- Email: [email protected]
Geomycology
f u n g a l b i o l o g y r e v i e w s 2 3 ( 2 0 0 9 ) 9 1 e9 3
journal homepage: www.elsevier.com/locate/fbr
Editorial
Geomycology
“Geomycology” can be defined as “the scientific study of the role of fungi in processes of fundamental importance to geology” (Gadd, 2006, 2007, 2008). This includes past, current and potential future fungal activities and such roles include the alteration and weathering of rocks and minerals, soil formation, the transformation and accumulation of metals, organic matter decomposition, and nutrient and element cycling. In fact, any process by which fungi directly or indirectly affect the physical and chemical characteristics and components of the biosphere could be included. “Geomycology” can be considered to be a subset of “geomicrobiology”, i.e. the roles of microorganisms in geological and geochemical processes, and in a wider sense “geobiology” which includes all biotic influences on the geochemistry of the planet (Konhauser, 2007; Ehrlich and Newman, 2009). Decomposition of organic substances is a primary fungal role in the biosphere and results in major geochemical cycling of elements derived from carbon and energy sources. Apart from their role in carbon cycling, fungi are also clearly involved in other important biogeochemical cycles, including those for N, P, S, and essential and inessential metals (Sterflinger, 2000; Gadd, 2007, 2009). However, a broad appreciation of fungi as agents of biogeochemical change is lacking within geobiology, and apart from obvious connections with the carbon cycle, they are frequently neglected in geomicrobiological and geochemical contexts. Fungi are ubiquitous and important components of rockinhabiting microbial communities and found in a wide range of rock types (e.g. limestone, soapstone, marble, granite, sandstone, andesite, basalt, gneiss, dolerite, amphibolite and quartz) (Sterflinger, 2000; Verrecchia, 2000; Burford et al., 2003; Gorbushina, 2007). In soil and under harsh environmental conditions (e.g. low pH, toxic metal pollution) fungi can often become the dominant group when compared to other microorganisms such as bacteria (Khan and Scullion, 2002; Fomina et al., 2005; Thorn and Lynch, 2007). Fungi are also components of microbial biofilms, on and in rocks, that are believed to be major biotic factors in rock decay, and the formation of patinas, films, varnishes, crusts and stromatolites in rock substrates (Gorbushina and Broughton, 2009). One of the most successful mechanisms that enable fungi to
survive in extreme sub-aerial environments is the formation of mutualistic symbioses with algae and/or cyanobacteria in lichens (Sterflinger, 2000; Haas and Purvis, 2006). In soil, the formation of mutualistic symbioses with plant roots makes mycorrhizal fungi central for plant nutrient uptake in most terrestrial ecosystems (Smith and Read, 1997). These fungi are involved in major mineral transformations and redistributions of inorganic nutrients, e.g. essential metals and phosphate, as well as carbon flow (Landeweert et al., 2001; Finlay and Rosling, 2006; Fomina and Gadd, 2007; Bonneville et al., 2009). A prime fungal attribute that underpins ecological success is their hyphal growth form and associated morphological strategies, and these should be considered key to their environmental roles in mutualistic, pathogenic, explorative and exploitative contexts but also as agents of physical change. The predominantly filamentous branching growth habit has a role in the maintenance of soil structure, with frequent exopolymer production, while biomechanical pressure is exerted by growing fungi in confined locations such as rock fissures. Hyphae and any associated exopolymeric materials can also enmesh soil particles, and release organic metabolites that enhance aggregate stability (Bronick and Lal, 2005). Furthermore, roots and their associated mycorrhizal fungi create local conditions in forest soils that favor bacterial communities with high weathering capacity suggesting the action of biotic consortia in the process of mineral weathering (Uroz et al., 2009). In summary, the biogeochemical importance of fungi is significant in several key areas. These include organic and inorganic transformations, nutrient and element cycling, rock and mineral transformations, bioweathering, mycogenic mineral formation, fungaleclay interactions, and metalefungal interactions. While such transformations can occur in both aquatic and terrestrial habitats, it is in the terrestrial environment that fungi probably have the greatest influence, especially when considering soil, rock and mineral surfaces, and the plant rootesoil interface. Of special significance are the mutualistic symbioses, lichens and mycorrhizas. It is clear that the concept of “geomycology” is appropriate in emphasising many of the major roles of fungi in the
