Insect symbioses are surprisingly fragile
An introduced bacterium displaces the sawtoothed grain beetle's symbiotic partner
To the Point
Defenseless symbiont: A new bacterium (Sodalis praecaptivus) can destroy the millions-year-old mutualistic relationship between the sawtoothed grain beetle Oryzaephilus surinamensis and its symbiont Shikimatogenerans silvanidophilus within a few generations.
Fragile nature of an ancient symbiosis: The infection resulting from the injection of Sodalis into female beetles spreads throughout their bodies. Sodalis is passed on to the offspring via the eggs. While the beetle host exhibits a strong immune response, the original symbiont is unable to respond to the intruder due to its high degree of specialization.
New avenues for research into symbiont change: The study shows that a highly specialized symbiosis can be quickly destroyed.
The mutual dependence between insects and their bacterial symbionts is the result of millions of years of coevolution. Many insects live in close mutualistic relationships with symbiotic bacteria that provide them with essential nutrients. This partnership has developed and proven itself over millions of years. However, seemingly stable symbioses are not unchangeable. In some insect species, the loss of original symbionts or their replacement by new bacteria has been observed, even when the original partners had formed a close symbiosis over long periods of time. The mechanisms and reasons behind this exchange are largely unexplored, primarily due to the lack of experimentally accessible systems.
"The lack of an easily manageable symbiosis was the driving force behind our study," explains Ronja Krüsemer, the first author from the Department of Insect Symbiosis at the Max Planck Institute for Chemical Ecology. "Our goal was to establish a controllable model system that would allow us to directly observe and study symbiont exchange."
Sodalis praecaptivus as an intruder
In collaboration with Colin Dale from the University of Utah, who had already established an artificial symbiosis between grain weevils and the bacterium Sodalis praecaptivus, Martin Kaltenpoth's team at the Max Planck Institute for Chemical Ecology took a targeted approach. They injected the bacterium into female grain beetles (Oryzaephilus surinamensis) to test its influence on natural symbiosis.
The novel bacterium proved to be highly adaptable. It colonized nearly all of the beetles' tissues and organs and, surprisingly, was successfully transmitted from mother to offspring via eggs. The researchers were able to raise several beetle generations, which led to a surprising discovery. In the third generation, the original symbiont, Shikimatogenerans silvanidophilus had disappeared.
However, infection with Sodalis affected more than just the original symbiont. The beetles exhibited lighter cuticles, reduced life expectancy, and lower reproduction rates. At the same time, their immune systems were activated, as evidenced by increased expression of immune genes. Sodalis invaded the bacteriomes, the specialized organs that harbor the original symbiont, and altered the conditions there to the disadvantage of the old symbiont.
Genome erosion plays a decisive role here. Shikimatogenerans, which has coexisted with its host for millions of years and is exclusively found in beetles, has lost many genes due to a lack of selection pressure. This makes the symbiont more susceptible to changes in the host environment. Following the introduction of Sodalis, Shikimatogenerans was unable to adapt to the new conditions, displayed morphological abnormalities and was ultimately displaced. "We didn't expect the original symbiont to be completely lost this fast," says Ronja Krüsemer.
A pioneering model system for the future of symbiosis research
The Oryzaephilus surinamensis-Sodalis praecaptivus system is proving to be a promising model for investigating the mechanisms behind symbiont exchange, symbiosis establishment, and the evolution of mutualisms. Future studies will examine how genetic mutations influence the fitness of hosts and symbionts, and will include large-scale fitness experiments with infected beetles and their offspring.
"With our system, we can directly observe the dynamics behind symbiont exchange," says study leader Martin Kaltenpoth. "Our study shows that new bacteria can displace the original symbionts, and this process can happen faster than previously thought. Furthermore, the loss of the original symbiont can occur in the context of an incipient symbiont exchange."