The microbiome of a native plant is much more resilient than expected

April 17, 2018    No. 4/2018 (188)

Their diversity and adaptability protect plant bacterial communities against antimicrobial substances 

The microbiome, which consists of all microorganisms that live on or in plants, animals and also humans, is important for the health and development of these organisms. In a new study published in eLife, scientists from the Max Planck Institute for Chemical Ecology in Jena, Germany, investigated how a plant responds to manipulations of its microbial associations. For their field experiments, the researchers used plants of the wild tobacco species Nicotiana attenuata which produced antimicrobial peptides (AMPs). The scientist targeted beneficial bacteria of the plant to evaluate their function in nature. Astonishingly, neither the plants nor their bacterial partners seemed impressed, and the scientists found no negative consequences of AMP expression for the plant.  The results indicate that the enormous bacterial diversity residing in natural soils may account for the stability of the plant-microbiome relationship. (eLife, April 17, 2018, DOI: 10.7554/eLife.28715).

What is the function of the microbiome? Which impact do bacteria, which have been recruited by a plant from the soil, have on plant performance in nature (here: coyote tobacco Nicotiana attenuata)? Can they improve nutrient uptake, do they increase growth and fecundity? Can they provide resistance against the attack of herbivores, such as the tobacco hornworm Manduca sexta? And what happens if plants express antimicrobial peptides (AMP) which target specific bacterial partners? The results of the study show that AMP activity leaves the plants and their bacterial partners largely unimpressed. Graphic: Arne Weinhold, Max Planck Institute for Chemical Ecology.

Without microorganisms humans would not be able to survive. Especially our gut flora is an extremely densely populated ecosystem that houses billions of bacteria which help us to digest or detoxify food, supply us with vitamins, or modulate our immune system. Similarly, plants have also a so-called microbiome. In contrast to animals and humans, microorganisms associated with plants are primarily soil microbiota. Scientists consider the soil microbiome as a kind or external plant immune system. However, due to the enormous complexity of these microbiomes it is very difficult for scientists to group bacteria as beneficial or deleterious, and some bacterial taxa are even able to morph from Dr. Jekyll into Mr. Hyde upon environmental stresses.

A team of scientists led by Ian T. Baldwin, Department of Molecular Ecology, is investigating the microbiome of the wild tobacco species Nicotiana attenuata. “In order to manipulate the microbiome, we used the expression of antimicrobial peptides. Our plants showed activity against different Bacillus species, which are mainly known as plant beneficial microbes. We assumed that that these transgenic plants might show deficits in growth or reproduction in field experiments. In other words: we wanted to make an unhappy plant to see how important microbes are for them. To our surprise, the plants appeared rather unimpressed when we compared them with controls in the field,” first author Arne Weinhold summarizes.

However, a closer look and the results of further experiments indicate that different strains of the same bacterial species differ in AMP-sensitivity. Current methods used to characterize the microbiome fail to recognize these differences. The scientists believe that the antimicrobial peptides target single strains. Yet, the enormous diversity of bacteria in the soil provides a vast potential for new partnerships. The potential negative effects that AMP expression might have on a transgenic plant are lower than previously thought.

On their field site at Brigham Young University's Lytle Ranch Preserve, the scientists of the Department of Molecular Ecology study ecological interactions of the wild tobacco species Nicotiana attenuata in the plant's native habitat. Photo: Arne Weinhold, MPI Chem. Ecol.

Animals and plants produce natural antimicrobial peptides. Even in our gut, antimicrobial peptides are produced. Since most of the commensal or beneficial microbes from the human gut flora are naturally resistant to inflammation-associated antimicrobial peptides they help to keep the gut flora in balance during an inflammation. For medical purpose the agents are even considered as potential alternatives to antibiotics to fight pathogens which have become drug resistant. While antimicrobial peptides may be very potent against single bacterial strains under laboratory conditions, their effect on a whole community of bacterial strains in natural environments has rarely been evaluated and is rather questionable. “This is why it is so important to study plants not only in the greenhouse, but also under natural conditions, in the natural soils of their ancestral habitat. Laboratory experiments, in which humans control the variables that will be varied, will only provide results that are limited by the human imagination. Experiments conducted in the real world, in nature, deliver results, which sometimes challenging to interpret, are not bounded by human imagination,” says the leader of the study, Ian Baldwin, who has been studying the ecological interactions of Nicotiana attenuata in nature for more than 20 years.

Studying the microbiome of a plant and its effects on the plant’s development and the health, turns out to be much more difficult and complex than expected. The Jena researchers are now planning further experiments with tobacco plants in order to find out how these plants recruit soil bacteria, how they maintain the relationship with their bacterial partners and how they keep them from morphing into deleterious pathogens.


Original Publication:
Weinhold, A., Dorcheh, El. K., Li, R., Rameshkumar, N., Baldwin, I.T. (2018). Antimicrobial peptide expression in a wild tobacco plant reveals the limits of host-microbe-manipulations in the field, eLife, DOI: 10.7554/eLife.28715
https://doi.org/10.7554/eLife.28715 


Further Information:
Prof. Ian T. Baldwin, Max Planck Institute for Chemical Ecology, Hans-Knöll-Straße 8, 07745 Jena, Germany, Phone +49 (0)3641 571101, baldwin@ice.mpg.de 


Download of high resolution images via http://www.ice.mpg.de/ext/downloads2018.html