92
biosphere, and the interdisciplinary nature of the topics and mechanisms encompassed under this heading. The combination of physical, chemical, biological and mathematical approaches appears to be integral to future research and understanding. In May 2008, international experts on various aspects of geomycology met at the Swedish University of Agricultural Sciences (SLU) in Uppsala, for a workshop. The aim of the meeting was to discuss fungalemineral interactions in the context of different climatic and ecosystem conditions, and in relation to different temporal and spatial scales. Among the topics discussed were the importance of fungal weathering in soil; factors controlling fungal weathering; separate and combined contributions of fungi and bacteria to weathering; approaches to modelling fungal weathering and issues of scale-up from the level of the fungal tip to the ecosystem. The current issue of Fungal Biology Reviews is largely an outcome of discussions held at this Geomycology Workshop. The significance of fungal weathering at an ecosystem level remains a controversial subject and the two first contributions reflect different critical opinions in this debate. In the first paper, Sverdrup argues that chemical weathering models accurately describe weathering in forest ecosystems and that biological activity is systematically included in the models as tree growth driven mass flow of nutrients. Finlay and coauthors, on the other hand, argue that fungal biogeochemical activity must be explicitly acknowledged in models of forest nutrient availability in order to obtain a fuller understanding of how these ecosystems function and respond to changing conditions. Ultimately the debate reflects different views of the soil ecosystem. While Sverdrup’s model soil is a homogeneous matrix with a soil solution interface where chemical processes control nutrient availability to plants Finlay et al. argue that soil is a heterogeneous matrix in which plant roots, fungi and bacteria control nutrient availability through uptake, release and translocation. Rosenstock reviews weathering as an induced mechanism in fungi and plants. Studies examining carbon partitioning and exudation patterns in response to nutrient-limiting growth conditions are reviewed and future experimental designs to examine induced weathering are discussed. In recent years, our ability to study and understand characteristics of the mineralemicrobial interface have been greatly improved though the development of advanced molecular and microscopy techniques, and the microbeemineral interface is the focus of the two following reviews. Hutchens discusses microbial selectivity with respect to minerals and its implications for weathering processes, while Smits and colleagues discuss micro-analytical techniques in the context of the microbeemineral interface. Mathematical modelling provides an important framework to examine the relevance of experimental data and two articles in this issue cover modelling of fungal weathering at different spatial scales. Smits examines the effects of spatial variations in oxalate concentration in relation to feldspar weathering to simulate local concentration gradients surrounding fungal hyphae. In the final article Rosling and co-authors discuss how available mycelial growth models can be developed to explore the growth and activity of fungal mycelia, including
A. Rosling et al.
those emerging from colonized ectomycorrhizal root tips, in mineral soil substrates. Together the seven articles in this special issue provide an exciting overview of the expansive field of geomycology. Current understanding of fungal weathering at scales ranging from the hyphal tip to ecosystem function is covered and emerging fields such as selective mineral colonization, induced weathering activity and multi-scale modelling are highlighted as future directions for this complex and interdisciplinary field of science.
