Unravelling mechanisms of wood decay fungal community change in the post-genomic era
Lead Research Organisation:
CARDIFF UNIVERSITY
Department Name: School of Biosciences
Abstract
About a third of the carbon in the biosphere is in forest ecosystems, mostly in woody plant tissues. Photosynthesis continually adds to this, but in balanced systems a similar amount is broken down to CO2 and H2O, and nutrients are released. The organisms responsible for this decay and cycling are almost exclusively a narrow range of fungi - basidiomycetes and a few ascomycetes. Fungi do not grow in isolation in wood, but form a 3-D mosaic of individuals of the same and different species, which compete with neighbours. Competition leads to community change. Decay rate depends on fungal community composition, climate and the competitive interactions themselves. It is not known how predicted climatic change might influence these interactions and the balance of carbon and nutrient cycling in forests.
Since wood is a solid organic substance, competition for resources is effectively competition for space/territory. Fungi defend and obtain new territory by combative, antagonistic interactions. The overall outcomes are deadlock, where neither species gains headway, or replacement where one species wrests territory from the other, but sometimes partial replacement or mutual replacement. With the complexity of multiple species and environmental conditions, many different antagonistic mechanisms operate. Responses to antagonists include rapid cell division and death, production of pigments, volatile (VOCs) and diffusible organic compounds, and other antimicrobial agents. These responses determine the outcome of interactions, but we do not understand the underlying mechanisms which is crucial for understanding wood decomposition.
Ultimately we want to know how wood decay communities function in natural ecosystems. We will investigate the physiological changes during interactions between species of decay fungi in wood representing the succession from primary coloniser to secondary and tertiary decomposers, under differing environmental conditions. New post-genomic tools allow us to get a complete picture of the genes that are switched on and off during interactions. We will focus on a secondary coloniser Trametes versicolor, and its interaction with another secondary coloniser with which it deadlocks, a primary coloniser that it replaces, and a tertiary coloniser that it is replaced by.
There are 5 main things we want to understand: Firstly, what are the responses of fungal cells during antagonistic confrontation with other mycelia in wood? We will analyse the full complement of transcribed genes, extracellular proteins, VOCs and selected enzymes in the laboratory. Secondly, how are competitive outcomes influenced by environment - temperature, water availability and amount of decay? We will vary conditions and focus on a subset of important genes. Thirdly, are these interaction responses common to wood decay fungi in general? We will interact Trametes versicolor with 15 wood decay species representative of different fungal families and different decay abilities, focusing on a subset of important genes. Fourthly, do responses in the lab reflect the real world? Some of the combinations of fungi paired in wood will be placed on the forest floor, and then changes in expression of important genes measured. Finally, what happens in more complex situations, commonly found in nature, where several wood decay fungi interact with each other simultaneously? We will measure expression of important genes in wood discs colonised with T. versicolor left on the forest floor for 6, 12, 18 and 24 months, allowing natural colonisation from many spores and mycelium in the soil.
This ambitious project uses a logical progression from controlled lab-based experiments to the natural environment using state-of-the-art molecular technologies. It will provide solid foundations for the investigation of complex community-based decay processes, and knowledge to aid the control of timber decay and source novel antimicrobial compounds and other chemicals.
Since wood is a solid organic substance, competition for resources is effectively competition for space/territory. Fungi defend and obtain new territory by combative, antagonistic interactions. The overall outcomes are deadlock, where neither species gains headway, or replacement where one species wrests territory from the other, but sometimes partial replacement or mutual replacement. With the complexity of multiple species and environmental conditions, many different antagonistic mechanisms operate. Responses to antagonists include rapid cell division and death, production of pigments, volatile (VOCs) and diffusible organic compounds, and other antimicrobial agents. These responses determine the outcome of interactions, but we do not understand the underlying mechanisms which is crucial for understanding wood decomposition.
Ultimately we want to know how wood decay communities function in natural ecosystems. We will investigate the physiological changes during interactions between species of decay fungi in wood representing the succession from primary coloniser to secondary and tertiary decomposers, under differing environmental conditions. New post-genomic tools allow us to get a complete picture of the genes that are switched on and off during interactions. We will focus on a secondary coloniser Trametes versicolor, and its interaction with another secondary coloniser with which it deadlocks, a primary coloniser that it replaces, and a tertiary coloniser that it is replaced by.
