Microbial communities of the host and its environment influence each other
CRC 1182-research team investigates the interactions between microbial communities in host organisms and their direct environment using nematodes as a model
The entirety of bacteria, viruses and fungi that exist in and on a multicellular host organism forms its natural microbiome. It performs various vital tasks for the host, from supporting food utilisation to protecting against pathogens. On the other hand, disorders of the microbiome are associated with various serious diseases.
The Collaborative Research Centre (CRC) 1182 “Origin and Function of Metaorganisms” at Kiel University has been investigating the highly complex interactions between hosts and microorganisms and their involvement in central life history processes for several years. In a recent study, the researchers focussed on the question of how the microbiome of a living organism and its immediate microbial environment influence each other.
They found evidence that the microbiome of nematodes of the genus Caenorhabditis does not have a core, universal composition, but is instead highly individual and dependent on the microbial environment of its habitat. Furthermore, they gathered evidence that the animals may also be able to influence the microbial composition of their immediate environment – possibly to create a niche with favourable living conditions. This was also shown by the fact that apples colonised by worms had a significantly different metabolome signature than those without worms. The new results on reciprocal microbiome dynamics were recently published by a team from Kiel University’s Evolutionary Ecology and Genetics research group led by Professor Hinrich Schulenburg in the scientific journal mSystems.
Comparative study of nematode and apple microbiomes
A fundamental research question is how the microbial colonisation of a living organism is initially assembled. In particular, researchers are discussing whether a specific, stable (“core”) microbiome typical of its species develops in different organisms, whose members fulfil certain functions for the host. The CRC 1182 research team uses the model organism C. elegans, which feeds on bacteria and lives on rotting fruit, for such investigations. Its microbiome is therefore strongly characterised by its immediate environment, the substrate. “Although studies on worm microbiomes in natural substrates already exist, we have now investigated how the natural microbial environment influences the microbiome composition of the animals by systematically comparing different substrates,” explains Dr Julia Johnke, first author of the study and research associate in Schulenburg’s research group.
In order to clarify this missing aspect, the Kiel research team analysed such a natural substrate and its interactions with the nematode: they used a natural compost heap containing apples from an orchard. “Over a period of two years, we removed ten apples each week and analysed the microbiome of the nematodes found on them, as well as the microbiome of the apples themselves,” says CRC 1182 member Johnke.
Environment and host microbiome influence each other
More than in other organisms, the microbiome of the bacterivorous nematode is directly affected by the substrate on which it lives and from which it feeds. “If you compare, for example, worms from an apple with worms from other substrates, their microbiomes are very different. Certain abundant bacterial genera clearly indicate their origin from the apple substrate,” says Johnke. Interestingly, the microbial colonisation of individual worms is distinct even if they come from the same substrate, for example the same apple. “This observation confirms that there is no so-called “core” microbiome in and that other factors control the microbiome composition of the animals,” says the biologist. The researchers assume that important functions in the worm microbiome are therefore not necessarily conserved in certain bacterial species, but can possibly also be provided by different, randomly assembled microbiome compositions.
The research team identified an effect known as ‘dispersal limitation’ as the determining factor in this largely random microbiome composition of the nematode: “The worm cannot move in a wider radius and forms a separate ecosystem in its gut. Its microbiome therefore only contains bacteria that it can ingest from its immediate environment. As a result, establishment and displacement processes take place in the intestine among the bacterial species ingested. Ultimately, this results in a microbiome composition that is dependent on access to the substrate source and on competition in a closed system – and is therefore characterised by chance,” explains Johnke.
In a next step, the research team collaborated with Dr. Thomas Stegemann from Kiel University’s Pharmaceutical Institute and Dr. Dorothee Langel from Kiel University’s Botanical Institute for a metabolome analysis to investigate the metabolic products associated with the microbiomes in the apples. “Initially, one would assume that the microbial substrate mainly influences the microbiome of the worms and thus their metabolism. However, we have actually discovered evidence that the worms also influence the microbial composition of the apple and their metabolic processes, possibly even more strongly than vice versa,” emphasises Johnke.
This indicates a possible niche construction in which the worm can influence the microbiome of its environment and thus possibly create favourable living conditions for itself. A comparison with nematode-free apples also showed that certain bacteria and metabolic products were present in apples colonised by worms, indicating a different degree of ripeness in the apples. The presence of C. elegans therefore apparently changed the metabolic processes of the apple – or the worms tend to favour riper apples when choosing their habitat.
“Our analyses underline a significant reciprocal influence of host organisms and substrate in the formation of the microbiome composition. Of particular interest is our evidence that a host organism can influence the microbial composition of its environment, including its metabolic capacity, in previously unknown ways. Overall, this improves our general understanding of host-microbiome interactions in their natural habitat,” summarises CRC 1182 spokesperson Schulenburg.
Original publication:
J. Johnke, J. Zimmermann, T. Stegemann, D. Langel, A. Franke, L. Thingholm, H. Schulenburg (2025): Caenorhabditis nematodes influence microbiome and metabolome characteristics of their natural apple substrates over time. mSystems
First published: 10 January 2025 DOI: 10.1128/msystems.01533-24
Images are available for download:
https://www.uni-kiel.de/de/pressemitteilungen/2020/073-johnke-env-microbio-author.jpg
Caption: Using nematodes as an example, Dr Julia Johnke and her colleagues investigated the interactions of microbial composition in host organisms and their direct environment.
© Christian Urban, Kiel University
https://www.uni-kiel.de/de/pressemitteilungen/2020/229-zarate-plospath-wurm.jpg
Caption: The CRC 1182 researchers showed that the microbiome of nematodes such as C. elegans is highly individual and dependent on the microbial environment of its habitat and that the worms can also influence the microbial composition of the substrate around them.
© Prof. Hinrich Schulenburg
https://www.uni-kiel.de/de/pressemitteilungen/2025/035-johnke-msys-apples.jpg
Caption: By systematically comparing different substrates, for example rotting apples from a compost, the research team investigated the influence of the natural microbial environment on the microbiome composition of the host organism.
© Dr Julia Johnke
Contact:
Prof. Hinrich Schulenburg
Evolutionary Ecology und Genetics Group, Head
Kiel University
Phone: +49 431-880-4141
Email: hschulenburg@zoologie.uni-kiel.de
Dr Julia Johnke
Evolutionary Ecology und Genetics Group
Kiel University
Phone: +49 431-880-4146
Email: jjohnke@zoologie.uni-kiel.de
More information:
Evolutionary Ecology und Genetics Group,
Zoological Institute, Kiel University:
www.uni-kiel.de/zoologie/evoecogen