references
Bonneville, S., Smits, M.M., Brown, A., Harrington, J., Leake, J.R., Brydson, R., Benning, L.G., 2009. Plant-driven fungal weathering: early stages of mineral alteration at the nanometer scale. Geology 37, 615e618. Bronick, C.J., Lal, R., 2005. Soil structure and management: a review. Geoderma 124, 3e22. Burford, E.P., Fomina, M., Gadd, G.M., 2003. Fungal involvement in bioweathering and biotransformation of rocks and minerals. Mineralogical Magazine 67, 1127e1155. Ehrlich, H.L., Newman, D.K., 2009. Geomicrobiology. CRC Press, Boca Raton, FL. Finlay, R.D., Rosling, A., 2006. Integrated nutrient cycles in boreal forest ecosystems e the role of mycorrhizal fungi. In: Gadd, G.M. (ed), Fungi in Biogeochemical Cycles. Cambridge University Press, Cambridge, pp. 28e50. Fomina, M., Burford, E.P., Gadd, G.M., 2005. Toxic metals and fungal communities. In: Dighton, J., White, J.F., Oudemans, P. (eds), The Fungal Community: its Organization and Role in the Ecosystem. CRC Press, Boca Raton, pp. 733e758. Fomina, M., Gadd, G.M., 2007. Metal and mineral transformations: a mycorediation perspective. In: Robson, G.D., van West, P., Gadd, G.M. (eds), Exploitation of Fungi. Cambridge University Press, Cambridge, pp. 236e254. Gadd, G.M. (ed), 2006. Fungi in Biogeochemical Cycles. Cambridge University Press, Cambridge. Gadd, G.M., 2007. Geomycology: biogeochemical transformations of rocks, minerals, metals and radionuclides by fungi, bioweathering and bioremediation. Mycological Research 111, 3e49. Gadd, G.M., 2008. Fungi and their role in the biosphere. In: Jorgensen, S.E., Fath, B. (eds), Encyclopedia of Ecology. Elsevier, Amsterdam, pp. 1709e1717. Gadd, G.M., 2009. Biosorption: critical review of scientific rationale, environmental importance and significance for pollution treatment. Journal of Chemical Technology and Biotechnology 84, 13e28. Gorbushina, A.A., 2007. Life on the rocks. Environmental Microbiology 9, 1613e1631. Gorbushina, A.A., Broughton, W.J., 2009. Atmosphereerock interface: how biological interactions and physical stresses modulate a sophisticated microbial ecosystem. Annual Review of Microbiology 63, 431e450. Haas, J.R., Purvis, O.W., 2006. Lichen biogeochemistry. In: Gadd, G.M. (ed), Fungi in Biogeochemical Cycles. Cambridge University Press, Cambridge, pp. 344e376. Khan, M., Scullion, J., 2002. Effects of metal (Cd, Cu, Ni, Pb or Zn) enrichment of sewage-sludge on soil micro-organisms and their activities. Applied Soil Ecology 20, 145e155. Konhauser, K., 2007. Introduction to Geomicrobiology. Blackwell, Oxford.
Geomycology
Landeweert, R., Hoffland, E., Finlay, R.D., Kuyper, T.W., van Breemen, N., 2001. Linking plants to rocks: ectomycorrhizal fungi mobilize nutrients from minerals. Trends in Ecology and Evolution 16, 248e254. Smith, S.E., Read, D.J., 1997. Mycorrhizal Symbiosis. Academic Press, San Diego. Sterflinger, K., 2000. Fungi as geologic agents. Geomicrobiology Journal 17, 97e124. Thorn, R.G., Lynch, M.D.J., 2007. Fungi and eucaryotic algae. In: Paul, E.A. (ed), Soil Microbiology, Ecology, and Biochemistry. Elsevier, Amsterdam, pp. 145e162. Uroz, S., Calvaruso, C., Turpault, M.-P., Frey-Klett, P., 2009. Mineral weathering by bacteria: ecology, actors and mechanisms. Trends in Microbiology 17, 378e387. Verrecchia, E.P., 2000. Fungi and sediments. In: Riding, R.E., Awramik, S.M. (eds), Microbial Sediments. Springer-Verlag, Berlin, Heidelberg, pp. 69e75.
