A Discussion of Lichen Biology (Nash 2008)
Chapter 3: Mycobionts (R. Honegger)
Let’s recall some basics. Within the lichen symbiosis there are two partners with defined roles: the photobiont and the mycobiont. The photobiont is the partner that photosynthesizes light into sugars – these include green algae and/or cyanobacteria (see Chapter 2 reading for more on the different photobionts). The mycobiont is the fungal partner. The mycobiont plays many roles, one of them is that the lichen is named after the mycobiont because its easier than naming the lichen after the photobiont (because photobiont taxonomy is currently more in a state of flux than fungal taxonomy) – it’s all about simplicity, not necessarily about who is the boss, cause that is debatable (see Chapter 2 readings on the photobiont for more information). The mycobiont also plays the role of creating 95% of the lichen body (Kendrick 2001), which lichenologists call the thallus. Now that we’ve covered those initial terms, lets dive into “Chapter 3: The Mycobionts”. This chapter is in Lichen Biology (second edition) edited by Thomas Nash III, and is written by Dr. Rosmarie Honegger a professor of plant biology at the University of Zurich in Switzerland who came up with the idea of the fungi creating a greenhouse for the photobiont.
Scientific literature usually starts with origins. But, before we talk a bit about where lichenized fungi “came from”, lets talk a bit about phylogenetics. Lets think about the tree of life.
According to the current scientific view of evolution, all living creatures that exist today came from one or a perhaps a few very simple organisms that evolved into the organisms we see around us today. Those early life forms create the the trunk of the tree. As we go further up the tree we go towards our present time. The first main branches of the tree make up the different kingdoms of life – The Plant Kingdom, The Fungal Kingdom, the Animal Kingdom, and so forth. Each group of organisms found stemming from one of those main branches is considered a monophyletic group – that means that they all have a common ancestor, they come from the same branch of the tree. So all the fungi in the Fungal Kingdom are considered a monophyletic group because they evolved from a common ancestor. Within the Fungal Kingdom there are two main groups, or phylums, that concern our topic: these are the Ascomycete Phylum which compose more than 99% of all lichen, and the Basidiomycete Phylum which compose less than 1% of all lichenized fungi. Ascomycetes are the morels and your food molds. Basidiomycetes are your gilled mushrooms: the shaggy manes, the matsutake, the crimini, the boletes (yes a porcini’s pores are technically gills because they contain the reproductive feature called basidia instead of the reproductive feature in ascomycetes which are called ascoma). All these fungi are monophyletic when you get down to the main branch of the Fungal Kingdom. When organisms do not all evolve from the same ancestor they are considered a polyphyletic group, meaning the individuals in the group do not share the same ancestor, they do not all come from the same branch of the tree.
The fungi who developed the nutritional strategy of lichenization are polyphyletic. This means that way back in the past, fungi from different parts of the Fungal Kingdom developed the technique of cooperating with a photobiont to create the lichen symbiosis. A similar analogy can be found with humans and the development of agriculture – human communities around the world developed agriculture on their own without having contact between each other to share the idea. This is called convergent evolution.
The Ancestors of Lichenized Fungi
So who are the ancestors of lichenized fungi? You might assume that they all come from fungi that previously were parasitic with plants and decided to become morally redeemed. Or perhaps they were saprobes (consumers of dead stuff) who decided that instead of eating dead algae they would assist the struggling algae to grow in difficult environments. Or maybe they were fungi that were mycorrhizal (a symbiosis between fungi and vascular plant roots) and they decided to branch out and make those cute little green algae part of their harmonious community, too. Well, surprisingly, the lichenized fungi come from all three of those groups. And all those fungi share the same nutritional strategy of working with green algae or cyanobacteria for their existence. And this is quite interesting, for it shows us that even though the common ancestor of fungi had evolved into many very different fungal creatures, many of them created the potential to work in symbiosis with green algae and/or cyanobacteria.
