Novel metabolic interactions and environmental conditions mediate the boreal peatmoss-cyanobacteria mutualism

Alyssa A. Carrell; Dušan Veličković; Travis J. Lawrence; Benjamin P. Bowen; Katherine B. Louie; Dana L. Carper; Rosalie K. Chu; Hugh D. Mitchell; Galya Orr; Lye Meng Markillie; Sara S. Jawdy; Jane Grimwood; A. Jonathan Shaw; Jeremy Schmutz; Trent R. Northen; Christopher R. Anderton; Dale A. Pelletier; David J. Weston

doi:10.1038/s41396-021-01136-0

Novel metabolic interactions and environmental conditions mediate the boreal peatmoss-cyanobacteria mutualism

Alyssa A. Carrell, Dušan Veličković, Travis J. Lawrence, Benjamin P. Bowen, Katherine B. Louie, Dana L. Carper, Rosalie K. Chu, Hugh D. Mitchell, Galya Orr, Lye Meng Markillie, Sara S. Jawdy, Jane Grimwood, A. Jonathan Shaw, Jeremy Schmutz, Trent R. Northen, Christopher R. Anderton, Dale A. Pelletier, David J. Weston

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27 Scopus citations

Abstract

Interactions between Sphagnum (peat moss) and cyanobacteria play critical roles in terrestrial carbon and nitrogen cycling processes. Knowledge of the metabolites exchanged, the physiological processes involved, and the environmental conditions allowing the formation of symbiosis is important for a better understanding of the mechanisms underlying these interactions. In this study, we used a cross-feeding approach with spatially resolved metabolite profiling and metatranscriptomics to characterize the symbiosis between Sphagnum and Nostoc cyanobacteria. A pH gradient study revealed that the Sphagnum–Nostoc symbiosis was driven by pH, with mutualism occurring only at low pH. Metabolic cross-feeding studies along with spatially resolved matrix-assisted laser desorption/ionization mass spectrometry imaging (MALDI-MSI) identified trehalose as the main carbohydrate source released by Sphagnum, which were depleted by Nostoc along with sulfur-containing choline-O-sulfate, taurine and sulfoacetate. In exchange, Nostoc increased exudation of purines and amino acids. Metatranscriptome analysis indicated that Sphagnum host defense was downregulated when in direct contact with the Nostoc symbiont, but not as a result of chemical contact alone. The observations in this study elucidated environmental, metabolic, and physiological underpinnings of the widespread plant–cyanobacterial symbioses with important implications for predicting carbon and nitrogen cycling in peatland ecosystems as well as the basis of general host-microbe interactions.

Original language	English
Pages (from-to)	1074-1085
Number of pages	12
Journal	ISME Journal
Volume	16
Issue number	4
DOIs	https://doi.org/10.1038/s41396-021-01136-0
State	Published - Apr 2022

Funding

We thank the editor and anonymous reviewers for detailed and thoughtful comments that improved the manuscript. Collection of starting Sphagnum angustifolium was made possible through the SPRUCE project, which is supported by Office of Science; Biological and Environmental Research (BER); US Department of Energy (DOE), Grant/Award Number: DE-AC05–00OR22725. Experimentation, sample collection, and analyses were supported by the DOE BER Early Career Research Program. Oak Ridge National Laboratory is managed by UT-Battelle, LLC, for the US DOE under contract no DE-AC05–00OR22725. AJS was supported by NSF DEB-1737899, 1928514. A portion of this research was performed under the Facilities Integrating Collaborations for User Science (FICUS) program and used resources at the DOE Joint Genome Institute and the Environmental Molecular Sciences Laboratory (grid.436923.9), which are DOE Office of Science User Facilities. Both facilities are sponsored by the Biological and Environmental Research program and operated under Contract Nos. DE-AC02-05CH11231 (JGI) and DE-AC05-76RL01830 (EMSL). Figs. 2 and 8 were created with BioRender.com. We thank the editor and anonymous reviewers for detailed and thoughtful comments that improved the manuscript. Collection of starting Sphagnum angustifolium was made possible through the SPRUCE project, which is supported by Office of Science; Biological and Environmental Research (BER); US Department of Energy (DOE), Grant/Award Number: DE-AC05–00OR22725. Experimentation, sample collection, and analyses were supported by the DOE BER Early Career Research Program. Oak Ridge National Laboratory is managed by UT-Battelle, LLC, for the US DOE under contract no DE-AC05–00OR22725. AJS was supported by NSF DEB-1737899, 1928514. A portion of this research was performed under the Facilities Integrating Collaborations for User Science (FICUS) program and used resources at the DOE Joint Genome Institute and the Environmental Molecular Sciences Laboratory (grid.436923.9), which are DOE Office of Science User Facilities. Both facilities are sponsored by the Biological and Environmental Research program and operated under Contract Nos. DE-AC02-05CH11231 (JGI) and DE-AC05-76RL01830 (EMSL). Figs. 2 and 8 were created with BioRender.com. The authors declare that they have no conflict of interests. This manuscript has been authored by UT-Battelle, LLC under Contract No. DE-AC05-00OR22725 with the U.S. Department of Energy. The United States Government retains and the publisher, by accepting the article for publication, acknowledges that the United States Government retains a non-exclusive, paid-up, irrevocable, world-wide license to publish or reproduce the published form of this manuscript, or allow others to do so, for United States Government purposes. The Department of Energy will provide public access to these results of federally sponsored research in accordance with the DOE Public Access Plan (http://energy.gov/downloads/doe-public-access-plan).

