Pathogen evades immune system by targeting the microbiome

Added on 09 December 2021

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Pathogen evades immune system by targeting the microbiome

A team of biologists has identified that the pathogenic fungus Verticillium dahliae, responsible for wilt disease in many crops, secretes an 'effector' molecule to target the microbiome of plants to promote infection. The research was performed by the team of Alexander von Humboldt Professor Dr Bart Thomma at the University of Cologne (UoC) within the framework of the Cluster of Excellence on Plant Sciences (CEPLAS) in collaboration with the team of Dr Michael Seidl at the Theoretical Biology & Bioinformatics group of Utrecht University in the Netherlands. The study 'An ancient antimicrobial protein co-opted by a fungal plant pathogen for in planta mycobiome manipulation' has appeared in the Proceedings of the National Academy of Sciences (PNAS).

Scientists increasingly recognize that an organism's microbiome -- the totality of bacteria and other microbes living in and on it -- is an important component of its health. For humans as well as other animals, particular microbes inhabiting the gut and the skin have beneficial effects. This is similarly true for plants. Moreover, it has been established that plants can 'recruit' beneficial microbes from their environment, for instance from the soil surrounding the roots, to help them withstand disease.

At the UoC, together with Dr Nick Snelders lead author of the study Dr Thomma hypothesized that if plants can do this, perhaps some pathogens have 'learned' to perturb this 'cry for help' and disturb the plant's microbiome in order to promote invasion. Thus, in addition to the direct suppression of the plant host's immune responses, these pathogens can suppress immunity indirectly by affecting the plant's healthy microbiome.

Verticillium dahliae is a well-known pathogen of many plants, including greenhouse crops like tomatoes and lettuce, but also olive trees, ornamental trees and flowers, cotton, potatoes, and others. The current study shows that the fungus secretes the antimicrobial protein VdAMP3 in order to manipulate the plant's microbiome as an effector.

Generally, effector molecules target components of the host immune system, leading to immune suppression. The authors have now shown that these targets extend to inhabitants of the host's microbiome: during host colonization, the VdAMP3 molecule suppresses beneficial organisms in the microbiome of the plant, leading to microbiome disturbance or 'dysbiosis', so that the fungus can complete its life cycle and produce progeny that can spread and start new infections.

'In terms of evolution, the molecule that is secreted is very old. Homologs also occur in organisms that are not pathogenic on plants,' said Thomma. 'It looks like Verticillium "used" the molecule to "exploit" it during the process of disease development on the host. Interestingly, the molecule does not act like a broad-spectrum antibiotic that targets any microbe, but specifically against "competitor" fungi that have abilities to hinder Verticillium.'

Initially, the researchers wanted to find out whether Verticilium had 'effectors' in its arsenal that have antimicrobial activity. Different candidates were then tested for their ability to inhibit the growth of test microbes in the laboratory. VdAMP3 was one of these potential candidates. Follow-up experiments then showed that without the 'effector', other fungi -- antagonists -- could thrive and suppress the formation of Verticillium reproduction structures. VdAMP3 is mainly active in later stages of disease development, when Verticillium needs to produce these new reproduction structures to start infections of new hosts. However, this is not the first such molecule the scientists have identified: A year ago, they found a molecule that does not act against competing fungi, like VdAMP3, but against bacterial competitors.

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