93
Anna Rosling, Roger D. Finlay* Department of Forest Mycology and Pathology, Uppsala BioCenter, SLU, Box 7026, 750 07 Uppsala, Sweden *Corresponding author. Tel.: þ46 18 67 15 54; fax: þ46 18 67 35 99. E-mail address: [email protected] (R.D. Finlay) Geoffrey M. Gadd Division of Molecular Microbiology, College of Life Sciences, University of Dundee, Dundee DD1 5EH, Scotland, UK 1749-4613/$ e see front matter ª 2010 The British Mycological Society. Published by Elsevier Ltd. All rights reserved. doi:10.1016/j.fbr.2010.03.005
journal homepage: www.elsevier.com/locate/fbr
Editorial
Geomycology
“Geomycology” can be defined as “the scientific study of the role of fungi in processes of fundamental importance to geology” (Gadd, 2006, 2007, 2008). This includes past, current and potential future fungal activities and such roles include the alteration and weathering of rocks and minerals, soil formation, the transformation and accumulation of metals, organic matter decomposition, and nutrient and element cycling. In fact, any process by which fungi directly or indirectly affect the physical and chemical characteristics and components of the biosphere could be included. “Geomycology” can be considered to be a subset of “geomicrobiology”, i.e. the roles of microorganisms in geological and geochemical processes, and in a wider sense “geobiology” which includes all biotic influences on the geochemistry of the planet (Konhauser, 2007; Ehrlich and Newman, 2009). Decomposition of organic substances is a primary fungal role in the biosphere and results in major geochemical cycling of elements derived from carbon and energy sources. Apart from their role in carbon cycling, fungi are also clearly involved in other important biogeochemical cycles, including those for N, P, S, and essential and inessential metals (Sterflinger, 2000; Gadd, 2007, 2009). However, a broad appreciation of fungi as agents of biogeochemical change is lacking within geobiology, and apart from obvious connections with the carbon cycle, they are frequently neglected in geomicrobiological and geochemical contexts. Fungi are ubiquitous and important components of rockinhabiting microbial communities and found in a wide range of rock types (e.g. limestone, soapstone, marble, granite, sandstone, andesite, basalt, gneiss, dolerite, amphibolite and quartz) (Sterflinger, 2000; Verrecchia, 2000; Burford et al., 2003; Gorbushina, 2007). In soil and under harsh environmental conditions (e.g. low pH, toxic metal pollution) fungi can often become the dominant group when compared to other microorganisms such as bacteria (Khan and Scullion, 2002; Fomina et al., 2005; Thorn and Lynch, 2007). Fungi are also components of microbial biofilms, on and in rocks, that are believed to be major biotic factors in rock decay, and the formation of patinas, films, varnishes, crusts and stromatolites in rock substrates (Gorbushina and Broughton, 2009). One of the most successful mechanisms that enable fungi to
survive in extreme sub-aerial environments is the formation of mutualistic symbioses with algae and/or cyanobacteria in lichens (Sterflinger, 2000; Haas and Purvis, 2006). In soil, the formation of mutualistic symbioses with plant roots makes mycorrhizal fungi central for plant nutrient uptake in most terrestrial ecosystems (Smith and Read, 1997). These fungi are involved in major mineral transformations and redistributions of inorganic nutrients, e.g. essential metals and phosphate, as well as carbon flow (Landeweert et al., 2001; Finlay and Rosling, 2006; Fomina and Gadd, 2007; Bonneville et al., 2009). A prime fungal attribute that underpins ecological success is their hyphal growth form and associated morphological strategies, and these should be considered key to their environmental roles in mutualistic, pathogenic, explorative and exploitative contexts but also as agents of physical change. The predominantly filamentous branching growth habit has a role in the maintenance of soil structure, with frequent exopolymer production, while biomechanical pressure is exerted by growing fungi in confined locations such as rock fissures. Hyphae and any associated exopolymeric materials can also enmesh soil particles, and release organic metabolites that enhance aggregate stability (Bronick and Lal, 2005). Furthermore, roots and their associated mycorrhizal fungi create local conditions in forest soils that favor bacterial communities with high weathering capacity suggesting the action of biotic consortia in the process of mineral weathering (Uroz et al., 2009). In summary, the biogeochemical importance of fungi is significant in several key areas. These include organic and inorganic transformations, nutrient and element cycling, rock and mineral transformations, bioweathering, mycogenic mineral formation, fungaleclay interactions, and metalefungal interactions. While such transformations can occur in both aquatic and terrestrial habitats, it is in the terrestrial environment that fungi probably have the greatest influence, especially when considering soil, rock and mineral surfaces, and the plant rootesoil interface. Of special significance are the mutualistic symbioses, lichens and mycorrhizas. It is clear that the concept of “geomycology” is appropriate in emphasising many of the major roles of fungi in the
