Are All Fungi Everywhere?
While this may seem like a ridiculous question, the subject is actually a source of recent debate in the academic world. Stated more precisely, the argument centers around the degree to which fungi are ubiquitous in suitable habitats. While no one would argue that Boletus edulis should be found growing on your carpet (although I wish it grew on mine), it does seem like Penicillium mold is ubiquitous as far as my bread is concerned. While strictly speaking it is far fetched, yet the idea that fungi are everywhere has a degree of acceptance. Take, for instance, this passage from the text Fungal Biology: Understanding the Fungal Life Style, which states that, “Fungi are virtually everywhere; as a result of their very effective means of reproduction and spore dispersal, fungi are always present when a suitable substrate becomes available.”
The idea that microbes, such as fungi and bacteria, are relatively ubiquitous was first articulated by a Dutch microbiologist, Baas-Becking, who in 1934 hypothesized that, “Everything is everywhere, but, the environment selects.” The belief that the world is awash in an unlimited sea of microbial propagules waiting for a suitable habitat to open up has profound implications for ecology and evolution. And, until quite recently, the Baas-Becking view of the microbial world was accepted without much challenge. However, the support for Baas-Becking was primarily based on morphological observations, which are notoriously poor at separating the vast majority of fungal and bacterial species. It’s easy to see how the mistaken attribution of European names, such as in the case of early Amanita phalloides records in the U.S. (Pringle & Vellinga 2006), could lend weight to the idea of fungal ubiquity. Now, however, the popularization of DNA-based techniques to accurately identify morphologically simple organisms has allowed microbiologists to begin rigorous testing of key predictions of the Baas-Becking theory. Recent research has focused primarily on two predictions. The first and more evolutionary prediction is that microbial organisms should not exhibit the same biogeographical patterns observed in plants and animals. The second, more ecological, prediction is that microbial communities will show very little species turnover at small spatial scales.
Biogeography, the observation of geographical patterns in the distribution of organisms, played a major role in Charles Darwin’s and Alfred Russel Wallace’s discovery of evolution by natural selection. Wallace, for instance, noticed a consistent break point in the similarity of flora and fauna between nearby islands in the Malay archipelago. The line, named after Wallace, is a channel of deep water that marks the boundary between the Sunda and Sahil shelves and is mirrored by the Australasian and Asian biota. Because these land masses were never joined they had separate evolutionary histories and evolved separate biotas. According to the Baas-Becking hypothesis, no barriers exist to microbial dispersal so we should not expect to see such clear geographical patterns of relatedness among microbial species.
So what do molecules tell us about fungi? A recent review of Examples from the kingdom Fungi by Taylor et al. (2006) finds quite conclusively that fungi are not everywhere. They show that for even the most widely recognized fungal morphospecies, such as Schizophyllum commune or Saccharomyces cerevisiae (brewer’s yeast), when analyzed at the molecular level each global morphospecies breaks down into clear patterns of geographically restricted genotypes. In another example, patterns of genetic relatedness among matsutake trace the route they must have followed after evolving in North America and migrating across the Beringian land bridge into Europe and Asia along with their coniferous tree hosts (Chapela & Garbelotto 2004). These examples show quite clearly that, even for species with globally distributed habitats, there are significant barriers to dispersal, which lead to endemism patterns similar to those found for plants and animals.
The second, aforementioned, prediction rests on the idea that if microbes disperse ubiquitously, the distribution of these species should be very even within suitable habitats. And, because microbes are small, almost all of the species within an assemblage should co-occur over very small spatial scales. If this is true, we would expect to find almost all of the species in a community within a very small area, and would discover few if any new species by sampling larger areas. Counting the number of species from smaller to larger areas produces something called a species-area relationship, and the rate at which species increase with area has important implications for the conservation of both biodiversity and ecosystem function. For example, if most fungi are present in very small areas, we shouldn’t worry that destroying large amounts of habitat will reduce fungal diversity. While this idea may sound preposterous, a study by Fenchel and Finlay (2004) found as many morpho-species of protists in a single lake as had been previously described throughout the entire globe.
Two recent studies on fungi, one by Greene et al. (2004) and Peay et al. (2007) attempted to create species-area relationships for fungi using molecular data. Both studies found significant spatial turnover of fungi; however, they differed in the strength of the species-area relationship. Green et al., working with soil ascomycetes, found a species-area relationship lower than that commonly observed for larger organisms. Peay et al. looked at the species richness of ectomycorrhizal fungi on patches of trees that ranged in size from a single tree to over 10,000m2 and found a rate of species increase much closer to that observed for plants and animals. While arguing about which study is more correct is the biological equivalent of counting angels on the head of a pin, taken together these studies show that, even at small scales, fungi do not disperse ubiquitously and can exhibit levels of spatial turnover equivalent to plants and animals.
Both the evolutionary and ecological evidence strongly suggest that fungi may not disperse quite as easily as was previously believed. At larger scales this dispersal limitation leads to genetic diversification and the endemic mycofloras that are beginning to be described across the globe, and at smaller scales to the patchy distributions of fungi that we notice out on forays. Does this mean that fungi aren’t microbes, or does it mean that microbes in general aren’t everywhere? In regards to the former, the jury is out. In many ways fungi are typical microbes—their spores are small (often <10μm) and disperse easily, and their hyphae are also microscopic (<5μm diameter). However, fungal individuals can grow quite large, occupying territories that can be meters in size, and produce fruit bodies that can be gigantic. As for the latter, the weight of the molecular evidence being collected from bacteria, phytoplankton, and protists are also showing the same patterns of biogeographic differentiation and spatial turnover. This suggests that dispersal limitation is important no matter how small you are.
- Baas-Becking LGM. (1934). Geobiologie of inleiding tot de milieukunde. W.P. Van Stockum & Zoon, The Hague, the Netherlands.
- Chapela I, Garbelotto M. (2004). Phylogeography and evolution in matsutake and close allies inferred by analyses of ITS sequences and AFLPs. Mycologia, 96(4) 730–741. (PDF)
- Fenchel, T. & Finlay, B.J. (2004). The ubiquity of small species: patterns of local and global diversity. Bioscience, 54, 777–784. (Abstract)
- Green, J.L., Holmes, A.J., Westoby, M., Oliver, I., Briscoe, D., Dangerfield, M. et al. (2004). Spatial scaling of microbial eukaryote diversity. Nature, 432, 747–750. (PDF)
- Peay KG, Bruns TD, Kennedy PG, Bergemann SE, Garbelotto M. (2007). A strong species–area relationship for eukaryotic soil microbes: island size matters for ectomycorrhizal fungi. Ecology Letters, 10: 470–480. (PDF)
- Pringle, A., E. C. Vellinga. (2006). Last chance to know? Using literature to explore the biogeography of and invasion biology of the death cap mushroom Amanita phalloides. (Vaill. Ex Fr. :Fr) Link. Biological Invasions, 8: 1131–1144. (PDF)
- Taylor, J.W., Turner, E., Townsend, J.P., Dettman, J.R. & Jacobson, D. (2006). Eukaryotic microbes, species recognition and the geographic limitation of species: Examples from the kingdom Fungi. Philos. Trans. R. Soc. B, 361, 1947–1963. (PDF)