Forest health in the time of a pandemic: how genomic biosurveillance discovered a new hybrid pathogen variant

Genomic biosurveillance of the pathogen responsible for sudden oak death in the United States and sudden larch death in Europe reveals a novel variant that is a hybrid between European and American lineages.

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I am a very lucky person. I am a nature lover and my job involves spending time in the woods to monitor forest health and collect samples to analyse. My entire family gets into it and they know that walking in the woods with me will involve digging up roots or looking at fungal fruiting bodies and dead branches. During the COVID19 pandemic, daily forest bathing kept me sane and healthy. In the forest, where the air is pure, is where I find peace and recharge my batteries.

Hiking in the forest
Forests provide a peaceful environment to recharge our batteries. Photo R. Hamelin 

More and more studies are linking our health with the presence or proximity of trees and forests. Healthy forests support a healthy environment – they purify the water and the air, maintain wildlife habitats and help preserve healthy soils, just to name a few of the benefits. Trees are just good for us.

Tree hugging
Forests provide important ecosystem services, include human health. Photo Bettina Hamelin

Increasingly, our forests are facing unprecedented threats from invasive species that can cause irreversible damage to ecosystems. This trend is driven by globalization1. The increase in the movement of goods and people is the main reason behind the accidental introduction of most forest enemies. This is exacerbated by climate change that increases tree stress and expands the range of invasive species.

Genomic surveillance is a powerful approach that has been instrumental in the identification of variants of SARS-CoV-2 and the monitoring of the virus evolution2. Similarly, genomic surveillance (also called biosurveillance) can help us discover and track new variants of tree pests and pathogens3,4. The BioSurveillance of Alien Forest Enemies (BioSAFE; www.biosafegenomics.ca) project aims at developing new tools and resources to improve our ability to identify and track forest pests and pathogens.

My co-author and BioSAFE co-PI, Guillaume Bilodeau, is the Head of the Plant Pathogen Identification Research Lab at the Canadian Food Inspection Agency. He is an expert on Phytophthora ramorum, the pathogen that causes sudden oak and larch death. Guillaume has developed a method to identify the lineages that make up the population of this pathogen5. His lab systematically applies this method to all P. ramorum samples that are found during nursery inspections and surveys. This is important because this pathogen is regulated by quarantines in Canada, the USA and Europe.  Having a clearer picture of the dynamics of the pathogen across time and space helps tracking the pathogen movement.

Guillaume and his team have noticed that some of the pathogen samples they received showed unusual genotypic patterns, potentially a new variant. They sequenced their genomes and when we included them in our genomic biosurveillance dataset, it became clear that they were hybrids between European and North American lineages. This is the first time that sexual reproduction has been reported in nature for this pathogen. We showed that those hybrids are viable, can produce spores and are able to infect plant tissues.

Co-authors Nicolas Feau (Natural Resources Canada) and Renate Heinzelmann (WSL) went to great length to demonstrate that the hybrid was the result of a sexual recombination event, not simply anastomosis (the fusion of hyphae). This is important because it shows that these lineages that diverged hundreds of thousands of years ago are not reproductively isolated, as previous laboratory experiments suggested. Also, it means that the hybrid could potentially introgress, i.e., recombine with one of the parental lineages and generate a multitude of new genotypes.

The behavior of hybrid pathogens can be unpredictable. Some can attack new hosts or expand their range. Some can become resistant to fungicides. Even prior to our discovery of hybridization in P. ramorum, its behavior had been somewhat unpredictable and surprising. It can sporulate profusely on the foliage of some hosts such as bay laurel, but without causing much damage. Yet when the pathogen infects oak trees, it attacks the stems and can cause a lethal disease. Three decades after the beginning of the outbreak, the pathogen was discovered attacking the foliage, stems and branches of a conifer, larch, in the UK, killing millions of trees. This sent a chill down the spine of forest health specialists.

Sudden larch death
Sudden larch death, caused by Phytophthora ramorum, in Scotland. Photo R. Hamelin
Sudden larch death symptoms.
Cankers caused by Phytophthora ramorum on larch. Photo Richard Hamelin

What are the potential impacts of this discovery? It’s hard to tell. The pathogen has been eradicated in the nursery where it was found. But given the unpredictability of this pathogen, it is important to monitor its presence and to assess its pathogenicity on a broad range of trees and plants. Certainly, the ability of P. ramorum to attack and kill conifers is worrisome to countries like Canada and the USA with vast conifer forests.

Our team showed that genomic biosurveillance is possible for tree pathogens and, just like the SARS-CoV-2 genomic surveillance effort, can lead to the discovery and tracking of novel variants. This new tool in our fight against invasive species comes at the right time as pressure increases on many ecosystems. There is a long list of environmental catastrophes caused by invasive tree pathogens in the last centuries: Dutch elm disease, chestnut blight, ash dieback, white pine blister rust, to name a few. Preventing future outbreaks will ensure that we can enjoy the pleasures and benefits of walking in the forest.

Read the original paper:  Hamelin, R.C., Bilodeau, G.J., Heinzelmann, R., Hrywkiw, K., Capron, A., Dort, E., Dale, A.L., Giroux, E., Kus, S., Carleson, N.C., Grünwald, N.J., Feau, N., 2022. Genomic biosurveillance detects a sexual hybrid in the sudden oak death pathogen. Communications Biology 5, 477. https://doi.org/10.1038/s42003-022-03394-w

https://rdcu.be/cNTw9

References

  1. Santini, A., Liebhold, A., Migliorini, D. & Woodward, S. Tracing the role of human civilization in the globalization of plant pathogens. The ISME journal 12, 647–652 (2018).
  2. Cyranoski, D. Alarming COVID variants show vital role of genomic surveillance. Nature 589, (2021).
  3. Roe, A. D. et al. Fitness dynamics within a poplar hybrid zone: I. Prezygotic and postzygotic barriers impacting a native poplar hybrid stand. Ecology and Evolution n/a-n/a (2014).
  4. Hamelin, R. C. & Roe, A. D. Genomic biosurveillance of forest invasive alien enemies: A story written in code. Evolutionary Applications 13, 95–115 (2020).
  5. Bilodeau, G. J., Levesque, C. A., de Cock, A. W. A. M., Briere, S. C. & Hamelin, R. C. Differentiation of European and North American genotypes of Phytophthora ramorumby real-time polymerase chain reaction primer extension. Canadian Journal Of Plant Pathology-Revue Canadienne De Phytopathologie 29, 408–420 (2007).

Richard Hamelin

Professor and Head, Forest and Conservation Sciences Department, University of British Columbia

I am a forest pathologist, I study tree diseases. My research interests are to develop genomic approaches to better understand tree disease outbreaks and help mitigate their impact.