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

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

doi:10.1038/s41396-021-01136-0

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

Journal Article · Sun Nov 28 23:00:00 EST 2021 · The ISME Journal

DOI:https://doi.org/10.1038/s41396-021-01136-0· OSTI ID:1832954

; Veličković, Dušan; Lawrence, Travis J.; ; Louie, Katherine B.; Carper, Dana L.; ; Mitchell, Hugh D.; Orr, Galya; ; Jawdy, Sara S.; Grimwood, Jane; Shaw, A. Jonathan; ; ; ; ;

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.

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Sponsoring Organization:: USDOE

OSTI ID:: 1832954

Alternate ID(s):: OSTI ID: 1833955
OSTI ID: 1894634

Journal Information:: The ISME Journal, Journal Name: The ISME Journal Journal Issue: 4 Vol. 16; ISSN 1751-7362

Publisher:: Oxford University PressCopyright Statement

Country of Publication:: United Kingdom

Language:: English

References (59)

Pathways of assimilation and transfer of fixed nitrogen in coralloid roots of cycad-Nostoc symbioses Pate, J. S.; Lindblad, P.; Atkins, C. A. Planta, Vol. 176, Issue 4 https://doi.org/10.1007/BF00397652	journal	January 1988
To What Extent Do Food Preferences Explain the Trophic Position of Heterotrophic and Mixotrophic Microbial Consumers in a Sphagnum Peatland? Jassey, Vincent E. J.; Meyer, Caroline; Dupuy, Christine Microbial Ecology, Vol. 66, Issue 3 https://doi.org/10.1007/s00248-013-0262-8	journal	July 2013
Taurine Is a Major Carbon and Energy Source for Marine Prokaryotes in the North Atlantic Ocean off the Iberian Peninsula Clifford, Elisabeth L.; Varela, Marta M.; De Corte, Daniele Microbial Ecology, Vol. 78, Issue 2 https://doi.org/10.1007/s00248-019-01320-y	journal	January 2019
Symbiotic abilities of Sinorhizobium fredii with modified expression of purL Xie, Bo; Chen, Da-Song; Zhou, Kui Applied Microbiology and Biotechnology, Vol. 71, Issue 4 https://doi.org/10.1007/s00253-005-0186-4	journal	July 2006
Effects of the purL Gene Expression Level on the Competitive Nodulation Ability of Sinorhizobium fredii Xie, Bo; Chen, Dasong; Cheng, Guojun Current Microbiology, Vol. 59, Issue 2 https://doi.org/10.1007/s00284-009-9420-0	journal	May 2009
Allantoin: Emerging Role in Plant Abiotic Stress Tolerance Kaur, Harmeet; Chowrasia, Soni; Gaur, Vikram Singh Plant Molecular Biology Reporter, Vol. 39, Issue 3 https://doi.org/10.1007/s11105-021-01280-z	journal	January 2021
Proposed minimum reporting standards for chemical analysis: Chemical Analysis Working Group (CAWG) Metabolomics Standards Initiative (MSI) Sumner, Lloyd W.; Amberg, Alexander; Barrett, Dave Metabolomics, Vol. 3, Issue 3 https://doi.org/10.1007/s11306-007-0082-2	journal	September 2007
MapMan4: A Refined Protein Classification and Annotation Framework Applicable to Multi-Omics Data Analysis Schwacke, Rainer; Ponce-Soto, Gabriel Y.; Krause, Kirsten Molecular Plant, Vol. 12, Issue 6 https://doi.org/10.1016/j.molp.2019.01.003	journal	June 2019
Multimodal MSI in Conjunction with Broad Coverage Spatially Resolved MS ² Increases Confidence in Both Molecular Identification and Localization Veličković, Dušan; Chu, Rosalie K.; Carrell, Alyssa A. Analytical Chemistry, Vol. 90, Issue 1 https://doi.org/10.1021/acs.analchem.7b04319	journal	December 2017
Global peatland dynamics since the Last Glacial Maximum: GLOBAL PEATLANDS SINCE THE LGM Yu, Zicheng; Loisel, Julie; Brosseau, Daniel P. Geophysical Research Letters, Vol. 37, Issue 13 https://doi.org/10.1029/2010GL043584	journal	July 2010
Sphagnum mosses harbour highly specific bacterial diversity during their whole lifecycle Bragina, Anastasia; Berg, Christian; Cardinale, Massimiliano The ISME Journal, Vol. 6, Issue 4 https://doi.org/10.1038/ismej.2011.151	journal	November 2011