Lichenization as a nutritional strategy for fungi
So is lichenization a pretty common way for fungi to get their nutritional needs met? Yes indeed. About 1 out of every 5 fungal species chooses the lichen mode of obtaining nutrients. But these fungi are not obligate symbionts – this means that these fungi do not have to have a photobiont to physiologically exist. These fungi can grow on their own, in little sterile petri dishes of agar in a lab. But they grow so slowly that researchers believe they would be quickly out competed in the wild, and thus these fungi are considered ecologically obligate symbionts, they need a photobiont if they are to survive in the wild.
But, recent research has shown that the lichenized fungi sometimes evolve to become unlichenized, meaning these fungi decided a long time ago to ditch the lichen symbiosis and eek out a living on their own, without a photobiont. And this research has been groundbreaking. Basically, lichenologist Francois Lutzoni from Duke University did extensive genetic testing of many different lichenized and non-lichenized fungi. What he showed rattled the lichenological world because previously scientists considered the lichen symbiosis to be the “ultimate state” for a lichenized fungi. Ultimate state? Yes, essentially, scientists didn’t think a fungi would want to evolve from the luxury of a lichen symbiosis into a non-lichen strategy of obtaining nutrients. Why this evolution has occurred is still a debate, but the genetic research suggests that many fungi existing today were previously lichenized fungi – for some reason they decided to de-lichenize during their evolution. This reminds me of the primitivist movement and their push to abandon industrial civilization (i.e. Zerzan), but perhaps I’m anthropomorphizing too much.
Lutzoni’s groundbreaking research
Lutzoni’s research (Lutzoni et al. 2001) was also groundbreaking in other ways. Honegger lists what his extensive genetic testing of lichenized fungi indicates: (Nash/Honegger p. 30)
- Lichen evolved much earlier than previously assumed.
- Ascomycetes (which make up the majority of lichen) chose to lichenize much less frequently during their evolution than previously thought. I don’t quite understand the implications of that yet, but I’ll fill you in when I do.
- The lichen symbiosis was lost several times during the evolution of different fungi. This includes the subclass Eurotiomycetidae. One example of a Eurotiomycetidae fungi that you know of is Penicillin, another example is Aspergillus. Both of these fungi were lichen way back in the past, and are now saprobes and/or parasites. They are very successful growing and surviving in the wild, not just successful in sterile petri dishes like their lichenized compadres. And, both of these fungi have chemical compounds that are very strong, and very useful in the field of biotechnology. Could these chemical compounds be an artifact from their ancestral lichen ways?
So, in sum, number three is quite interesting because it does show us that evolution is not definitely linear, there may be backtracking, there is no “ultimate state.”
And number one is quite interesting because, well, whats cooler than old fossils, especially lichen fossils?! Well, unfortunately there are not many lichen fossils out there, so Lutzoni’s research shows us what is difficult to find in the fossil records: that lichen date back to the early days, how early? I’ll have a post on Lutzoni’s research in a couple weeks, so stay tuned!
But what do the fossil records of lichen indicate? Honegger points us to 1) the Doushantuo Formation, approximately 600 million years before present over in Southern China, and 2) the Early Devonion Rhynie chert beds in Scotland approximately 480 million years before present. In both of these locations scientists have found colonies of coccoid cyanobacteria or unicellular algae that have fungal hyphae within their cells and these cells are surrounded by a mucilaginous coating. This type of setup seems odd when compared to our typical macrolichens, but is not so odd when you start looking at some of the less visible lichen. Honegger points to research by Henssen (1963, 1986, 1995) and Budel (1987) which indicates a similar photobiont-mycobiont interface within some genera in the Lichinaceae, and then there are the ascomycetes Epigloea which may be symbiotic with (but at least live with) massive gelatinous colonies of a green algae called Coccomyxa dispar.
