Image Credit: Scientific Frontline / stock image
Scientific Frontline: Extended "At a Glance" Summary: The Evolutionary Origin of Fungal Effector Proteins
The Core Concept: Fungal effector proteins, which modern pathogens use to infect their hosts, originally evolved from ancient antimicrobial proteins utilized for basic microbial competition.
Key Distinction/Mechanism: Unlike purely immunosuppressive molecules, these fungal effectors serve a deadly dual function. They directly penetrate host cells to manipulate immune reactions, while simultaneously deploying antimicrobial properties to attack and disrupt the host organism's protective microbiome.
Major Frameworks/Components:
- Effector Proteins: Secreted molecules utilized by pathogenic fungi to actively suppress host immunity.
- Microbiome Disruption: The biological principle that up to half of a fungus's secreted proteins possess antimicrobial activities designed to kill competing beneficial microbes.
- Vd424Y Mechanism: A specific effector in the plant pathogen Verticillium dahliae that demonstrates the ability to penetrate host cell nuclei to alter immune responses and microbiome composition.
- Evolutionary Co-optation: The theoretical framework illustrating how primitive microbial defense tools were evolutionarily upgraded to manipulate multicellular hosts.
Branch of Science: Evolutionary Biology, Microbiology, Plant Sciences, and Mycology.
Future Application: This research provides foundational knowledge for developing advanced agricultural disease control strategies, exploring new approaches for treating human and animal fungal infections, and mining fungal catalogs to engineer next-generation antibiotics.
Why It Matters: This discovery fundamentally shifts the understanding of pathogenesis. It reveals that the evolutionary arms race of microbial competition was the necessary precursor to host manipulation, demonstrating that targeting the microbiome is central to how fungal diseases develop.
An international research team led by Cologne-based plant scientist Professor Dr Bart Thomma from the Institute for Plant Sciences, the Collaborative Research Centre MiBiNet and the CEPLAS Cluster of Excellence for Plant Sciences has discovered the surprising evolutionary origin of fungal effector proteins: molecules that pathogens use today to infect their hosts appear to have evolved from ancient antimicrobial proteins. The findings can contribute to a better understanding of the development of diseases. These results provide new insights into how fungi attack both the host immune system and the surrounding microbiome during infection and suggest that this strategy could extend far beyond plant pathogens. The study has just been published under the title “Plant-associated fungi co-opt ancient antimicrobials for host manipulation” in the journal Science Advances.
In addition to harmful fungi, bacteria and viruses, the microbiomes of plants and other organisms also include many beneficial microorganisms that help to ward off diseases. Plants secrete diverse metabolic products to keep pathogens at bay and recruit beneficial microbes for support. Microorganisms that want to infect a plant and cause disease must overcome the protection that is provided by this microbiome.
“We already know that ‘effectors’ play an important role in this process. These are molecules, often proteins, which are secreted by pathogenic fungi to weaken the host plant’s immune system. To our surprise, we found that quite a few effectors also have antimicrobial effects and attack the host’s microbiome,” explains Bart Thomma, head of the study. In their study, the scientists use the example of the Verticillium dahliae effector Vd424Y to show how an effector influences the plant microbiome during infection and manipulates host immunity.
Lead author Dr Fantin Mesny has discovered that, roughly speaking, up to half of all proteins secreted by a fungus have antimicrobial activities, i.e. they can disrupt or kill microorganisms. Each fungus probably secretes hundreds of such antimicrobial proteins that have not yet been recognized to have such activities.
The scientists also noticed that many of the effectors that pathogenic fungi use to suppress the host plant’s immune system to cause disease are very common throughout the fungal Kingdom and even show structural similarities to effectors in non-pathogenic fungi. “We conclude from this that fungi do not primarily possess these antimicrobial proteins to cause diseases, but rather to be able to compete with other microorganisms,” says Thomma.
From an evolutionary perspective, the ancestors of today’s harmful fungi were not yet pathogenic. However, they developed antimicrobial proteins to compete with other microorganisms in their environment and to be able to defend themselves against bacteria, for example. Over the course of evolution, plants and other organisms developed that became colonized by fungi. The fungi at that time used their antimicrobial proteins to prevail over other microorganisms during host colonization. Subsequently, evolutionary changes occurred in the antimicrobial proteins, which gave them additional functions, such as suppressing the host’s immune system. The team was able to show that the ancient antimicrobial effector protein Vd424Y of the plant pathogen Verticillium dahliae alters the composition of the plant microbiota during infection and thus contributes to disease development. In addition, mutations have given this effector the ability to penetrate host cells, reach the cell nucleus, and directly influence plant immune reactions and other cellular processes. Ultimately, this effector therefore fulfils a dual function: It manipulates the host immune system, while also providing an advantage in competition with other microorganisms – the host falls victim to the fungus.
“We now not only understand better how fungi trigger plant diseases, but also how the fungi’s weapons have evolved and where they come from. Microbial competition is therefore not just a side effect, but a fundamental function of effector proteins that likely already existed before pathogenic interactions with hosts developed,” says Thomma.
The researchers also suspect that this principle may not be limited to plant-associated fungi. “Since antimicrobial activity is deeply rooted in the evolution of fungi, similar mechanisms could also underlie how fungi infect animals and humans – where interactions with the host-associated microbiota and the immune system are equally crucial,” says Thomma.
Beyond the fundamental findings, the results could also have practical significance. A better understanding of how pathogens influence the host-associated microbiota could enable new strategies for disease control in agriculture while also providing approaches for dealing with fungal infections in medicine. In addition, the extensive catalogues of antimicrobial substances produced by fungi could be searched specifically for novel active substances that could be used to develop new antibiotics in the future.
Published in journal: Science Advances
Title: Plant-associated fungi co-opt ancient antimicrobials for host manipulation
Authors: Fantin Mesny, Valentina Wolf, Ana López-Moral, Anton Kraege, Wilko Punt, Saifei Liu, Jinyi Zhu, Jiyeun Park, Yukiyo Sato, and Bart P. H. J. Thomma
Source/Credit: University of Cologne
Reference Number: ebio043026_01