Purine biosynthesis-deficient Burkholderia mutants are incapable of symbiotic accommodation in the stinkbug Kim, Jiyeun Kate; Jang, Ho Am; Won, Yeo Jin The ISME Journal, Vol. 8, Issue 3 https://doi.org/10.1038/ismej.2013.168	journal	October 2013
Interaction and signalling between a cosmopolitan phytoplankton and associated bacteria Amin, S. A.; Hmelo, L. R.; van Tol, H. M. Nature, Vol. 522, Issue 7554 https://doi.org/10.1038/nature14488	journal	May 2015
Bidirectional C and N transfer and a potential role for sulfur in an epiphytic diazotrophic mutualism Stuart, Rhona K.; Pederson, Eric R. A.; Weyman, Philip D. The ISME Journal, Vol. 14, Issue 12 https://doi.org/10.1038/s41396-020-00738-4	journal	August 2020
Insights into functional bacterial diversity and its effects on Alpine bog ecosystem functioning Bragina, Anastasia; Berg, Christian; Müller, Henry Scientific Reports, Vol. 3, Issue 1 https://doi.org/10.1038/srep01955	journal	June 2013
Towards resolving the spatial metabolome with unambiguous molecular annotations in complex biological systems by coupling mass spectrometry imaging with structures for lossless ion manipulations Nagy, Gabe; Veličković, Dusan; Chu, Rosalie K. Chemical Communications, Vol. 55, Issue 3 https://doi.org/10.1039/C8CC07482H	journal	January 2019
Effect of trehalose on survival of Bradyrhizobium japonicum during desiccation Streeter, J. G. Journal of Applied Microbiology, Vol. 95, Issue 3 https://doi.org/10.1046/j.1365-2672.2003.02017.x	journal	September 2003
Calcareous groundwater raises bogs; the concept of ombrotrophy revisited Lamers, Leon P. M.; Farhoush, Cornelis; Van Groenendael, Jan M. Journal of Ecology, Vol. 87, Issue 4 https://doi.org/10.1046/j.1365-2745.1999.00380.x	journal	August 1999
Tansley Review No. 116: Cyanobacterium-plant symbioses Rai, A. N.; SÖDerbÄCk, E.; Bergman, B. New Phytologist, Vol. 147, Issue 3 https://doi.org/10.1046/j.1469-8137.2000.00720.x	journal	September 2000
Molecular Tools to Study Physcomitrella patens Frank, W.; Decker, E. L.; Reski, R. Plant Biology, Vol. 7, Issue 3 https://doi.org/10.1055/s-2005-865645	journal	May 2005
SPAdes: A New Genome Assembly Algorithm and Its Applications to Single-Cell Sequencing Bankevich, Anton; Nurk, Sergey; Antipov, Dmitry Journal of Computational Biology, Vol. 19, Issue 5 https://doi.org/10.1089/cmb.2012.0021	journal	May 2012
Biological nitrogen fixation in non-legume plants Santi, Carole; Bogusz, Didier; Franche, Claudine Annals of Botany, Vol. 111, Issue 5 https://doi.org/10.1093/aob/mct048	journal	March 2013
QUAST: quality assessment tool for genome assemblies Gurevich, Alexey; Saveliev, Vladislav; Vyahhi, Nikolay Bioinformatics, Vol. 29, Issue 8 https://doi.org/10.1093/bioinformatics/btt086	journal	February 2013
Prokka: rapid prokaryotic genome annotation Seemann, T. Bioinformatics, Vol. 30, Issue 14 https://doi.org/10.1093/bioinformatics/btu153	journal	March 2014
HTSeq--a Python framework to work with high-throughput sequencing data Anders, S.; Pyl, P. T.; Huber, W. Bioinformatics, Vol. 31, Issue 2 https://doi.org/10.1093/bioinformatics/btu638	journal	September 2014
Large-Scale Analysis of Gene Expression Profiles during Early Stages of Root Nodule Formation in a Model Legume, Lotus japonicus Kouchi, H. DNA Research, Vol. 11, Issue 4 https://doi.org/10.1093/dnares/11.4.263	journal	January 2004
Cyanobacteria-bryophyte symbioses Adams, D. G.; Duggan, P. S. Journal of Experimental Botany, Vol. 59, Issue 5 https://doi.org/10.1093/jxb/ern005	journal	February 2008