92
biosphere, and the interdisciplinary nature of the topics and mechanisms encompassed under this heading. The combination of physical, chemical, biological and mathematical approaches appears to be integral to future research and understanding. In May 2008, international experts on various aspects of geomycology met at the Swedish University of Agricultural Sciences (SLU) in Uppsala, for a workshop. The aim of the meeting was to discuss fungalemineral interactions in the context of different climatic and ecosystem conditions, and in relation to different temporal and spatial scales. Among the topics discussed were the importance of fungal weathering in soil; factors controlling fungal weathering; separate and combined contributions of fungi and bacteria to weathering; approaches to modelling fungal weathering and issues of scale-up from the level of the fungal tip to the ecosystem. The current issue of Fungal Biology Reviews is largely an outcome of discussions held at this Geomycology Workshop. The significance of fungal weathering at an ecosystem level remains a controversial subject and the two first contributions reflect different critical opinions in this debate. In the first paper, Sverdrup argues that chemical weathering models accurately describe weathering in forest ecosystems and that biological activity is systematically included in the models as tree growth driven mass flow of nutrients. Finlay and coauthors, on the other hand, argue that fungal biogeochemical activity must be explicitly acknowledged in models of forest nutrient availability in order to obtain a fuller understanding of how these ecosystems function and respond to changing conditions. Ultimately the debate reflects different views of the soil ecosystem. While Sverdrup’s model soil is a homogeneous matrix with a soil solution interface where chemical processes control nutrient availability to plants Finlay et al. argue that soil is a heterogeneous matrix in which plant roots, fungi and bacteria control nutrient availability through uptake, release and translocation. Rosenstock reviews weathering as an induced mechanism in fungi and plants. Studies examining carbon partitioning and exudation patterns in response to nutrient-limiting growth conditions are reviewed and future experimental designs to examine induced weathering are discussed. In recent years, our ability to study and understand characteristics of the mineralemicrobial interface have been greatly improved though the development of advanced molecular and microscopy techniques, and the microbeemineral interface is the focus of the two following reviews. Hutchens discusses microbial selectivity with respect to minerals and its implications for weathering processes, while Smits and colleagues discuss micro-analytical techniques in the context of the microbeemineral interface. Mathematical modelling provides an important framework to examine the relevance of experimental data and two articles in this issue cover modelling of fungal weathering at different spatial scales. Smits examines the effects of spatial variations in oxalate concentration in relation to feldspar weathering to simulate local concentration gradients surrounding fungal hyphae. In the final article Rosling and co-authors discuss how available mycelial growth models can be developed to explore the growth and activity of fungal mycelia, including
A. Rosling et al.
those emerging from colonized ectomycorrhizal root tips, in mineral soil substrates. Together the seven articles in this special issue provide an exciting overview of the expansive field of geomycology. Current understanding of fungal weathering at scales ranging from the hyphal tip to ecosystem function is covered and emerging fields such as selective mineral colonization, induced weathering activity and multi-scale modelling are highlighted as future directions for this complex and interdisciplinary field of science.