Funders	Funder number
DOE BER
National Science Foundation	DE-AC02-05CH11231, 1928514, DE-AC05-76RL01830, DEB-1737899
U.S. Department of Energy	DE-AC05–00OR22725
Office of Science
Biological and Environmental Research
Oak Ridge National Laboratory
Joint Genome Institute

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Carrell, A. A., Veličković, D., Lawrence, T. J., Bowen, B. P., Louie, K. B., Carper, D. L., Chu, R. K., Mitchell, H. D., Orr, G., Markillie, L. M., Jawdy, S. S., Grimwood, J., Shaw, A. J., Schmutz, J., Northen, T. R., Anderton, C. R., Pelletier, D. A., & Weston, D. J. (2022). Novel metabolic interactions and environmental conditions mediate the boreal peatmoss-cyanobacteria mutualism. ISME Journal, 16(4), 1074-1085. https://doi.org/10.1038/s41396-021-01136-0

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title = "Novel metabolic interactions and environmental conditions mediate the boreal peatmoss-cyanobacteria mutualism",

abstract = "Interactions between Sphagnum (peat moss) and cyanobacteria play critical roles in terrestrial carbon and nitrogen cycling processes. Knowledge of the metabolites exchanged, the physiological processes involved, and the environmental conditions allowing the formation of symbiosis is important for a better understanding of the mechanisms underlying these interactions. In this study, we used a cross-feeding approach with spatially resolved metabolite profiling and metatranscriptomics to characterize the symbiosis between Sphagnum and Nostoc cyanobacteria. A pH gradient study revealed that the Sphagnum–Nostoc symbiosis was driven by pH, with mutualism occurring only at low pH. Metabolic cross-feeding studies along with spatially resolved matrix-assisted laser desorption/ionization mass spectrometry imaging (MALDI-MSI) identified trehalose as the main carbohydrate source released by Sphagnum, which were depleted by Nostoc along with sulfur-containing choline-O-sulfate, taurine and sulfoacetate. In exchange, Nostoc increased exudation of purines and amino acids. Metatranscriptome analysis indicated that Sphagnum host defense was downregulated when in direct contact with the Nostoc symbiont, but not as a result of chemical contact alone. The observations in this study elucidated environmental, metabolic, and physiological underpinnings of the widespread plant–cyanobacterial symbioses with important implications for predicting carbon and nitrogen cycling in peatland ecosystems as well as the basis of general host-microbe interactions.",

author = "Carrell, {Alyssa A.} and Du{\v s}an Veli{\v c}kovi{\'c} and Lawrence, {Travis J.} and Bowen, {Benjamin P.} and Louie, {Katherine B.} and Carper, {Dana L.} and Chu, {Rosalie K.} and Mitchell, {Hugh D.} and Galya Orr and Markillie, {Lye Meng} and Jawdy, {Sara S.} and Jane Grimwood and Shaw, {A. Jonathan} and Jeremy Schmutz and Northen, {Trent R.} and Anderton, {Christopher R.} and Pelletier, {Dale A.} and Weston, {David J.}",

