscular mycorrhizal) that influence fungal communities and ecosystem processes in temperate forests. Sources for images below: 1, 2, 3, and 4.
Exploration typE
Exploration typE
For ectomycorrhizal fungi, genera and species are categorized into exploration types ranging from contact- to long-distance (seen on the left). For arbuscular mycorrhizal fungi, species are grouped based on edaphophilic or rhizophilic habits, which means that some species will grow more extensively into the soil or inside the root, respectively. Exploration types and hyphal growth are important for nutrient uptake, carbon demands on hosts, and soil nutrient cycling.
Enzyme production
Enzyme production
Ectomycorrhizal fungal species are generally known to produce a stronger suite of enzymes than arbuscular mycorrhizal fungi and this allows them to mine the soil for nitrogen and phosphorous in nutrient poor environments. Further, within the ectomycorrhizal fungal group, there are species who have conserved plant cell wall degrading enzymes from their saprotrophic ancestors. These fungi can decompose complex cellulose, hemicellulose, and even some lignin compounds.
Reproductive traits
Reproductive traits
Traits like spore ornamentation (seen to the left), size, abundance, and fruiting body type, size, and abundance, influence fungal dispersal and investment in reproductive tissues. In addition, some mycorrhizal fungi reproduce asexually, produce belowground fruiting structures, or spread vegetatively through hyphae and colonized root tips. These traits are important for understanding mycorrhizal fungal lifecycles, community dynamics, and ecosystem carbon and nitrogen cycles.
melanin content
melanin content
Melanin is a group of complex compounds that is deposited in fungal cell walls. Melanin compounds can increase fungal and host tolerance to environmental stressors such as heat, drought, and mycophagy. The degree of melanization in fungal tissues varies by species (and even individuals), and this variation influences decomposition rates.
phenology
phenology
The seasonality, or phenology, of mycorrhizal fungi influences fungal lifecycles, community dynamics, and functions like the timing of nutrient uptake and transfer to hosts. In regards to fungal lifecycles, we can ask questions about the timing of organ development. For example, in ectomycorrhizal fungi, when are mantles, mycelia, and fruiting bodies produced? We can also ask how the community composition shifts over the course of the year (stay tuned for more on this).
Hurdles and opportunities in constructing a mycorrhizal trait-based framework
Now that we’re all convinced that traits are cool and can tell us stuff, let me catch you up on the exciting challenges faced by the modern mycologist. First, the lessons we can learn from plant and animal trait studies aren’t always translatable to mycorrhizal fungi and other microbial organisms. This discrepancy comes from the cryptic nature of many mycorrhizal fungal species, and traits that are difficult to measure and observe. Next, the fact that mycorrhizal traits are an emergent property arising from two organisms causes variation in trait values and context dependent results. Finally, similar to what was discussed by Selosse and co, bias of researchers coming from different backgrounds creates plant- or fungal-centric views of mycorrhizal systems and can lead to inconsistent definitions of mycorrhizal traits.
Moving forward, one way to address these issues is to describe and study mycorrhizal traits based on location. For example, because mycorrhizal traits emerge from both the fungal and plant species engaged in the symbiosis, fungal mycorrhizal traits, plant mycorrhizal traits, and symbiotic mycorrhizal traits can all be defined and studied. Many important fungal traits were already mentioned above, but plant- and symbiotic mycorrhizal traits can be found in Chaudhary et al. 2022 (see Table 2). Until the time comes for me to bury you with another blog post, check out the below figure from Chaudhary and co. to get a sense of the different categories of mycorrhizal traits.
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