Lipo-Chitooligosaccharides Induce Specialized Fungal Metabolite Profiles That Modulate Bacterial Growth

Tomás A. Rush; Joanna Tannous; Matthew J. Lane; Muralikrishnan Gopalakrishnan Meena; Alyssa A. Carrell; Jacob J. Golan; Milton T. Drott; Sylvain Cottaz; Sébastien Fort; Jean Michel Ané; Nancy P. Keller; Dale A. Pelletier; Daniel A. Jacobson; David Kainer; Paul E. Abraham; Richard J. Giannone; Jesse L. Labbé

doi:10.1128/msystems.01052-22

Lipo-Chitooligosaccharides Induce Specialized Fungal Metabolite Profiles That Modulate Bacterial Growth

Tomás A. Rush, Joanna Tannous, Matthew J. Lane, Muralikrishnan Gopalakrishnan Meena, Alyssa A. Carrell, Jacob J. Golan, Milton T. Drott, Sylvain Cottaz, Sébastien Fort, Jean Michel Ané, Nancy P. Keller, Dale A. Pelletier, Daniel A. Jacobson, David Kainer, Paul E. Abraham, Richard J. Giannone, Jesse L. Labbé

Research output: Contribution to journal › Article › peer-review

6 Scopus citations

Abstract

Lipo-chitooligosaccharides (LCOs) are historically known for their role as microbial-derived signaling molecules that shape plant symbiosis with beneficial rhizobia or mycorrhizal fungi. Recent studies showing that LCOs are widespread across the fungal kingdom have raised questions about the ecological function of these compounds in organisms that do not form symbiotic relationships with plants. To elucidate the ecological function of these compounds, we investigate the metabolomic response of the ubiquitous human pathogen Aspergillus fumigatus to LCOs. Our metabolomics data revealed that exogenous application of various types of LCOs to A. fumigatus resulted in significant shifts in the fungal metabolic profile, with marked changes in the production of specialized metabolites known to mediate ecological interactions. Using network analyses, we identify specific types of LCOs with the most significant effect on the abundance of known metabolites. Extracts of several LCO-induced metabolic profiles significantly impact the growth rates of diverse bacterial species. These findings suggest that LCOs may play an important role in the competitive dynamics of non-plant-symbiotic fungi and bacteria. This study identifies specific metabolomic profiles induced by these ubiquitously produced chemicals and creates a foundation for future studies into the potential roles of LCOs as modulators of interkingdom competition.

Original language	English
Journal	mSystems
Volume	7
Issue number	6
DOIs	https://doi.org/10.1128/msystems.01052-22
State	Published - Dec 2022

Funding

This research was funded by the Genomic System Sciences Program, U.S. Department of Energy, Office of Science, Biological and Environmental Research, as part of the Plant-Microbe Interfaces Scientific Focus Area at Oak Ridge National Laboratory (ORNL; http://pmi.ornl.gov; ORNL is managed by UT-Battelle, LLC, for the U.S. Department of Energy under contract DEAC05-00OR22725). To perform the network-theoretic analysis, M.G.M. used the resources of the Oak Ridge Leadership Computing Facility at ORNL, which is supported by the DOE Office of Science under contract number DE-AC05-00OR22725.

Access to Document

10.1128/msystems.01052-22

Cite this

Rush, T. A., Tannous, J., Lane, M. J., Meena, M. G., Carrell, A. A., Golan, J. J., Drott, M. T., Cottaz, S., Fort, S., Ané, J. M., Keller, N. P., Pelletier, D. A., Jacobson, D. A., Kainer, D., Abraham, P. E., Giannone, R. J., & Labbé, J. L. (2022). Lipo-Chitooligosaccharides Induce Specialized Fungal Metabolite Profiles That Modulate Bacterial Growth. mSystems, 7(6). https://doi.org/10.1128/msystems.01052-22

@article{ad9f82ce6232456494a2c28558392463,

title = "Lipo-Chitooligosaccharides Induce Specialized Fungal Metabolite Profiles That Modulate Bacterial Growth",

abstract = "Lipo-chitooligosaccharides (LCOs) are historically known for their role as microbial-derived signaling molecules that shape plant symbiosis with beneficial rhizobia or mycorrhizal fungi. Recent studies showing that LCOs are widespread across the fungal kingdom have raised questions about the ecological function of these compounds in organisms that do not form symbiotic relationships with plants. To elucidate the ecological function of these compounds, we investigate the metabolomic response of the ubiquitous human pathogen Aspergillus fumigatus to LCOs. Our metabolomics data revealed that exogenous application of various types of LCOs to A. fumigatus resulted in significant shifts in the fungal metabolic profile, with marked changes in the production of specialized metabolites known to mediate ecological interactions. Using network analyses, we identify specific types of LCOs with the most significant effect on the abundance of known metabolites. Extracts of several LCO-induced metabolic profiles significantly impact the growth rates of diverse bacterial species. These findings suggest that LCOs may play an important role in the competitive dynamics of non-plant-symbiotic fungi and bacteria. This study identifies specific metabolomic profiles induced by these ubiquitously produced chemicals and creates a foundation for future studies into the potential roles of LCOs as modulators of interkingdom competition.",

