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Biomass, community structure and phosphorus uptake of ectomycorrhizal fungi in response to phosphorus limitation and nitrogen deposition

  • Juan Pablo Almeida
Publishing year: 2019-01
Language: English
Document type: Dissertation
Publisher: Lunds universitet

Abstract english

Popular science summary

Mycorrhizal associations

Mycorrhizal fungi are organisms that live in association with plant roots and provide plants with water and nutrients in exchange for the sugars obtained during photosynthesis. In forested ecosystems mycorrhizal fungi are crucial for tree nutrition and trees rely heavily on these associations to take up key elements like nitrogen and phosphorus. As result, big amounts of the atmospheric CO2 converted in sugars by trees are delivered to the soils to support the fungal partners.
In boreal and temperate forests, nitrogen is present in the soils in forms that are generally not available for tree consumption. Due to the cold conditions in these ecosystems, the cycling of nutrients in the soils is slow and nitrogen accumulates in complex organic molecules (slowly degrading dead plant and animal tissues) with no nutritious value for the trees. However, mycorrhizal fungi have developed different strategies to access the nitrogen locked in such molecules. For that reason, a great amount of carbon is sent to the fungal partners to enhance nitrogen uptake that is in high demand. Indeed, temperate and boreal forests soils are one of the most important reservoirs for carbon in the world.

Mycorrhizal associations, nitrogen deposition and phosphorus demand

Nitrogen pollution caused by human industrial activities deposits from the atmosphere onto forest soils, increases the availability of nitrogen and reduces the need of the trees to maintain the fungal partners. As a consequence, less carbon is delivered to the soils and roots causing a decrease in the growth of mycorrhizal fungi, which might impact ecosystem functioning. A reduction in mycorrhizal biomass can lead to less nitrogen uptake, which will be leached through the soils.
Initially, excess nitrogen favors tree growth, but eventually the trees stop growing because a new nutrient is now in high demand and is required to keep sustaining growth. This nutrient is phosphorus.
Like nitrogen, phosphorus in soils can be present in form of organic molecules. Besides, phosphorus is also found in soil minerals and ores. Mycorrhizal fungi have the ability to release phosphorus from organic molecules and also from ores and minerals. Therefore, when phosphorus tree demand increases in forests, mycorrhizal fungi growth is expected to be stimulated to enhance phosphorus foraging and uptake from the soils.
In this thesis I measured ectomycorrhizal growth in a forest where nitrogen deposition has resulted in high phosphorus demand. Mycorrhizal growth was measured using ingrowth meshbags, which are bags made of a 25 micrometers mesh containing sand. The size of the mesh prevents the growth of the plants fine roots but allows the growth of the fungal filaments (series of attached cells that extend into the soil). This method allows the study of mycorrhizal fungi colonizing the inside of the bags in the search for nutrients. Moreover, I added nutrients rich in nitrogen and phosphorus inside the meshbags to see how nutrient foraging is affected in forests with high P demand. The meshbags were then placed underground in the forest where they were colonized internally by mycorrhizal fungi.
I found that when phosphorus demand increases in the forest, there is also an increase in mycorrhizal growth suggesting that trees rely again on these fungal associations and send carbon belowground to support mycorrhizal fungi and improve phosphorus nutrition. The increase in mycorrhizal growth was significantly enhanced when the meshbags contained either nitrogen or phosphorus rich nutrients. This suggests that higher mycorrhizal growth due to P demand influences nutrient foraging for phosphorus but also for nitrogen. Thus, the increase in mycorrhizal growth can help the ecosystems to retain more nitrogen and prevent leaching. Moreover, enhanced carbon deliver to the soils can increase carbon sequestration, which is important to mitigate CO2 emissions.