And you know whats super cool? That a lichen fossil from the Early Devonian period seems to be from a part of the Fungal Kingdom that no longer lichenizes, or at least, we haven’t yet found an example except for this fossil. But haven’t we already discussed this? No, because the fungi that Lutzoni looked at were from Ascomycetes and Basidiomycetes, which are fungal phylums that both contain lichenized fungi. This particular lichen fossil shows that the fungal Phylum Zygomycota used to have lichenized fungi, but now they don’t (at least there is no evidence of it yet). And what is so cool about the Zygomycota? Well, the zygomycetes are fungi that have… drum roll please… motile spores! Yup, fungi who create spores with little flagellum that push them around! But of course this is all very controversial because no zygomycetes are known to be lichenized today. Check out Taylor et al. 1995 a,b, and 1997).
And you know whats even cooler – that fossil records show really old mycorrhizal symbiosis (the arbuscular kind – i.e. the fungi wraps around the root and up in between the cortical cells of the plant roots, feeding it nutrients in exchange for sugars), check out Taylor et al. 1995a. Today more than 70% of higher plants have arbuscular mycorrhizal symbionts. But, the fossils show that the level of evolution of this mycorrhizal symbiosis “has already reached an astonishing level of morphological and physiological complexity, although the early vascular plants (Rhyniales) were just starting to colonize terrestrial ecosystems” (Nash/Honegger 31). Basically, what this evidence indicates is that complex interactions between fungi and a photobiont partner were already highly evolved and differentiated 480 million years ago when plants started to move onto land! So when did the symbiosis between fungi and photosynthesizing agents actually begin? The evidence is not out on that one yet, so we wait.
So while we wait for the super ancient history of lichens to roll in, there are plenty of younger lichen fossils to be dazzled by, particularly the amazingly beautiful macrolichens. Macrolichens have been found in sedimentary rocks from the Tertiary period, approximately 65-1.5 million years before present, and then there is an impression of a Lobaria thallus that was found in Miocene deposits dating back to 24-12 million years before present. That Lobaria impression was found in the geological remains of what was a humid conifer forest over in Trinity County, California. Check out MacGinitie 1937, and Peterson 2000 for more about that find! And then there are some lichen preserved in amber from back 55-35 million years ago for those found in the Baltics and 20-15 million years ago for those found in the Dominican Republic. Man these lichen have sure been getting around for a long time now.
Cell structure of lichenized fungi vs the other fungi
Is there any difference in the cell structure of a lichenized fungi versus fungi that eats dead leaves, or is a parasite, or is mycorrhizal with plant roots? Nope. As far as current research is concerned, there is no evidence for fundamental difference in the cells of lichenized and non-lichenized fungi. Back in the day scientists thought that only lichenized fungi had cellular organelles called concentric bodies. Concentric bodies are spherical semicrystalline structures that have a shell composed of lots of proteins and electrons and have gas on the inside. These structures are usually found in clusters near the periphery of the cell (i.e. near the cell membrane). Researchers later found out that these concentric bodies are in all sorts of ascomycete fungi, from saprobes to plant pathogens, not just lichenized fungi. And these concentric bodies are also found in all sorts of fungal cells – from the hyphae (which are the explorer and nutrient gathering cells) to the asci (which are the spore bearing surface), to the ascospores themselves (the little rocket ship seed that brings the a new generation into the wild blue yonder). Concentric bodies are not found in all fungi, but are found in fungi that experience periods of wet and dry conditions, so many researchers hypothesize that these organelles help the fungi, or the lichen in our case, to tolerate dry periods.
Honegger also mentions that in some species of Peltigeraceae and Parmeliaceae there exists what is known as a multiperforate septa. Okay, lets dig a bit more into some mycology terms. So, septa are the walls within a hyphal cell. Remember that a hyphal cell are the explorer and nutrient gathering cells (as opposed to the reproduction oriented cells). So within the hyphal cell are some walls that are called septa. These walls perform various functions, and the functions are based upon their design. Some functions of the septa are well accepted by the scientific community, such as the septa offer structural support, blocks loss of cytoplasm and cellular organelles “upstream” if a hyphal section “downstream” is damaged. Functions that are more specific to different types of septa are less understood, including the multiperforate septa which are not as common in the ascomycetes as the Woronin bodies (large septal pores that are blocked by spherical bodies called Woronin bodies that act to “plug the drain.”
