More than the primary decomposers: microbiome predators as emerging catalysers of decomposition

The soil microbiome (bacteria and fungi) are key determinants of the global carbon cycle, with abiotic factors known to affect microbial decomposition. Here we show that also predation by protists profoundly INCREASES microbial decomposition, a recently unknown process that warrants attention!
Published in Microbiology

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Life on Earth is changing. Wherever you are, you have seen a change in the last years: climate is becoming more extreme, droughts and storms are increasing, temperature is warming, just to name a few. These anthropogenic changes are mainly associated to increased levels of greenhouse gases, most known being CO2. The increased carbon levels in the atmosphere are caused by deforestation and therefore reduced carbon fixation potential and even more emissions from fossil fuels. Strikingly, however, by far most carbon is emitted through microbial respiration in soils: a process called decomposition.

Microbial decomposers are mainly bacteria and fungi. Those organisms contain, with the exception of plants, by far most biotically bound carbon (Bar-On et al., 2018). The biodiversity of these microbes has created at least some taxa that can virtually use all carbon sources— from plant litter to oil to complex plastics! As such, plant litter consists of rather simple carbon compounds with many different microbes being able to use this resource as food. These microbes are, however, not alone. They interact with another and are preyed upon by larger soil organisms. Thereby nutrients move up the food web up to larger animals as well as recycle for plant uptake. Among the first predators of the microbiome are protists.

Protists are, like bacteria and fungi, microorganisms. Protists are functionally diverse with many being photosynthetic (all eukaryotic algae including the vast amount of those organisms that fix 50% of Earth´s carbon in the sea), many are parasites, plant pathogens and so forth (Geisen et al., 2018). The key functional importance of protists in soils is their role as microbiome predators. Through the above-mentioned release of nutrients, they not only provide larger animals with food, but also release nutrients that benefit plant growth. Protists feed also selectively on microbiome taxa, such as on less active ones and those that are “more digestible” (often producing fewer secondary metabolites). The question remains, could there even be a link between protist predation and other microbial-induced processes such as decomposition?

To address this question, we needed some synergy. I teamed up with Ciska Veen to merge expertise on microbes especially protists (Stefan) with microbial decomposition (Ciska). We always wanted to perform a study together and this became feasible when Shunran Hu came in to ask for a master thesis project. Thomas Edison dela Cruz from the Philippines visited me for a research stay and brought in the expertise and culture on the model protist Physarum polycephalum (see Fig. 1)– the team was complete! With a joint effort we performed a straight-forward and rather simple experiment. In short, we added a mix of microbes (a total of 16 microbes, half bacterial and half fungal species that were kindly provided by Paolina Garbeva and Freddy ten Hooven) to sterile litter in glass tubes and added Physarum to half of the containers. Half we incubated at 17 and the other half at 21 °C to further check if temperature affects potential changes in microbial decomposition in presence of predators.

Fig. 1. Physarum polycephalum- a special model protist. thanks to Maries Elemans for the nice pictures of these super small organisms!

What we found was striking: litter decomposition was stimulated by up to 50 % at 17 °C in in presence of protists! Interestingly, decomposition rate with protists was not significantly increased at 21 °C. To evaluate potential underlying mechanism, we performed some interaction assays and found that protists were interacting in different ways with the microbes. In fact, protist growth was actually nearly entirely stopped in presence of some microbes suggesting that those species that actually are efficient decomposer benefit from reduced competition. Many other mechanisms than differential interactions between the protist and the microbiome that remain to be explored might underlie the observed changes in decomposition, such as increased microbial activity and changes in enzyme production (potentially as a response to fight-off predators but also help in decomposition).

What can we deduce from this experiment that we just published in The ISME Journal: Microbial decomposition is not only controlled by differences in abiotic properties such as the well-known factors of temperature or water content (just imagine the slow decomposition rate in the tundra that safes our planet from access CO2 release), but also by biotic factors, in this case predation! Of course, our experiment is super simplistic and rather artificial, as natural systems contain plenty more microorganisms, protists and other organisms under more abiotic variation than explored here. Still, our experiment suggests that microbiome predation is a major driving factor of decomposition especially in cold or temperate places where the bottom-up abiotic factors that stimulate decomposition are less strong (Fig. 2).

Fig. 2. Conceptual model showing that microbiome predators, such as protists, increase litter decomposition through catalyzing microbial processes- especially when abiotic parameters are less dominant.

Therefore, microbiome predation needs to be studied in natural systems to determine its relative importance: it could well be that a substantial amount of litter on Earth, and therefore greenhouse gas emissions are induced by microbiome predation! To be continued! Personally, this project shows once again that collaborations between people with different expertise and cultural background (4 people from 4 countries) is not only fun but also can lead to new knowledge!

Read more about this study HERE

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