note = "Publisher Copyright: {\textcopyright} 2021, UT-Battelle, LLC.",

year = "2022",

month = apr,

doi = "10.1038/s41396-021-01136-0",

language = "English",

volume = "16",

pages = "1074--1085",

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Carrell, AA, Veličković, D, Lawrence, TJ, Bowen, BP, Louie, KB, Carper, DL, Chu, RK, Mitchell, HD, Orr, G, Markillie, LM, Jawdy, SS, Grimwood, J, Shaw, AJ, Schmutz, J, Northen, TR, Anderton, CR, Pelletier, DA & Weston, DJ 2022, 'Novel metabolic interactions and environmental conditions mediate the boreal peatmoss-cyanobacteria mutualism', ISME Journal, vol. 16, no. 4, pp. 1074-1085. https://doi.org/10.1038/s41396-021-01136-0

TY - JOUR

T1 - Novel metabolic interactions and environmental conditions mediate the boreal peatmoss-cyanobacteria mutualism

AU - Carrell, Alyssa A.

AU - Veličković, Dušan

AU - Lawrence, Travis J.

AU - Bowen, Benjamin P.

AU - Louie, Katherine B.

AU - Carper, Dana L.

AU - Chu, Rosalie K.

AU - Mitchell, Hugh D.

AU - Orr, Galya

AU - Markillie, Lye Meng

AU - Jawdy, Sara S.

AU - Grimwood, Jane

AU - Shaw, A. Jonathan

AU - Schmutz, Jeremy

AU - Northen, Trent R.

AU - Anderton, Christopher R.

AU - Pelletier, Dale A.

AU - Weston, David J.

PY - 2022/4

Y1 - 2022/4

N2 - Interactions between Sphagnum (peat moss) and cyanobacteria play critical roles in terrestrial carbon and nitrogen cycling processes. Knowledge of the metabolites exchanged, the physiological processes involved, and the environmental conditions allowing the formation of symbiosis is important for a better understanding of the mechanisms underlying these interactions. In this study, we used a cross-feeding approach with spatially resolved metabolite profiling and metatranscriptomics to characterize the symbiosis between Sphagnum and Nostoc cyanobacteria. A pH gradient study revealed that the Sphagnum–Nostoc symbiosis was driven by pH, with mutualism occurring only at low pH. Metabolic cross-feeding studies along with spatially resolved matrix-assisted laser desorption/ionization mass spectrometry imaging (MALDI-MSI) identified trehalose as the main carbohydrate source released by Sphagnum, which were depleted by Nostoc along with sulfur-containing choline-O-sulfate, taurine and sulfoacetate. In exchange, Nostoc increased exudation of purines and amino acids. Metatranscriptome analysis indicated that Sphagnum host defense was downregulated when in direct contact with the Nostoc symbiont, but not as a result of chemical contact alone. The observations in this study elucidated environmental, metabolic, and physiological underpinnings of the widespread plant–cyanobacterial symbioses with important implications for predicting carbon and nitrogen cycling in peatland ecosystems as well as the basis of general host-microbe interactions.

AB - Interactions between Sphagnum (peat moss) and cyanobacteria play critical roles in terrestrial carbon and nitrogen cycling processes. Knowledge of the metabolites exchanged, the physiological processes involved, and the environmental conditions allowing the formation of symbiosis is important for a better understanding of the mechanisms underlying these interactions. In this study, we used a cross-feeding approach with spatially resolved metabolite profiling and metatranscriptomics to characterize the symbiosis between Sphagnum and Nostoc cyanobacteria. A pH gradient study revealed that the Sphagnum–Nostoc symbiosis was driven by pH, with mutualism occurring only at low pH. Metabolic cross-feeding studies along with spatially resolved matrix-assisted laser desorption/ionization mass spectrometry imaging (MALDI-MSI) identified trehalose as the main carbohydrate source released by Sphagnum, which were depleted by Nostoc along with sulfur-containing choline-O-sulfate, taurine and sulfoacetate. In exchange, Nostoc increased exudation of purines and amino acids. Metatranscriptome analysis indicated that Sphagnum host defense was downregulated when in direct contact with the Nostoc symbiont, but not as a result of chemical contact alone. The observations in this study elucidated environmental, metabolic, and physiological underpinnings of the widespread plant–cyanobacterial symbioses with important implications for predicting carbon and nitrogen cycling in peatland ecosystems as well as the basis of general host-microbe interactions.

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Novel metabolic interactions and environmental conditions mediate the boreal peatmoss-cyanobacteria mutualism

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