Frog microbiome prepared for future exposure to deadly chytrid fungus by vaccine.

A living organism’s microbiome, including bacteria and fungi, can positively affect its immune system. But, the effects of vaccines against harmful pathogens on the microbiome remain to be determined. A new study done by Penn State researchers discovered that an innovative vaccine against the deadly chytrid fungus in frogs can alter the microbiome composition, making them more capable of fighting future exposure to the fungus.

The research, published in the Philosophical Transactions of the Royal Society B journal’s special issue of June 12, implies that the microbiome response can be a crucial but neglected part of vaccine efficacy.

Gui Becker, the study leader and a biology associate professor at Penn State, stated, “The microorganisms that make up an animal’s microbiome can often help defend against pathogens, for example, by producing beneficial substances or by competing against the pathogens for space or nutrients. But what happens to your microbiome when you get a vaccine, like a COVID vaccine, a flu shot, or a live-attenuated vaccine like the yellow fever vaccine? In this study, we used frogs as a model system to start exploring this question.”

The chytrid fungus endangers both frogs and other amphibians, with reported extinctions and significant population declines across several continents. In certain susceptible species, it induces a lethal skin disorder.

Becker, who is also a member of Penn State’s One Health Microbiome Center and the Center for Infectious Disease Dynamics, explained that “Chytrid is one of the worst, if not the worst, pathogen for wildlife conservation in recent history, and there is a critical need to develop tools to control its spread. We found that, in some cases, vaccines can induce a protective shift in the microbiome, which suggests that carefully manipulating the microbiome could be used as part of a broader strategy to help amphibians, and perhaps other vertebrates, deal with emerging pathogens.”

The researchers gave tadpoles a specific vaccine, which included non-lethal chytrid fungus metabolites. The researchers tracked the changes in bacteria species and their relative proportions within the microbiome after five weeks. They also measured each species’s effect on the fungus, including whether it encouraged, inhibited, or had no effect. They combined their results with a significant database of this information.

“Increasing the concentration and duration of exposure to the chytrid product prophylaxis significantly shifted the composition of the microbiome so that there was a higher proportion of bacteria producing anti-chytrid substances,” commented Samantha Siomko, the paper’s first author and a former master’s student in the Becker Lab at the University of Alabama. “This protective shift suggests that, if an animal were exposed to the same fungus again, its microbiome would be better capable of fighting the pathogen.”

Previous attempts to modify the microbiome focused on introducing one or more potent antifungal metabolites-producing bacteria species, or probiotics. However, the researchers cautioned that bacteria must contend with other microbes and is not always successful in becoming a permanent member of the microbiome.

“These frogs have hundreds of bacterial species on their skin that they pick up from their environment, and the composition changes regularly, including with the seasons,” said Becker. “Attempting to manipulate the community, for example, by adding bacterial probiotics, is challenging because the dynamics are complex and unpredictable. Our results are promising because we have essentially manipulated the entire bacterial community, making it more effective against fighting the fungal pathogen without adding a living thing that needs to compete for resources to survive.”

The researchers noted that the microbiome’s diversity was not affected, only the composition and relative proportions of species. They believe that this is promising because a decline in diversity can lead to illness or death, and it is generally agreed that preserving a diverse microbiome allows the bacteria and microbe species community to react more dynamically and with higher functional redundancy to threats.

The researchers have named this adaptive change in the microbiome composition the “microbiome memory,” which they claim could play a significant role in vaccine efficacy. The research team hopes to explore the mechanisms behind the shift and study microbiome memory in adult frogs as well as other vertebrate species in the future.

“Our collaborative team implemented a prophylaxis technique that relied on metabolic product derived from the chytrid fungus,” said Becker. “It’s possible that vaccines based on mRNA or live cells, like those often used to protect against bacterial or viral infections, may affect the microbiome differently, and we are excited to explore this possibility.”

The University of Connecticut’s Teagan McMahon, who developed the prophylaxis approach, and the University of Alabama’s Sasha Greenspan, Wesley Neely, and Stanislava Chtarbanova, the University of Massachusetts’ Douglas Woodhams, and Emory University’s K.M. Barnett are also part of the research team.

 

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