Genome-wide fitness profiling reveals molecular mechanisms that bacteria use to interact with Trichoderma atroviride exometabolites
Abstract
Trichoderma spp. are ubiquitous rhizosphere fungi capable of producing several classes of secondary metabolites that can modify the dynamics of the plant-associated microbiome. However, the bacterial-fungal mechanisms that mediate these interactions have not been fully characterized. Here, a random barcode transposon-site sequencing (RB-TnSeq) approach was employed to identify bacterial genes important for fitness in the presence of Trichoderma atroviride exudates. We selected three rhizosphere bacteria with RB-TnSeq mutant libraries that can promote plant growth: the nitrogen fixers Klebsiella michiganensis M5aI and Herbaspirillum seropedicae SmR1, and Pseudomonas simiae WCS417. As a non-rhizosphere species, Pseudomonas putida KT2440 was also included. From the RB-TnSeq data, nitrogen-fixing bacteria competed mainly for iron and required the siderophore transport system TonB/Exb for optimal fitness in the presence of T . atroviride exudates. In contrast, P . simiae and P . putida were highly dependent on mechanisms associated with membrane lipid modification that are required for resistance to cationic antimicrobial peptides (CAMPs). A mutant in the Hog1-MAP kinase (Δ tmk 3) gene of T . atroviride showed altered expression patterns of many nonribosomal peptide synthetase (NRPS) biosynthetic gene clusters with potential antibiotic activity. In contrast with exudates from wild-type T . atroviride , bacterial mutants containing lesionsmore »
- Publication Date:
- Research Org.:
- Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER); USDOE Office of Science (SC), Basic Energy Sciences (BES). Scientific User Facilities (SUF)
- OSTI Identifier:
- 2004597
- Alternate Identifier(s):
- OSTI ID: 1997561; OSTI ID: 2234068
- Grant/Contract Number:
- AC02-05CH11231
- Resource Type:
- Published Article
- Journal Name:
- PLoS Genetics
- Additional Journal Information:
- Journal Name: PLoS Genetics Journal Volume: 19 Journal Issue: 8; Journal ID: ISSN 1553-7404
- Publisher:
- Public Library of Science (PLoS)
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; pseudomonas putida; polymyxins; fungi; rhizosphere; antibiotic resistance; purines; bacterial genetics; operons
Citation Formats
Villalobos-Escobedo, José Manuel, Mercado-Esquivias, Maria Belen, Adams, Catharine, Kauffman, W. Berkeley, Malmstrom, Rex R., Deutschbauer, Adam M., Glass, N. Louise, and Richter, ed., Ingrid. Genome-wide fitness profiling reveals molecular mechanisms that bacteria use to interact with Trichoderma atroviride exometabolites. United States: N. p., 2023.
Web. doi:10.1371/journal.pgen.1010909.
Villalobos-Escobedo, José Manuel, Mercado-Esquivias, Maria Belen, Adams, Catharine, Kauffman, W. Berkeley, Malmstrom, Rex R., Deutschbauer, Adam M., Glass, N. Louise, & Richter, ed., Ingrid. Genome-wide fitness profiling reveals molecular mechanisms that bacteria use to interact with Trichoderma atroviride exometabolites. United States. https://doi.org/10.1371/journal.pgen.1010909
Villalobos-Escobedo, José Manuel, Mercado-Esquivias, Maria Belen, Adams, Catharine, Kauffman, W. Berkeley, Malmstrom, Rex R., Deutschbauer, Adam M., Glass, N. Louise, and Richter, ed., Ingrid. Thu .
"Genome-wide fitness profiling reveals molecular mechanisms that bacteria use to interact with Trichoderma atroviride exometabolites". United States. https://doi.org/10.1371/journal.pgen.1010909.
@article{osti_2004597,
title = {Genome-wide fitness profiling reveals molecular mechanisms that bacteria use to interact with Trichoderma atroviride exometabolites},
author = {Villalobos-Escobedo, José Manuel and Mercado-Esquivias, Maria Belen and Adams, Catharine and Kauffman, W. Berkeley and Malmstrom, Rex R. and Deutschbauer, Adam M. and Glass, N. Louise and Richter, ed., Ingrid},
abstractNote = {Trichoderma spp. are ubiquitous rhizosphere fungi capable of producing several classes of secondary metabolites that can modify the dynamics of the plant-associated microbiome. However, the bacterial-fungal mechanisms that mediate these interactions have not been fully characterized. Here, a random barcode transposon-site sequencing (RB-TnSeq) approach was employed to identify bacterial genes important for fitness in the presence of Trichoderma atroviride exudates. We selected three rhizosphere bacteria with RB-TnSeq mutant libraries that can promote plant growth: the nitrogen fixers Klebsiella michiganensis M5aI and Herbaspirillum seropedicae SmR1, and Pseudomonas simiae WCS417. As a non-rhizosphere species, Pseudomonas putida KT2440 was also included. From the RB-TnSeq data, nitrogen-fixing bacteria competed mainly for iron and required the siderophore transport system TonB/Exb for optimal fitness in the presence of T . atroviride exudates. In contrast, P . simiae and P . putida were highly dependent on mechanisms associated with membrane lipid modification that are required for resistance to cationic antimicrobial peptides (CAMPs). A mutant in the Hog1-MAP kinase (Δ tmk 3) gene of T . atroviride showed altered expression patterns of many nonribosomal peptide synthetase (NRPS) biosynthetic gene clusters with potential antibiotic activity. In contrast with exudates from wild-type T . atroviride , bacterial mutants containing lesions in genes associated with resistance to antibiotics did not show fitness defects when RB-TnSeq libraries were exposed to exudates from the Δ tmk3 mutant. Unexpectedly, exudates from wild-type T . atroviride and the Δ tmk 3 mutant rescued purine auxotrophic mutants of H . seropedicae , K . michiganensis and P . simiae . Metabolomic analysis on exudates from wild-type T . atroviride and the Δ tmk 3 mutant showed that both strains excrete purines and complex metabolites; functional Tmk3 is required to produce some of these metabolites. This study highlights the complex interplay between Trichoderma -metabolites and soil bacteria, revealing both beneficial and antagonistic effects, and underscoring the intricate and multifaceted nature of this relationship.},
doi = {10.1371/journal.pgen.1010909},
journal = {PLoS Genetics},
number = 8,
volume = 19,
place = {United States},
year = {Thu Aug 31 00:00:00 EDT 2023},
month = {Thu Aug 31 00:00:00 EDT 2023}
}
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