Phosphorus demand and mycorrhizal communities

Hundreds of different mycorrhizal species inhabits the forest soils and more than tens of different species are associated with the root system of the same individual tree. These species have different abilities to take up phosphorus from soils and to endure the conditions where the trees allocate less carbon due to high nutrient availability.
In this thesis I also studied how the communities of mycorrhizal fungi species are affected when phosphorus is in high demand. I extracted DNA from soils and meshbags collected in the forest described above. Based on the DNA sequences abundance, I estimated mycorrhizal fungi species abundance and the structure of the mycorrhizal fungal communities. I found that phosphorus demand had a strong effect on mycorrhizal communities and stimulated mycorrhizal species more efficient to release phosphorus from organic molecules and soil minerals.
Boletus badius is one of the species that increased in abundance during phosphorus demand conditions. Previous studies showed that Boletus badius has the ability to take up and storage high amounts of phosphorus from soils. Moreover, it thrives next to phosphorus rich mineral sources especially in high phosphorus demand conditions suggesting that it has the ability to release phosphorus from minerals.
In a laboratory experiment I showed that Paxillus involutus (another species previously reported to thrive under P demand conditions) had the ability to utilize phosphorus from different compounds that form part of the soil phosphorus pool. Furthermore, I demonstrated the elegant chemical mechanisms that this species has to extract phosphorus from soil minerals and ores. It can produce molecules called organic acids that have strong affinity for mineral surfaces and when released they bind the mineral and displace phosphorus, which can be taken up by the fungus. Moreover, Paxillus involutus has the ability to produce molecules that donate electrons to the iron present in certain minerals bound to phosphorus. When iron gains this electrons it gets reduced and phosphorus is released and becomes available for plant and fungi consumption.

In conclusion, mycorrhizal growth in forests is a dynamic process regulated by nitrogen and phosphorus availability. These dynamic processes are very important for carbon delivery and storage in the soils. Mycorrhizal community composition assemblage is also dependent on the nutrient status of the trees, and mycorrhizal species adapted to take up phosphorus from different sources can be important to help trees endure phosphorus deficiency.

High levels of nitrogen (N) deposition might result in a transition from N to phosphorus (P) limitation in high latitude forests. This
could have fundamental consequences for forest production, nutrient acquisition and nutrient leaching.
I studied a Norway spruce forest in a region of high N deposition in southwest Sweden and added N, P or N+P to force the
system to N or P limitation. I studied tree growth and foliar nutrient concentration. Also, using ingrowth meshbags, I followed
ectomycorrhizal (EMF) production, foraging for N and P patches (urea and apatite) and community composition.
I found that tree production was limited by P. Furthermore, P fertilization reduced EMF production indicating that EMF biomass
production was stimulated by P-limiting conditions. Apatite had a positive effect on EMF production when the system was Plimited.
P fertilization reduced foraging for nutrients by EMF, also for N rich urea. P had a stronger effect on the composition of
EMF communities than N, suggesting that P nutrition had a larger impact on belowground carbon (C) allocation than N in this
ecosystem. Furthermore, certain EMF species responded positively to apatite under P limiting conditions, which might have
increased mobilization of P from this source.
To enhance my understanding of P mobilization from different P compounds by EMF, I studied one species, Paxillus involutus,
under more controlled conditions in the laboratory. P. involutus is adapted to high N deposition levels and has a documented
capability to take up P from poorly soluble sources. I found that P. involutus was able to take up P from apatite, P bound to
goethite and from phytic acid. Moreover, I found that iron-reducing activity was produced when these sources were provided
but not when the fungus was provided with soluble P (phosphate). One possible interpretation to this result was that iron (Fe)
reduction is a way for the fungus to prevent that newly liberated phosphate ions are captured by Fe3+ and became unavailable
for uptake.
In conclusion, the high production of EMF found in P-limited forest decline when P is added, probably due to reduced
belowground C allocation when less foraging for P is needed. EMF communities are strongly regulated by P in these forests
and species better adapted for P foraging are probably selected for under these conditions.


Blå hallen, Ekologihuset, Sölvegatan 37, Lund
  • Andrea Polle (Professor)


  • Natural Sciences
  • Biological Sciences
  • Phosphorus and nitrogen limitation, nitrogen deposition, ectomycorrhizal fungi, community composition,apatite, Paxillus involutus
  • Phosphorus and nitrogen limitation, nitrogen deposition, ectomycorrhizal fungi, community composition,apatite, Paxillus involutus


  • Håkan Wallander
  • Nicholas Rosenstock
  • ISBN: 978-91-7753-953-7
  • ISBN: 978-91-7753-952-0
Juan Pablo Almeida
E-mail: juan [dot] almeida [at] biol [dot] lu [dot] se

Doctoral student




Research group

Microbial Ecology




Main supervisor

Håkan Wallander

Assistant supervisor

Nicholas Rosenstock