references
Bonneville, S., Smits, M.M., Brown, A., Harrington, J., Leake, J.R., Brydson, R., Benning, L.G., 2009. Plant-driven fungal weathering: early stages of mineral alteration at the nanometer scale. Geology 37, 615e618. Bronick, C.J., Lal, R., 2005. Soil structure and management: a review. Geoderma 124, 3e22. Burford, E.P., Fomina, M., Gadd, G.M., 2003. Fungal involvement in bioweathering and biotransformation of rocks and minerals. Mineralogical Magazine 67, 1127e1155. Ehrlich, H.L., Newman, D.K., 2009. Geomicrobiology. CRC Press, Boca Raton, FL. Finlay, R.D., Rosling, A., 2006. Integrated nutrient cycles in boreal forest ecosystems e the role of mycorrhizal fungi. In: Gadd, G.M. (ed), Fungi in Biogeochemical Cycles. Cambridge University Press, Cambridge, pp. 28e50. Fomina, M., Burford, E.P., Gadd, G.M., 2005. Toxic metals and fungal communities. In: Dighton, J., White, J.F., Oudemans, P. (eds), The Fungal Community: its Organization and Role in the Ecosystem. CRC Press, Boca Raton, pp. 733e758. Fomina, M., Gadd, G.M., 2007. Metal and mineral transformations: a mycorediation perspective. In: Robson, G.D., van West, P., Gadd, G.M. (eds), Exploitation of Fungi. Cambridge University Press, Cambridge, pp. 236e254. Gadd, G.M. (ed), 2006. Fungi in Biogeochemical Cycles. Cambridge University Press, Cambridge. Gadd, G.M., 2007. Geomycology: biogeochemical transformations of rocks, minerals, metals and radionuclides by fungi, bioweathering and bioremediation. Mycological Research 111, 3e49. Gadd, G.M., 2008. Fungi and their role in the biosphere. In: Jorgensen, S.E., Fath, B. (eds), Encyclopedia of Ecology. Elsevier, Amsterdam, pp. 1709e1717. Gadd, G.M., 2009. Biosorption: critical review of scientific rationale, environmental importance and significance for pollution treatment. Journal of Chemical Technology and Biotechnology 84, 13e28. Gorbushina, A.A., 2007. Life on the rocks. Environmental Microbiology 9, 1613e1631. Gorbushina, A.A., Broughton, W.J., 2009. Atmosphereerock interface: how biological interactions and physical stresses modulate a sophisticated microbial ecosystem. Annual Review of Microbiology 63, 431e450. Haas, J.R., Purvis, O.W., 2006. Lichen biogeochemistry. In: Gadd, G.M. (ed), Fungi in Biogeochemical Cycles. Cambridge University Press, Cambridge, pp. 344e376. Khan, M., Scullion, J., 2002. Effects of metal (Cd, Cu, Ni, Pb or Zn) enrichment of sewage-sludge on soil micro-organisms and their activities. Applied Soil Ecology 20, 145e155. Konhauser, K., 2007. Introduction to Geomicrobiology. Blackwell, Oxford.
Geomycology
Landeweert, R., Hoffland, E., Finlay, R.D., Kuyper, T.W., van Breemen, N., 2001. Linking plants to rocks: ectomycorrhizal fungi mobilize nutrients from minerals. Trends in Ecology and Evolution 16, 248e254. Smith, S.E., Read, D.J., 1997. Mycorrhizal Symbiosis. Academic Press, San Diego. Sterflinger, K., 2000. Fungi as geologic agents. Geomicrobiology Journal 17, 97e124. Thorn, R.G., Lynch, M.D.J., 2007. Fungi and eucaryotic algae. In: Paul, E.A. (ed), Soil Microbiology, Ecology, and Biochemistry. Elsevier, Amsterdam, pp. 145e162. Uroz, S., Calvaruso, C., Turpault, M.-P., Frey-Klett, P., 2009. Mineral weathering by bacteria: ecology, actors and mechanisms. Trends in Microbiology 17, 378e387. Verrecchia, E.P., 2000. Fungi and sediments. In: Riding, R.E., Awramik, S.M. (eds), Microbial Sediments. Springer-Verlag, Berlin, Heidelberg, pp. 69e75.
93
Anna Rosling, Roger D. Finlay* Department of Forest Mycology and Pathology, Uppsala BioCenter, SLU, Box 7026, 750 07 Uppsala, Sweden *Corresponding author. Tel.: þ46 18 67 15 54; fax: þ46 18 67 35 99. E-mail address: [email protected] (R.D. Finlay) Geoffrey M. Gadd Division of Molecular Microbiology, College of Life Sciences, University of Dundee, Dundee DD1 5EH, Scotland, UK 1749-4613/$ e see front matter ª 2010 The British Mycological Society. Published by Elsevier Ltd. All rights reserved. doi:10.1016/j.fbr.2010.03.005