Genomic Changes Associated with the Evolutionary Transitions of Nostoc to a Plant Symbiont Warshan, Denis; Liaimer, Anton; Pederson, Eric Molecular Biology and Evolution, Vol. 35, Issue 5 https://doi.org/10.1093/molbev/msy029	journal	March 2018
HMMER web server: interactive sequence similarity searching Finn, R. D.; Clements, J.; Eddy, S. R. Nucleic Acids Research, Vol. 39, Issue suppl https://doi.org/10.1093/nar/gkr367	journal	May 2011
The Phenylalanine Ammonia Lyase Gene LjPAL1 Is Involved in Plant Defense Responses to Pathogens and Plays Diverse Roles in Lotus japonicus -Rhizobium Symbioses Chen, Yaping; Li, Fengjiao; Tian, Lu Molecular Plant-Microbe Interactions®, Vol. 30, Issue 9 https://doi.org/10.1094/MPMI-04-17-0080-R	journal	September 2017
Improvement of Drought Tolerance and Grain Yield in Common Bean by Overexpressing Trehalose-6-Phosphate Synthase in Rhizobia Suárez, Ramón; Wong, Arnoldo; Ramírez, Mario Molecular Plant-Microbe Interactions®, Vol. 21, Issue 7 https://doi.org/10.1094/MPMI-21-7-0958	journal	July 2008
Translocation in Legumes: Assimilates, Nutrients, and Signaling Molecules1 Atkins, Craig Anthony; Smith, Penelope Mary Collina Plant Physiology, Vol. 144, Issue 2 https://doi.org/10.1104/pp.107.098046	journal	June 2007
Functional Analysis of the Arabidopsis PAL Gene Family in Plant Growth, Development, and Response to Environmental Stress Huang, Junli; Gu, Min; Lai, Zhibing Plant Physiology, Vol. 153, Issue 4 https://doi.org/10.1104/pp.110.157370	journal	June 2010
Bryophyte-cyanobacteria associations as regulators of the northern latitude carbon balance in response to global change Lindo, Zoë; Nilsson, Marie-Charlotte; Gundale, Michael J. Global Change Biology, Vol. 19, Issue 7 https://doi.org/10.1111/gcb.12175	journal	March 2013
Experimental warming alters the community composition, diversity, and N ₂ fixation activity of peat moss ( Sphagnum fallax ) microbiomes Carrell, Alyssa A.; Kolton, Max; Glass, Jennifer B. Global Change Biology, Vol. 25, Issue 9 https://doi.org/10.1111/gcb.14715	journal	May 2019
Nitrogenase Activity in Relation to Intracellular Organisms in Sphagnum Mosses Granhall, Ulf; Hofsten, Angelica V. Physiologia Plantarum, Vol. 36, Issue 1 https://doi.org/10.1111/j.1399-3054.1976.tb05033.x	journal	January 1976
An assessment of photosynthetic downregulation in cyanobacteria from the Gunnera – Nostoc symbiosis Black, Kevin; Osborne, Bruce New Phytologist, Vol. 162, Issue 1 https://doi.org/10.1111/j.1469-8137.2004.01008.x	journal	February 2004
Provision of carbon skeletons for amide synthesis in non-nodulated soybean and pea roots in response to the source of nitrogen supply Ueda, Satoshi; Ikeda, Motoki; Yamakawa, Takeo Soil Science and Plant Nutrition, Vol. 54, Issue 5 https://doi.org/10.1111/j.1747-0765.2008.00293.x	journal	October 2008
Boreal feather mosses secrete chemical signals to gain nitrogen Bay, Guillaume; Nahar, Nurun; Oubre, Matthieu New Phytologist, Vol. 200, Issue 1 https://doi.org/10.1111/nph.12403	journal	June 2013
The Sphagnum microbiome: new insights from an ancient plant lineage Kostka, Joel E.; Weston, David J.; Glass, Jennifer B. New Phytologist, Vol. 211, Issue 1 https://doi.org/10.1111/nph.13993	journal	February 2016
Legumes Symbioses: Absence of Nod Genes in Photosynthetic Bradyrhizobia Giraud, Eric; Moulin, Lionel; Vallenet, David Science, Vol. 316, Issue 5829 https://doi.org/10.1126/science.1139548	journal	June 2007
Novel Mono-, Di-, and Trimethylornithine Membrane Lipids in Northern Wetland Planctomycetes Moore, Eli K.; Hopmans, Ellen C.; Rijpstra, W. Irene C. Applied and Environmental Microbiology, Vol. 79, Issue 22 https://doi.org/10.1128/AEM.02169-13	journal	August 2013
