Bacterial pathogens share genes to outsmart treatments and adapt to new environments

Exploring how plant pathogens evolve through the rapid acquisition of genetic elements

March 12, 2024

Bacterial pathogens can rapidly evolve antibiotic resistance by acquiring genes from other bacteria in the environment. This is true for human and plant pathogens, which are frequently controlled by applying antimicrobials like copper. This research, published in the journal PNAS, reveals how a common agricultural pathogen called Pseudomonas syringae rapidly acquires new abilities due to mobile genetic elements called Integrative and Conjugative Elements (ICEs). A newly defined family of ICEs is responsible for spreading copper resistance and virulence genes across even distantly related P. syringae. Scientists from Max Planck Institutes for Biology Tübingen and for Evolutionary Biology in Plön have discovered the extra genetic material introduced by these mobile elements allows bacterial pathogens to grow on specific compounds and rapidly adapt to changing conditions. This can influence the pathogen’s ability to infect plants and survive in the environment. This discovery reveals how pathogens gain a novel advantage through ICE-mediated gene exchange.

A destructive outbreak of kiwifruit bleeding canker disease threatened the global fruit industry and fragile local economies from 2010 onwards. The outbreak continues to affect kiwifruit-growing regions in Europe, Asia, Australia and Chile. This pandemic was caused by the bacterial pathogen Pseudomonas syringae, a common culprit among many agricultural plant diseases.

P. syringae can live on the plant surface as an epiphyte. To cause disease, it enters the plant via wounds or natural openings such as stomata. The pathogen parasitizes the water and nutrients inside the plant tissue, multiplying quickly and eventually causing host death. Despite the many defence mechanisms plants have evolved to reduce pathogen entry of pathogens, recent disease outbreaks in agricultural crops have been particularly destructive, posing effective control challenges. The advent of a new, aggressive strain known as Psa is one such example.

Unexpected cargo genes hitchhike into bacteria via mobile genetic elements

Integrative and conjugative elements (ICE) can rapidly introduce new functions to bacteria. They can move from one bacterial cell to another in minutes. The pool of ICEs identified in P. syringae consists of at least 53 distinct ICEs. Each ICE carries a set of core genes responsible for ICE movement and different sets of accessory cargo genes with encoding functions that can alter the bacterium’s ability to survive and grow in different environments. In human pathogens, the cargo genes often encode resistance to antibiotics frequently used in hospitals. Similar to ICEs found in human pathogens, ICEs in P. syringae have antimicrobial resistance genes and cargo genes whose function is not immediately apparent.

“We were already aware that ICEs move rapidly between strains and that different ICEs were circulating among the pandemic pathogen Psa” explains Dr. Honour McCann, Research Group Leader on Plant Pathogen Evolution at Max Planck Institute for Biology in Tübingen. “What surprised us is that a particular set of cargo genes linked to metabolism appears to have recently invaded ICEs, taking advantage of their mobility to spread across Psa and many other destructive P. syringae. This unexpected finding suggests this region might contribute to P. syringae’s ability to grow in different hosts and environments.”

Decoding the mechanisms of how mobile elements reprogram bacterial metabolism

To understand what this new cargo – called Tn6212 – is doing, Dr. Elena Colombi, now at the University of Melbourne, and a team of researchers used sequence analysis, genetics, and measurement of gene expression changes to investigate how Tn6212 affects bacterial growth. Dr. Colombi created multiple gene knockouts (deletions) in Tn6212 and found some were crucial for bacterial growth under nutrient-limited conditions. Strikingly, the absence of the cargo genes impaired the bacteria’s ability to grow well on compounds abundant in plant tissue. The team then found the Tn6212 cargo genes have major impacts on bacterial gene expression, likely reprogramming bacterial metabolism to capitalize on the presence of specific nutrients, resulting in faster growth. Tn6212's ability to manipulate metabolism helps the pathogen to quickly use its favourite energy sources in a given environment, such as plant tissue. This speed might allow harmful pathogens like Psa to thrive and spread more effectively.

Future research directions will delve deeper into the link between the ICE cargo genes’ manipulation of bacterial metabolism, how this manipulation impacts the success of bacterial pathogens during plant infections, and the spread of mobile elements within bacterial populations. Understanding the dynamics of mobile genetic element movement and cargo gene carriage provides crucial insight into how bacterial pathogens evolve and contributes to the development of targeted control strategies. Understanding how quickly pathogens adapt and interact with plants is essential for developing sustainable agricultural practices, crop resilience, and safeguarding our food supply.

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