Metabolism of spruce tree defenses in plant-insect-microorganism interactions
We aim to understand how insects and their associated fungi metabolize plant defensive compounds, and how these mechanisms shape interactions between plants, insects, and fungi.
Plants, insects, and microorganisms are connected through intricate chemical interactions that shape ecological relationships across terrestrial ecosystems. In forest environments, these interactions are especially evident in the Norway spruce–bark beetle system, where trees, herbivorous insects, and diverse fungal communities engage in a dynamic chemical arms race. Norway spruce relies on a broad spectrum of defensive metabolites, particularly phenolic compounds, to protect itself against insect attack and microbial invasion. Yet, despite these potent chemical defenses, bark beetles and associated microorganisms successfully colonize spruce phloem.
Our research aims to understand how plant defensive compounds are metabolized within plant–insect–microorganism interactions and how these metabolic processes influence ecological systems. We focus on the chemical transformations that occur as plant-derived compounds move across trophic levels, from spruce trees to insects, pathogenic fungi, symbionts, and further to entomopathogenic and mycoparasitic fungi. These transformations can alter toxicity and biological activity, thereby shaping survival, infection success, and competitive interactions among organisms. Using the bark beetle–spruce system as a model, our projects combine chemical ecology, metabolomics, molecular biology, genetics, and artificial intelligence–based data analysis. We investigate how insects activate plant defenses, how bark beetle symbionts and pathogens metabolize plant phenolic compounds, and how entomopathogenic and mycoparasitic fungi modify these chemical compounds to indirectly control bark beetle invasions. By linking metabolic pathways to gene and protein function, we aim to uncover the molecular mechanisms that underlie these interactions and determine their ecological significance.
Project 1: Chemical transformations shape plant–insect–entomopathogen interactions
Main researchers: Dr. Ruo Sun, Baoyu Hu and Maxwell Zienecker
Main collaborators. Dr. Yoko Nakamura (MPI-CE, Department of Natural Product Biosynthesis); Katrin Luck (MPI-CE, Department of Natural Product Biosynthesis); Prof. Xingcong Jiang (CEMPS, Chinese Academic institute for sciences)
Plants, insects, and microorganisms are connected by a hidden chemical language. Plants produce defensive chemicals to protect themselves. Insect herbivores ingest and modify these compounds while feeding, and entomopathogenic fungi must cope with, or overcome, these chemical defenses to survive and infect their hosts. What happens to these chemicals as they move through different organisms can strongly influence who survives and who does not. This project explores how plant-derived chemicals are transformed as they pass from trees to insects and then to entomopathogenic fungi. Using bark beetles and their natural fungal pathogens as a model system, we study how insects activate plant defense compounds and how fungi detoxify them to enable infection. These chemical transformations help explain why some pathogens succeed despite strong plant defenses. This project aims to reveal hidden chemical connections in complex biological systems. Understanding these processes improves our knowledge of ecological interactions and may support the development of more effective, environmentally friendly strategies for managing forest pests.
Project 2: Can beneficial fungi help spruce trees fight bark beetle symbiotic fungi (phytopathogen)?
Main researchers: Baoyu Hu and Marlene Fehrenbach
Main collaborators: Dr. Yoko Nakamura (MPICE, Department of Natural Product Biosynthesis); Dr. Veit Grabe (MPICE, Microscopy Imaging Service Group)
Bark beetle infestations are a growing threat to Norway spruce forests, partly because the fungi they carry act as potent pathogens, weakening tree defenses. Within spruce phloem, these pathogenic fungi convert stored plant compounds into active antifungal chemicals, creating a challenging environment for other microorganisms. Yet, certain beneficial fungi, known as mycoparasites, are able to survive and even parasitize these pathogens. How do these fungi detoxify the chemical defenses from their host environment? Our research explores the interactions between spruce trees, bark beetle-associated fungi, and mycoparasitic fungi such as Chaetomium globosum. We investigate whether and how they neutralize antifungal compounds and suppress pathogens, and what mechanisms allow mycoparasites to metabolize pathogenic fungi derived compounds. Understanding these questions could reveal new strategies for protecting spruce forests from bark beetle outbreaks and the fungi they vector, while also shedding light on the complex chemical and ecological networks in the microecosystem of Norway spruce trees.