Functional Role of Bradyrhizobium japonicum Trehalose Biosynthesis and Metabolism Genes during Physiological Stress and Nodulation Sugawara, Masayuki; Cytryn, Eddie J.; Sadowsky, Michael J. Applied and Environmental Microbiology, Vol. 76, Issue 4 https://doi.org/10.1128/AEM.02483-09	journal	February 2010
Regulation of Cellular Differentiation in Filamentous Cyanobacteria in Free-Living and Plant-Associated Symbiotic Growth States Meeks, J. C.; Elhai, J. Microbiology and Molecular Biology Reviews, Vol. 66, Issue 1 https://doi.org/10.1128/MMBR.66.1.94-121.2002	journal	March 2002
Physiological and genetic responses of bacteria to osmotic stress Csonka, L. N. Microbiological Reviews, Vol. 53, Issue 1 https://doi.org/10.1128/mr.53.1.121-147.1989	journal	March 1989
Pyrimidine and Purine Biosynthesis and Degradation in Plants Zrenner, Rita; Stitt, Mark; Sonnewald, Uwe Annual Review of Plant Biology, Vol. 57, Issue 1 https://doi.org/10.1146/annurev.arplant.57.032905.105421	journal	June 2006
Trehalose Metabolism and Signaling Paul, Matthew J.; Primavesi, Lucia F.; Jhurreea, Deveraj Annual Review of Plant Biology, Vol. 59, Issue 1 https://doi.org/10.1146/annurev.arplant.59.032607.092945	journal	June 2008
Differential effects of environment on potato phenylpropanoid and carotenoid expression Payyavula, Raja S.; Navarre, Duroy A.; Kuhl, Joseph C. BMC Plant Biology, Vol. 12, Issue 1 https://doi.org/10.1186/1471-2229-12-39	journal	January 2012
Molecular Mechanisms of Persistence of Mutualistic Bacteria Photorhabdus in the Entomopathogenic Nematode Host An, Ruisheng; Grewal, Parwinder S. PLoS ONE, Vol. 5, Issue 10 https://doi.org/10.1371/journal.pone.0013154	journal	October 2010
Soil ph and its role in Cyanobacterial Abundance and Diversity in rice Field Soils Nayak, S. Applied Ecology and Environmental Research, Vol. 5, Issue 2 https://doi.org/10.15666/aeer/0502_103113	journal	November 2007
Nitrogen Fixation in a Subarctic Mire Granhall, Ulf; Selander, Hans Oikos, Vol. 24, Issue 1 https://doi.org/10.2307/3543247	journal	January 1973
Nitrogen Fixation in Wet Minerotrophic Moss Communities of a Subarctic Mire Basilier, Karl; Granhall, Ulf; Stenström, Thor-Axel Oikos, Vol. 31, Issue 2 https://doi.org/10.2307/3543568	journal	January 1978
Fixation and Uptake of Nitrogen in Sphagnum Blue-Green Algal Associations Basilier, Karl Oikos, Vol. 34, Issue 2 https://doi.org/10.2307/3544188	journal	January 1980
Stress-Induced Phenylpropanoid Metabolism Dixon, Richard A.; Paiva, Nancy L. The Plant Cell, Vol. 7, Issue 7 https://doi.org/10.2307/3870059	journal	July 1995
Trehalose Metabolism: From Osmoprotection to Signaling Iturriaga, Gabriel; Suárez, Ramón; Nova-Franco, Barbara International Journal of Molecular Sciences, Vol. 10, Issue 9 https://doi.org/10.3390/ijms10093793	journal	September 2009
Analysis of Metabolomics Datasets with High-Performance Computing and Metabolite Atlases Yao, Yushu; Sun, Terence; Wang, Tony Metabolites, Vol. 5, Issue 3 https://doi.org/10.3390/metabo5030431	journal	July 2015
Symbiosis revisited: phosphorus and acid buffering stimulate N₂ fixation but not Sphagnum growth van den Elzen, Eva; Kox, Martine A. R.; Harpenslager, Sarah F. Biogeosciences, Vol. 14, Issue 5 https://doi.org/10.5194/bg-14-1111-2017	journal	January 2017
Attaining whole-ecosystem warming using air and deep-soil heating methods with an elevated CO ₂ atmosphere Hanson, Paul J.; Riggs, Jeffery S.; Nettles, W. Robert Biogeosciences, Vol. 14, Issue 4 https://doi.org/10.5194/bg-14-861-2017	journal	January 2017
Transparent soil microcosms for live-cell imaging and non-destructive stable isotope probing of soil microorganisms Sharma, Kriti; Palatinszky, Márton; Nikolov, Georgi eLife, Vol. 9 https://doi.org/10.7554/eLife.56275	journal	November 2020

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