The Plant Host Induces Antibiotic Production To Select the Most-Beneficial Colonizers

Abstract

Microbial ecosystems tightly associated with a eukaryotic host are widespread in nature. The genetic and metabolic networks of the eukaryotic hosts and the associated microbes have coevolved to form a symbiotic relationship. Both the Gram-positive Bacillus subtilis and the Gram-negative Serratia plymuthica can form biofilms on plant roots and thus can serve as a model system for the study of interspecies interactions in a host-associated ecosystem. We found that B. subtilis biofilms expand collectively and asymmetrically toward S. plymuthica, while expressing a nonribosomal antibiotic bacillaene and an extracellular protease. As a result, B. subtilis biofilms outcompeted S. plymuthica for successful colonization of the host. Strikingly, the plant host was able to enhance the efficiency of this killing by inducing bacillaene synthesis. In turn, B. subtilis biofilms increased the resistance of the plant host to pathogens. These results provide an example of how plant-bacterium symbiosis promotes the immune response of the plant host and the fitness of the associated bacteria. IMPORTANCE Our study sheds mechanistic light on how multicellular biofilm units compete to successfully colonize a eukaryote host, using B. subtilis microbial communities as our lens. The microbiota and its interactions with its host play various roles in the development and prevention of diseases. Using competing beneficial biofilms that are essential microbiota members on the plant host, we found that B. subtilis biofilms activate collective migration to capture their prey, followed by nonribosomal antibiotic synthesis. Plant hosts increase the efficiency of antibiotic production by B. subtilis biofilms, as they activate the synthesis of polyketides; therefore, our study provides evidence of a mechanism by which the host can indirectly select for beneficial microbiota members.on July 10, 2020 by guest http://aem.asm.org/ Downloaded from RESULTSB. subtilis biofilm actively expands toward a competing S. plymuthica colony. When grown on a solid biofilm-inducing medium, B. sutbilis biofilms form symmetrical, circular colonies. To determine the effect of a competing S. plymuthica colony on the development of a B. subtilis biofilm, the two species were inoculated next to each other on a solid biofilm medium. After 2 days, the B. subtilis colony reached S. plymuthica, forming a thick wrinkle around its edge and penetrating toward its center. By the third day, B. subtilis biofilm completely engulfed the S. plymuthica colony, covering it with a thin, unstructured film and enclosing it within the circular wrinkle (Fig. 1A). The location and shape of the B. subtilis center of the biofilm did not change during the interaction with S. plymuthica. However, the biofilm colony advanced asymmetrically toward the S. plymuthica colony, breaking from its usual circular shape ( Fig. 1A).We next examined the mechanisms that could mediate this asymmetric expansion toward a competitor. Many bacterial cells are capable of directional swimming using their flagella (2...

Quantifying the effects of the plant root on antibiotic production in the beneficial bacterium B. subtilis

“…In contrast, each of the induced antibiotics were shown to grant protection to the plant versus fungal and bacterial pathogens. Interestingly, we previously demonstrated that the interaction with the plant increases the capacity of B. subtilis to compete with Serattia Plymuthica, and our current results further indicate that the root is active regulator of the competitive interactions occurring on its roots (Ogran et al, 2019). The complexity of these antibiotic-host interactions suggests that B. subtilis biofilms can be considered a part of the plant microbiome, with the host actively promoting the establishment of the most beneficial bacterial community.…”

Weaponizing volatiles to inhibit competitor biofilms from a distance

“…Instead, we found that specific inhibition of ECM production inhibited normal biofilm development and limited colony spreading. In biofilms, bacteria frequently migrate towards new niches by sliding, powered by cell division and ECM production 8,15,54 . Blocking this collective motility may serve as an effective strategy to distance competitors.…”

“…However, in many instances, biofilms can be beneficial. One example is the biocontrol agents that form biofilms on the surface of plant roots, producing antibiotics that prevent the growth of bacterial and fungal pathogens and inducing the plant systemic response [7][8][9][10] .…”

“…Amyloid-like proteins such as TasA are extremely common in bacterial biofilms, and their assembly into fibres is important for the integrity and structure of biofilms 14 . In addition to its structural role, the ECM is essential for B. subtilis spreading 8,15,16 .…”

Impact of spatial proximity on territoriality among human skin bacteria

“…The use of flagella allows the bacterium to swim and swarm, but the flagellum-independent sliding occurs due to growth 25 . Sliding is a poorly understood process, but it is known to depend upon multiple factors, such as the production of surfactin and/or the extracellular proteins BslA and TasA 25 – 27 .…”