Adaptation of Bacillus thuringiensis to Plant Colonization Affects Differentiation and Toxicity

Lin, Yicen and Alstrup, Monica and Pang Janet, Ka Yan and Maróti, Gergely and Er-Rafik, Meriem (2021) Adaptation of Bacillus thuringiensis to Plant Colonization Affects Differentiation and Toxicity. MSYSTEMS, 6 (5). ISSN 2379-5077


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The Bacillus cereus group (Bacillus cereus sensu lato) has a diverse ecology, including various species that are vertebrate or invertebrate pathogens. Few isolates from the B. cereus group have however been demonstrated to benefit plant growth. Therefore, it is crucial to explore how bacterial development and pathogenesis evolve during plant colonization. Herein, we investigated Bacillus thuringiensis (Cry(-)) adaptation to the colonization of Arabidopsis thaliana roots and monitored changes in cellular differentiation in experimentally evolved isolates. Isolates from two populations displayed improved iterative ecesis on roots and increased virulence against insect larvae. Molecular dissection and recreation of a causative mutation revealed the importance of a nonsense mutation in the rho transcription terminator gene. Transcriptome analysis revealed how Rho impacts various B. thuringiensis genes involved in carbohydrate metabolism and virulence. Our work suggests that evolved multicellular aggregates have a fitness advantage over single cells when colonizing plants, creating a trade-off between swimming and multicellularity in evolved lineages, in addition to unrelated alterations in pathogenicity. IMPORTANCE Biologicals-based plant protection relies on the use of safe microbial strains. During application of biologicals to the rhizosphere, microbes adapt to the niche, including genetic mutations shaping the physiology of the cells. Here, the experimental evolution of Bacillus thuringiensis lacking the insecticide crystal toxins was examined on the plant root to reveal how adaptation shapes the differentiation of this bacterium. Interestingly, evolution of certain lineages led to increased hemolysis and insect larva pathogenesis in B. thuringiensis driven by transcriptional rewiring. Further, our detailed study reveals how inactivation of the transcription termination protein Rho promotes aggregation on the plant root in addition to altered differentiation and pathogenesis in B. thuringiensis.

Item Type: Article
Additional Information: Funding Agency and Grant Number: Chinese Scholarship CouncilChina Scholarship Council; Lendulet-Program of the Hungarian Academy of Sciences [LP2020-5/2020] Funding text: Y.L. was supported by a Chinese Scholarship Council fellowship. G.M. was supported by the Lendulet-Program of the Hungarian Academy of Sciences (LP2020-5/2020) . All authors contributed to, and approved, the final version of the paper. Y.L. and a.T.K. conceived the project. Y.L. performed the experiments and analyzed the data. M.A. and J.K.Y.P. constructed the rho mutant. M.E.-R. performed SEM. Y.L. and N.T. performed the RNA-Seq analysis. O.A.O. and G.M. provided resources and analysis methods. a.T.K. supervised the project. Y.L. and a.T.K. wrote the manuscript with input from all authors.
Uncontrolled Keywords: ESCHERICHIA-COLI; Pathogenesis; SUBTILIS; Biofilm formation; bacterial virulence; Arabidopsis thaliana; MICROBIAL BIOFILMS; Experimental evolution; Experimental evolution; Bacillus thuringiensis; swarming motility; MEMBRANE-DAMAGING TOXINS; CEREUS-GROUP;
Subjects: Q Science / természettudomány > QK Botany / növénytan > QK10 Plant physiology / növényélettan
Q Science / természettudomány > QR Microbiology / mikrobiológia
Depositing User: MTMT SWORD
Date Deposited: 07 Feb 2022 10:29
Last Modified: 07 Feb 2022 10:29

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