Fungal and bacterial contributions to decomposition in terrestrial and aquatic ecosystems

Climate change and anthropogenic disturbance in the environment affect the quality of terrestrial carbon and the microbial use of carbon in both terrestrial and aquatic systems. One of the most important unknown factors to C modelling and climate projections studies is the carbon use efficiency of microbial decomposers and the biological feedback of decomposition of organic matter to climate change.
The aim of my PhD project was to understand the ecology of the major microbial decomposers, bacteria and fungi, focusing on their contribution to carbon cycling. In contrast with terrestrial ecosystems, microbial growth rates and respiration have been extensively studied in aquatic ecosystems. I developed growth-based techniques to bridge the knowledge between aquatic and terrestrial microbial ecology, focusing on the microbial contribution to carbon cycling. To achieve this, I used field sites and laboratory microcosms and studied the partitioning of C between growth and respiration (carbon use efficiency) and how that was affected by environmental factors such as pH, fertility and organic matter quality, as well as heavy metals. I further compared microbial decomposition of litter in terrestrial and aquatic systems, and the effects of a labile carbon source of photosynthetic algal origin on the decomposition of litter.

Microorganisms play a key role in breaking down dead organic matter such as wood, branches and leaves, and during this process nutrients are released and made available for uptake by living plants. These microscopic decomposers consist of bacteria and fungi. While bacteria are small single-celled organisms, fungi form long tubular structures called hyphae. Both bacteria and fungi are present in a wide range of environments, such as forest and arable soils, deserts, streams and deep-sea sediments, and in a table spoon of soil billions of bacteria and kilometres of fungal hyphae can be found. In this thesis, I compared the contribution of bacteria and fungi to organic matter decomposition because these two groups have distinct life-styles and respond differently to environmental conditions such as pH, nutrient fertilization, and the quality of available organic matter.
During organic matter decomposition by microbes, a fraction of acquired carbon is used for cell growth, while another fraction is used for cell maintenance - this is often called microbial carbon use efficiency. I am interested in this topic because the amount of carbon devoted to biomass or growth can remain in soil for very long time as dead cells, while the fraction of carbon used for maintenance produces carbon dioxide, which is one of the main gases responsible for changes in the global climate. Carbon dioxide emissions from microbes are six times larger than those from human activities, so it is crucial to study carbon use efficiency and understand what determines how microbes divide carbon between growth and carbon dioxide production. Researchers have suggested that fungi have higher carbon use efficiency than bacteria due to the characteristics of the fungal cells, and therefore when decomposition is dominated by fungi less carbon dioxide is produced and more carbon remains in soil. In this thesis I revised a method that allowed me to measure bacterial and fungal growth in comparable units – units of carbon, and along with carbon dioxide measurements I estimated carbon use efficiency. I studied 9 sites from arctic and temperate regions in Sweden, including forest and agricultural sites which were different in fertility, and fertility is usually associated with high pH and high amounts of fertilizers such as nitrogen. I evaluated the environmental factors that stimulate bacterial and fungal contributions to decomposition and how that affected carbon use efficiency. I found that bacteria contributed more to decomposition than fungi and that resulted in high carbon use efficiency, contrary to what was expected. This was true for sites with low fertility. But each of the 9 sites (forest, agriculture, etc) was divided in fertile and unfertile plots. When I analysed each of these plots I discovered that fertile plots resulted in high carbon use efficiency and high contribution of bacteria. In the laboratory I ran experiments and discovered that carbon use efficiency was still higher when bacteria dominated decomposition in soil at high pH conditions. But when I added nitrogen fertilizer this resulted in decomposition being dominated by fungi which seemed contradictory. However, I think that most likely the presence of different plant communities in each of the sites (arctic forest, agriculture soils, etc) also contributed to the effect of fertility on carbon use efficiency.
I also tested the effect of stress on fungal and bacterial contributions to decomposition and resulting carbon use efficiency in a gradient of long-term heavy metal contamination and discovered that soil fungi are more tolerant to heavy metals than are bacteria. By adding more heavy metals to soils previously unexposed and also to those previously exposed to heavy metal contamination, I found out that that once microorganisms had grown accustomed or tolerant to high heavy metal concentrations, carbon use efficiency was unchanged by more heavy metal contamination, presumably because sensitive groups had been removed and replaced by others with higher tolerance to heavy metals.
The presence of easily available organic compounds such as sugars released by plant roots or algae during photosynthesis can also affect the contribution of fungi and bacteria to decomposition, and can also change the rate of (‘prime’) decomposition of organic matter, often called the Priming Effect. The Priming effect has been extensively studied in soils but it has not been very much explored in aquatic systems. In my thesis, I studied biofilms often found growing on decomposing plant litter in streams where they are exposed to sunlight, and where algae, bacteria and fungi live in close proximity. Even though easily available organic compounds released by photosynthetic algal origin did not increase the microbial decomposition of plant litter, fungi used this extra energy source to remove nutrients from plant litter.
Plant litter decomposition differs in aquatic and terrestrial environments but the specific comparison between system has rarely been made. In my thesis I investigated the roles of bacteria and fungi in plant litter decomposition along a fertility gradient in boreal forest floors and adjacent streams. I concluded that bacteria were similarly active in both streams and soils but that fungi dominated the decomposition processes in streams, a difference that was especially pronounced in low pH sites. The difference in fungal and bacterial dominance of litter decomposition led to distinct chemical changes of plant litter in streams and soils during the course of decomposition.
In summary, my thesis provided a deeper understanding of the fungal and bacterial contributions to decomposition in different systems and environmental conditions, and how that regulates carbon use efficiency.