What is particulary interesting about the multiperforate septa is that it is not universal in the hyphal cells observed in these particuar lichen. Only some of the medullary hyphae wtihin those particular lichen thalli have multiperforate septa while the other medullary hyphae within that same thallus do not! Does this mean that those particular hyphae are performing different functions than the other hyphae living within the lichen? And are these different hyphae actually appendages of the same individual fungi (like an arm and a leg from your body), or are they actually two different fungi? Because, its important to ask, exactly how many fungal individuals are living within one lichen? Honegger does not address this, but when you have an asci structure (look for those apothecia!) those are the sexual reproductive organs of two different fungi that merged together and made little spore children; and this sexual reproductive feature indicates the presence of two compatible fungi of the same species.
The structures that the mycobiont creates for the photobiont
One of the primary roles that fungi play in the lichen symbiosis is the creation of a structure in which the photobiont lives. We are used to seeing foliose macrolichens, but only one out of every four lichen-forming fungi actually have the physiology to create a three dimensional lichen structure. Honegger lists off the other types of structures formed by other lichenized fungi: these include ensheathed photobiont cells that then form microfilaments, microglobules, or crustose thalli (thalli is the plural of thallus, the body of the lichen) – these tiny lichen are some of the most difficult lichens to identify, and thats a struggle since they make up more than 55% of all lichen. Then about 20% of lichenized fungi create a little bit more of a structured home by forming squamules or placodioid thalli. And then about 25% form foliose or fruticose thalli that have internal stratification – this means that the algae are arranged in a very structured manner, as opposed to more haphazardly in the former two groups.
And how are the photobionts organized within the lichen symbiosis? Honegger explains that they are arranged “similarly to the palisade parenchyma” which is the most photosynthetically active parts in vascular plants (Honegger in Nash 35). Honegger makes a very interesting point that shows a mirror between the relationships between vascular plants and their fungal symbionts – except in this case the roles are reversed in a couple ways. Honegger states:
“In contrast to all other mutualistic symbioses of fungi and photoautotrophs, it is the fungal partner of these morphologically highly evolved lichens that secures adequate illumination and facilitates gas exchange of the photobiont” (Honegger in Nash 36) To learn more about this reversal of some roles see Honegger 1991a and 1992 articles.
Other strategies of lichen-forming fungi and associated fungi
How exactly do parasitic lichen do their thing? Well, parasitic lichen are lichen forming fungi that require their early developmental phase to take place on or within the body of the lichen. The parasitic lichen forming fungus grows over part or all of the host lichen, and takes it’s photobiont to create it’s own lichen. Sometimes the host lichen is completely killed, sometimes not; and in turn, sometimes the parasitic lichen lives its whole life on top of or within the host lichen and is thus considered a parasite, and sometimes it grows out and away from the host lichen, forming its own independent lichen. In this latter instance, this lichen may not necessarily be parasitic lichen, Honegger notes that extensive observations need to be made before such species are recognized as parasites (Honegger in Nash 36).
Honegger gives an example of one parasitic lichen performing what is called “algal switching” after it grows away from the host lichen and forms its own individual lichen: Diploschistes muscorum, a crustose forming parasitic lichen starts its development in the squamules and podetia of Cladonia spp. (the fairy cup lichen). When the D. muscorum is young, its steals the green algae Trebouxia irregularis from the host lichen. But as the D. muscorum lichen gets bigger and grows to be independent of the host, this crustose lichen have been found to have replaced the Trebouxia irregularis with Trebouxia showmanii! And this changing of the photobiont is called “algal switching” (Honegger in Nash 36) and it is not all that common of an occurrence (see Friedl 1987).