There are 5 main things we want to understand: Firstly, what are the responses of fungal cells during antagonistic confrontation with other mycelia in wood? We will analyse the full complement of transcribed genes, extracellular proteins, VOCs and selected enzymes in the laboratory. Secondly, how are competitive outcomes influenced by environment - temperature, water availability and amount of decay? We will vary conditions and focus on a subset of important genes. Thirdly, are these interaction responses common to wood decay fungi in general? We will interact Trametes versicolor with 15 wood decay species representative of different fungal families and different decay abilities, focusing on a subset of important genes. Fourthly, do responses in the lab reflect the real world? Some of the combinations of fungi paired in wood will be placed on the forest floor, and then changes in expression of important genes measured. Finally, what happens in more complex situations, commonly found in nature, where several wood decay fungi interact with each other simultaneously? We will measure expression of important genes in wood discs colonised with T. versicolor left on the forest floor for 6, 12, 18 and 24 months, allowing natural colonisation from many spores and mycelium in the soil.
This ambitious project uses a logical progression from controlled lab-based experiments to the natural environment using state-of-the-art molecular technologies. It will provide solid foundations for the investigation of complex community-based decay processes, and knowledge to aid the control of timber decay and source novel antimicrobial compounds and other chemicals.
Planned Impact
The core academic findings of the project will have a direct impact on academic researchers into fungal biology and ecology, forestry science, climate change scientists, practitioners in the timber industry, pharmaceutical and chemical industry, woodland managers, and the general public:
Academic beneficiaries: Detailed data on mechanisms of interspecific mycelial interactions, gene expression, metabolic costs and relation between community structure and decay will be important for fungal biologists, fungal ecologists, decomposition ecologists, systems ecologists and modellers. The effects of changing environmental conditions on interactions and decay will also be of relevance to research predicting the impact of climate change on biogeochemical cycling, particularly of carbon.
The timber industry: Loss of stored timber and timber in service through wood decay is a major source of financial loss. Understanding the underlying mechanisms, will be helpful in the long term in developing new diagnostic approaches and perhaps control measures for timber decay.
The pharmaceutical and chemical industry: This project will investigate biochemical processes in under exploited fungi. Fungi generate a wide range of novel chemicals through metabolic processes or the modification of extracellular substrates. Some compounds are produced in pure cultures, while others are produced in response to competition from other microbes or during decomposition. These compounds include major pharmaceuticals e.g. antibiotics such as penicillin, statins for cholesterol control, and cylosporines to prevent transplant tissue rejection, industrially valuable chemicals, e.g. citric acid, and new technologies, such as lignocellulosic breakdown products for biofuels and phenolics.
Woodland management: Tree pathogens are a major cause of financial loss, therefore their control is important. Understanding antagonistic interactions will give insights into ways of controlling pathogens. In forestry there is also a need to understand the rate of wood decay and hence nutrient release for continued tree growth.
General public: Though most people do not realize it, fungi are central to our lives. As well as being crucial to ecosystem function they have considerable amenity value as part of the woodland biota, some have yielded major pharmaceuticals and others are food sources or used in production of food. Knowledge of basic fungal biology and ecology of wood decay fungi will underpin future uses of the fungi.
Academic beneficiaries: Detailed data on mechanisms of interspecific mycelial interactions, gene expression, metabolic costs and relation between community structure and decay will be important for fungal biologists, fungal ecologists, decomposition ecologists, systems ecologists and modellers. The effects of changing environmental conditions on interactions and decay will also be of relevance to research predicting the impact of climate change on biogeochemical cycling, particularly of carbon.
The timber industry: Loss of stored timber and timber in service through wood decay is a major source of financial loss. Understanding the underlying mechanisms, will be helpful in the long term in developing new diagnostic approaches and perhaps control measures for timber decay.