Project 3: AI-based mass spectrometry analysis for metabolic transformation studies in chemical ecology
Main researcher: Dr. Guilin Hu
Chemical ecology explores how chemicals shape interactions between organisms and their environments. Many of these interactions depend on what happens to external compounds, such as plant chemicals, microbial products, or host-derived molecules, after they enter a living system. As these compounds are metabolized, they can influence feeding, defense, and cooperation or conflict between organisms. Understanding these metabolic transformations is key to revealing how chemicals drive ecological processes. Modern mass spectrometry allows us to detect thousands of chemicals from complex biological samples. However, the sheer complexity of these data makes it difficult to understand how detected molecules are related through biological metabolism, especially when reference information is limited. This project is developing an AI-powered tool, named “MSmaster”, to uncover metabolic connections within mass spectrometry data. Instead of focusing on single compounds, we use machine learning to organize chemical signals into networks that highlight likely metabolic relationships. By revealing how exogenous compounds are transformed and connected in biological systems, our approach helps generate new, biologically informed hypotheses and advances our understanding of chemical-driven interactions in nature.
Project 4: Uncovering how bark beetle symbiotic fungi overcome spruce defenses
Main researchers: Baoyu Hu, Shivani Nimbkar, and Chengcheng Li
Main collaborators: Dr. Yoko Nakamura (MPICE, Department of Natural Product Biosynthesis); Almuth Hammerbacher (Forestry and Agricultural Biotechnology Institute, University of Pretoria, South Africa); Prof. Benke Hong (Westlake University, China)
In Norway spruce forests, bark beetle infestations are often accompanied by fungal symbionts that the beetles carry into the tree. These fungi are thought to assist the beetles by overcoming the tree’s chemical defenses, including phenolic compounds that normally protect spruce from infection. Despite their ecological importance, the mechanisms by which these fungal partners neutralize or metabolize spruce defense chemicals remain largely unknown. This project aims to uncover how bark beetle-associated fungi adapt to and thrive in the chemically hostile environment of spruce phloem. We will begin by testing how spruce phenolic compounds affect the growth and activity of these fungal symbionts. Next, we will trace the pathways the fungi use to break down or modify defensive chemicals, exploring the underlying metabolic and molecular processes. By integrating ecological bioassays with protein- and gene-level analyses, we hope to reveal the strategies these fungi employ to survive, colonize, and support bark beetle infestations. Understanding these fungal detoxification mechanisms could provide new insights into forest ecosystem dynamics and the chemical arms race between trees and their microbial invaders. The study highlights the crucial role of fungal symbionts in shaping the success of bark beetle outbreaks.
Project 5: Fungal detoxification strategies in bark beetle–infested spruce trees
Main researcher: Dr. Ruo Sun
Main collaborator: Dr. Liujuan Zheng (Philipps University of Marburg)
Bark beetle infestation creates a complex fungal community within Norway spruce galleries, including phytopathogenic fungi, bark beetle–associated symbionts, entomopathogenic fungi, and mycoparasitic fungi. Although spruce trees respond to invasion by producing high concentrations of phenolic compounds with strong antifungal activity, these diverse fungi persist and remain functionally active within the chemically hostile environment of the phloem. We found that different fungi have used distinct strategies to detoxify plant defensive compounds.
This project investigates the molecular and ecological mechanisms by which fungi metabolize spruce phenolics into less toxic or non-toxic products. Using metabolomic analyses, we identify detoxification pathways employed by multiple fungal species and characterize the genes and proteins involved in these transformations. Functional analyses are conducted through targeted gene knockout mutants to determine the ecological roles of these detoxification mechanisms within the spruce–bark beetle–fungi system. Our results indicate that detoxification reactions mainly modify the hydroxyl groups of phenolic compounds. To better understand enzyme function, we further examine catalytically important amino acids through site-directed mutagenesis. By linking biochemical mechanisms with ecological outcomes, this research aims to clarify how fungal detoxification contributes to fungal survival, competition, and interaction dynamics in bark beetle–infested spruce trees.