Some lichen like to grow on decaying bryophytes (mosses, liverworts, hornworts). Honegger states that there is a large number of crustose lichen who choose bryophytes as their substrate on which to grow. An example is the Buellietum olivaceobrunae in the Arctic, see Kappen 1985. And some lichen choose to grow on living bryophytes and act as a sort of parasite to the mosses by grabbing photobionts from under the cuticle of the mosses’ leaf and stem cells or even within leaf cells (see Dobbeler and Poelt 1981 for more on that) and this is quite interesting for it shows that the mycobiont is actively seeking out photobionts, just as it does within those lichen that perform algal switching.
Foliicolous lichen are lichen that grow on the waxy perennial leaves (i.e. evergreen leaves) of plants in a vast range from the sea to the mountains, but most diversity is found in tropical and subtropical areas. These lichen are of primary interest because they often grow on crop plants like tea, coffee, rubber and chocolate plants, and are sometimes considered pests. But they are also interesting because some of these foliicolous lichen actually live within the leaf and Honegger notes that they are probably likely to benefit from the nutrients of that plant. Are those lichen parasites, or some kind of more mutualistic symbiont? The research evidence is still accumulating, but interestingly the lichenized fungi in foliicolous lichen may be assisting the plant, this is because some of the green algae that grow on the leaves of these crop plants are considered pests – and the mycobiont seems to contain these algae and slow down the growth of these algae on the leaves of the crops.
Lichenological literature often mentions what are called lichenicolous fungi, and this is not to be confused with lichenized fungi. Lichenized fungi are the fungi that play the role of the mycobiont and provide structure, chemical synthesis, and water potential roles (lowering the water potential of the lichen thallus so that water can be pulled in from the air). Lichenicolous fungi are those fungi that gain their nutrition from the lichen – whether that be as parasites (causing death) or as “parasymbionts” or “commensalists” (which cause much less damage and are considered “mild parasites”). Honegger notes that there exists little experimental data for what roles these lichenicolous fungi play in the lichen symbiosis. The mystery gets deeper when you take into account that an estimated 95% of all lichenicolous fungi have a strong host specificity. This indicates that most of the different species of lichenicolous fungi evolved to use a particular species of lichen as their host. What in the world is going on in there exactly? This is all getting quite complex. I could throw in for you Bates et al.’s paper from last year (2011) that would blow your minds even more: there are bacteria that are not photobionts that are living in and on the lichen that are both a) host specific and b) not found in the surrounding soil. The number of possible bionts (symbiotic partners) in the lichen symbiosis is growing from two and now up to a possible of four.
A lichen endophyte is a a fungi that grows within a lichen. Endophytes are a relatively new area of research for many plants (since all plants tested to date have endophytic fungi living symbiotically within their leaves or stems), and this type of research is also starting to grow within the field of lichenology, but it is young. The only lichen endophytes found to date have been found when parts of the lichen thalli were cultured in sterile environments, and another fungi (besides the mycobiont) emerged from a piece of thallus. These lichen endophytes are from different types of fungi, including saprobes, pant pathogens, and endophytes of higher plants. Honegger also notes that many of these fungi have not yet been found anywhere outside of the lichen, they are totally new to science! The implications of this is that these endophytes would be required to grow within the lichen in order to survive, and thus would have evolved to live with that particular species of lichen some number of years ago, again supporting the idea that lichen are an ecosystem, a community of individuals living together in mutualistic harmony. See Farrar 1976c and Seaward 1988 for further discussion on lichens as self contained miniature ecosystems.
So that’s the gist of our mycobionts, their cell structure, a bit on their role as structural agents, and a bit on the different types of fungi that are associated with lichen. Coming up next is a discussion of “Chapter 4: Thallus morphology and anatomy” by B. Budel and C. Scheidegger.
– Nastassja Noell