The pharmaceutical and chemical industry: This project will investigate biochemical processes in under exploited fungi. Fungi generate a wide range of novel chemicals through metabolic processes or the modification of extracellular substrates. Some compounds are produced in pure cultures, while others are produced in response to competition from other microbes or during decomposition. These compounds include major pharmaceuticals e.g. antibiotics such as penicillin, statins for cholesterol control, and cylosporines to prevent transplant tissue rejection, industrially valuable chemicals, e.g. citric acid, and new technologies, such as lignocellulosic breakdown products for biofuels and phenolics.
Woodland management: Tree pathogens are a major cause of financial loss, therefore their control is important. Understanding antagonistic interactions will give insights into ways of controlling pathogens. In forestry there is also a need to understand the rate of wood decay and hence nutrient release for continued tree growth.
General public: Though most people do not realize it, fungi are central to our lives. As well as being crucial to ecosystem function they have considerable amenity value as part of the woodland biota, some have yielded major pharmaceuticals and others are food sources or used in production of food. Knowledge of basic fungal biology and ecology of wood decay fungi will underpin future uses of the fungi.
Organisations
Publications
Hiscox J
(2017)
Threesomes destabilise certain relationships: multispecies interactions between wood decay fungi in natural resources.
in FEMS microbiology ecology
O'Leary J
(2019)
The whiff of decay: Linking volatile production and extracellular enzymes to outcomes of fungal interactions at different temperatures
in Fungal Ecology
Rawlings A
(2021)
Metabolic responses of two pioneer wood decay fungi to diurnally cycling temperature
in Journal of Ecology
Moody SC
(2018)
Interdependence of Primary Metabolism and Xenobiotic Mitigation Characterizes the Proteome of Bjerkandera adusta during Wood Decomposition.
in Applied and environmental microbiology
Johnston SR
(2019)
Highly competitive fungi manipulate bacterial communities in decomposing beech wood (Fagus sylvatica).
in FEMS microbiology ecology
Hiscox J
(2018)
Fungus wars: basidiomycete battles in wood decay.
in Studies in mycology
Boddy L
(2016)
Fungal Ecology: Principles and Mechanisms of Colonization and Competition by Saprotrophic Fungi.
in Microbiology spectrum
Hiscox J
(2017)
Armed and dangerous - Chemical warfare in wood decay communities
in Fungal Biology Reviews
Description | To understand how decomposition processes, fungal community structure and environment are related, we investigated outcome of interspecific interactions and production of enzymes and volatile organic compounds (VOCs) in pair-wise combinations of decay fungi in wood at 15 oC and 25 oC in the laboratory and in a forest, and with wood pre-colonised for different times. Abiotic conditions influenced outcomes of interactions, which were reflected by changes to enzyme activity, and enzyme activity altered throughout the course of interactions reflecting interaction progression and changes to territory occupation. Wood that was pre-colonised for longer prior to interactions decayed most slowly, while temperature had little impact on the rate of decomposition. However, altered temperature did cause changes to individual dominance and the suite and activity of lignocellulose degrading enzymes. A total of 78 metabolites were detected by thermal desorption gas chromatography time of flight mass spectrometry (TD-GC-ToF-MS), and the principal groups of VOCs comprised sesquiterpenes, alkanes and esters. VOC profiles altered as a result of changing temperature, but the extent of decay in wood prior to interactions was found to have a more pronounced effect on VOC production than direct climate variables. Furthermore, the suite of VOCs and abundance of particular compounds altered as a result of antagonism, compared to single species self-pairings. Abiotic conditions clearly mediate metabolic processes, which under predicted climate change conditions are likely to alter the rate of decomposition of dead wood in forest ecosystems. The other major objective of the grant was to provide our partners at Swansea with samples of wood interactions for proteomic and transcriptomic analysis. |
Exploitation Route | This has laid the groundwork for subsequent studies of metabolomics, proteomics and transcriptomics in decomposing wood, by providing reference libraries. |