author = "Rush, {Tom{\'a}s A.} and Joanna Tannous and Lane, {Matthew J.} and Meena, {Muralikrishnan Gopalakrishnan} and Carrell, {Alyssa A.} and Golan, {Jacob J.} and Drott, {Milton T.} and Sylvain Cottaz and S{\'e}bastien Fort and An{\'e}, {Jean Michel} and Keller, {Nancy P.} and Pelletier, {Dale A.} and Jacobson, {Daniel A.} and David Kainer and Abraham, {Paul E.} and Giannone, {Richard J.} and Labb{\'e}, {Jesse L.}",

year = "2022",

month = dec,

doi = "10.1128/msystems.01052-22",

language = "English",

volume = "7",

journal = "mSystems",

issn = "2379-5077",

publisher = "American Society for Microbiology",

number = "6",

}

Rush, TA, Tannous, J, Lane, MJ, Meena, MG , Carrell, AA, Golan, JJ, Drott, MT, Cottaz, S, Fort, S, Ané, JM, Keller, NP, Pelletier, DA , Jacobson, DA, Kainer, D, Abraham, PE , Giannone, RJ & Labbé, JL 2022, 'Lipo-Chitooligosaccharides Induce Specialized Fungal Metabolite Profiles That Modulate Bacterial Growth', mSystems, vol. 7, no. 6. https://doi.org/10.1128/msystems.01052-22

TY - JOUR

T1 - Lipo-Chitooligosaccharides Induce Specialized Fungal Metabolite Profiles That Modulate Bacterial Growth

AU - Rush, Tomás A.

AU - Tannous, Joanna

AU - Lane, Matthew J.

AU - Meena, Muralikrishnan Gopalakrishnan

AU - Carrell, Alyssa A.

AU - Golan, Jacob J.

AU - Drott, Milton T.

AU - Cottaz, Sylvain

AU - Fort, Sébastien

AU - Ané, Jean Michel

AU - Keller, Nancy P.

AU - Pelletier, Dale A.

AU - Jacobson, Daniel A.

AU - Kainer, David

AU - Abraham, Paul E.

AU - Giannone, Richard J.

AU - Labbé, Jesse L.

PY - 2022/12

Y1 - 2022/12

N2 - Lipo-chitooligosaccharides (LCOs) are historically known for their role as microbial-derived signaling molecules that shape plant symbiosis with beneficial rhizobia or mycorrhizal fungi. Recent studies showing that LCOs are widespread across the fungal kingdom have raised questions about the ecological function of these compounds in organisms that do not form symbiotic relationships with plants. To elucidate the ecological function of these compounds, we investigate the metabolomic response of the ubiquitous human pathogen Aspergillus fumigatus to LCOs. Our metabolomics data revealed that exogenous application of various types of LCOs to A. fumigatus resulted in significant shifts in the fungal metabolic profile, with marked changes in the production of specialized metabolites known to mediate ecological interactions. Using network analyses, we identify specific types of LCOs with the most significant effect on the abundance of known metabolites. Extracts of several LCO-induced metabolic profiles significantly impact the growth rates of diverse bacterial species. These findings suggest that LCOs may play an important role in the competitive dynamics of non-plant-symbiotic fungi and bacteria. This study identifies specific metabolomic profiles induced by these ubiquitously produced chemicals and creates a foundation for future studies into the potential roles of LCOs as modulators of interkingdom competition.

AB - Lipo-chitooligosaccharides (LCOs) are historically known for their role as microbial-derived signaling molecules that shape plant symbiosis with beneficial rhizobia or mycorrhizal fungi. Recent studies showing that LCOs are widespread across the fungal kingdom have raised questions about the ecological function of these compounds in organisms that do not form symbiotic relationships with plants. To elucidate the ecological function of these compounds, we investigate the metabolomic response of the ubiquitous human pathogen Aspergillus fumigatus to LCOs. Our metabolomics data revealed that exogenous application of various types of LCOs to A. fumigatus resulted in significant shifts in the fungal metabolic profile, with marked changes in the production of specialized metabolites known to mediate ecological interactions. Using network analyses, we identify specific types of LCOs with the most significant effect on the abundance of known metabolites. Extracts of several LCO-induced metabolic profiles significantly impact the growth rates of diverse bacterial species. These findings suggest that LCOs may play an important role in the competitive dynamics of non-plant-symbiotic fungi and bacteria. This study identifies specific metabolomic profiles induced by these ubiquitously produced chemicals and creates a foundation for future studies into the potential roles of LCOs as modulators of interkingdom competition.

UR - http://www.scopus.com/inward/record.url?scp=85144396828&partnerID=8YFLogxK

U2 - 10.1128/msystems.01052-22

DO - 10.1128/msystems.01052-22

M3 - Article

C2 - 36453934

AN - SCOPUS:85144396828

SN - 2379-5077

VL - 7

JO - mSystems

JF - mSystems

IS - 6

ER -

Lipo-Chitooligosaccharides Induce Specialized Fungal Metabolite Profiles That Modulate Bacterial Growth

Abstract

Funding

Access to Document

Other files and links

Fingerprint

Cite this