Sectors | Environment,Manufacturing, including Industrial Biotechology |
Description | Advisor to Woodland Trust |
Geographic Reach | National |
Policy Influence Type | Membership of a guideline committee |
Description | GW4+ PhD |
Amount | £110,000 (GBP) |
Organisation | Natural Environment Research Council |
Sector | Public |
Country | United Kingdom |
Start | 10/2014 |
End | 03/2018 |
Description | BBC Radio 4 Life Scientific 15 November 2016 |
Form Of Engagement Activity | A broadcast e.g. TV/radio/film/podcast (other than news/press) |
Part Of Official Scheme? | No |
Geographic Reach | International |
Primary Audience | Public/other audiences |
Results and Impact | A half hour programme based on my research career, and including work on fungal communities and decay processes in wood. Following the broadcast there was a lot of email interest in a wide range of aspects. |
Year(s) Of Engagement Activity | 2016 |
Description | BBC Radio Shropshire interview on fungi |
Form Of Engagement Activity | A press release, press conference or response to a media enquiry/interview |
Part Of Official Scheme? | No |
Geographic Reach | Regional |
Primary Audience | Media (as a channel to the public) |
Results and Impact | Radio interview |
Year(s) Of Engagement Activity | 2015 |
Description | BBC radio Wales 27 sept 2016 Science Café 'Unknown Wales' |
Form Of Engagement Activity | A talk or presentation |
Part Of Official Scheme? | No |
Geographic Reach | Regional |
Primary Audience | Public/other audiences |
Results and Impact | Explain the role of fungi in ecosystems, including wood decay processes |
Year(s) Of Engagement Activity | 2016 |
Description | BBC2 20 March 2016 World's weirdest events (plants communicating via mycorrhizal mycelium) |
Form Of Engagement Activity | A broadcast e.g. TV/radio/film/podcast (other than news/press) |
Part Of Official Scheme? | No |
Geographic Reach | International |
Primary Audience | Public/other audiences |
Results and Impact | BBC2 20 March 2016 World's weirdest events (plants communicating via mycorrhizal mycelium). Part of a TV documentary. |
Year(s) Of Engagement Activity | 2016 |
Description | Biology Rocks! |
Form Of Engagement Activity | Participation in an open day or visit at my research institution |
Part Of Official Scheme? | No |
Geographic Reach | Local |
Primary Audience | Public/other audiences |
Results and Impact | An information stand, with games and activities for children, was held in the National Museum of Wales as part of the outreach event 'Biology Rocks!'. The event was very busy with hundreds of attendees. The stand was very popular and we handed out lots of leaflets and stickers about fungi. Raising the profile of fungi in the wider community; many people (adults and children alike) were really interested and said they planned to use the material we gave them and attend fungus walks/ forays. |
Year(s) Of Engagement Activity | 2014 |
URL | http://events.cardiff.ac.uk/view/biology-rocks/ |
Description | Biology rocks |
Form Of Engagement Activity | Participation in an activity, workshop or similar |
Part Of Official Scheme? | No |
Geographic Reach | Local |
Primary Audience | Public/other audiences |
Results and Impact | Fungal activity stall for Biology week and UK Fungus day |
Year(s) Of Engagement Activity | 2015 |
Description | Copenhagen University seminar |
Form Of Engagement Activity | A talk or presentation |
Part Of Official Scheme? | No |
Geographic Reach | International |
Primary Audience | Postgraduate students |
Results and Impact | Talk on fungi of the forest floor |
Year(s) Of Engagement Activity | 2016 |
Description | ICF Windsor |
Form Of Engagement Activity | Participation in an activity, workshop or similar |
Part Of Official Scheme? | No |
Geographic Reach | National |
Primary Audience | Professional Practitioners |
Results and Impact | A workshop day of talks and interactive sessions on fungal colonisation of trees to a national group of foresters, to raise awareness of the importance of fungi in their profession. |
Year(s) Of Engagement Activity | 2017 |
Description | June 2016 Soapbox Science Cardiff |
Form Of Engagement Activity | Participation in an activity, workshop or similar |
Part Of Official Scheme? | No |
Geographic Reach | Regional |
Primary Audience | Public/other audiences |
Results and Impact | Soapbox science. Talked in the city centre on a soapbox |
Year(s) Of Engagement Activity | 2016 |
Description | June 2016 Tree Science day Cardiff |
Form Of Engagement Activity | Participation in an activity, workshop or similar |
Part Of Official Scheme? | No |
Geographic Reach | National |
Primary Audience | Professional Practitioners |
Results and Impact | Explaining mechanisms of wood decay to professional arborists |
Year(s) Of Engagement Activity | 2016 |
Description | Mycological Society of America 2014 - presented a talk |
Form Of Engagement Activity | A talk or presentation |
Part Of Official Scheme? | No |
Geographic Reach | International |
Primary Audience | Other academic audiences (collaborators, peers etc.) |
Results and Impact | Spoke at the MSA annual conference 2014 in Michigan to an international audience. Presented our work on priority effects. Useful discussions and potential collaborations |
Year(s) Of Engagement Activity | 2014 |
Description | October 2016 Tree decay Edinburgh Arb Association |
Form Of Engagement Activity | A talk or presentation |
Part Of Official Scheme? | No |
Geographic Reach | Regional |
Primary Audience | Professional Practitioners |
Results and Impact | Explain how trees decay to arborists |
Year(s) Of Engagement Activity | 2016 |
Description | Participation in an open day or visit at my research institution - Biology Rocks 2016! |
Form Of Engagement Activity | Participation in an activity, workshop or similar |
Part Of Official Scheme? | No |
Geographic Reach | Regional |
Primary Audience | Public/other audiences |
Results and Impact | Participation in an open day at the National Museum of Wales - Biology Rocks |
Year(s) Of Engagement Activity | 2016 |
Description | Seminar Birmingham |
Form Of Engagement Activity | A talk or presentation |
Part Of Official Scheme? | No |
Geographic Reach | Local |
Primary Audience | Postgraduate students |
Results and Impact | seminar on "Fungus wars" |
Year(s) Of Engagement Activity | 2016 |
Description | Seminar Universite of California Berkeley |
Form Of Engagement Activity | A talk or presentation |
Part Of Official Scheme? | No |
Geographic Reach | International |
Primary Audience | Postgraduate students |
Results and Impact | Seminar on fungus-fungus interactions, which sparked considerable discussion Possibilities for collaboration |
Year(s) Of Engagement Activity | 2014 |
Description | Seminar University of California Stanford Oct 2014 |
Form Of Engagement Activity | A talk or presentation |
Part Of Official Scheme? | No |
Geographic Reach | International |
Primary Audience | Postgraduate students |
Results and Impact | Seminar on fungus-fungus interactions, which sparked considerable discussion Changed the way in which some people will do their experiments |
Year(s) Of Engagement Activity | 2014 |
Description | Stakeholder talk ISA Washington |
Form Of Engagement Activity | A talk or presentation |
Part Of Official Scheme? | No |
Geographic Reach | International |
Primary Audience | Professional Practitioners |
Results and Impact | A talk on fungal colonisation of trees to an international group of arborists, to raise awareness of the importance of fungi in their profession. The session provoked a long (several hours) and lively discussion session |
Year(s) Of Engagement Activity | 2017 |
Description | Talk to the Miller Institute University of California Berkeley |
Form Of Engagement Activity | A talk or presentation |
Part Of Official Scheme? | No |
Geographic Reach | International |
Primary Audience | Other academic audiences (collaborators, peers etc.) |
Results and Impact | Seminar on fungal mycelia and interactions, to about 30 postdocs and professors from a wide diversity of scientific disciplines, which stimulated a lot of discussion Researchers from other disciplines sought me out at other talks and in the lab. |
Year(s) Of Engagement Activity | 2014 |
Description | Talks and demonstrations in Windsor Great Park |
Form Of Engagement Activity | Participation in an activity, workshop or similar |
Part Of Official Scheme? | No |
Geographic Reach | International |
Primary Audience | Professional Practitioners |
Results and Impact | Talks and demonstrations to arborists and environmsntalistsin Windsor Great Park |
Year(s) Of Engagement Activity | 2015 |
Description | Wood decay day for Arboriculture Association Ashton Court |
Form Of Engagement Activity | Participation in an activity, workshop or similar |
Part Of Official Scheme? | No |
Geographic Reach | Regional |
Primary Audience | Professional Practitioners |
Results and Impact | Talks and demonstration to arborist practitioners |
Year(s) Of Engagement Activity | 2015 |