Abstract
Sphagnum mosses mediate long-term carbon accumulation in peatlands. Given their functional role as keystone species, it is important to consider their responses to ecological gradients and environmental changes through the production of phenolics. We compared the extent to which Sphagnum phenolic production was dependent on species, microhabitats and season, and how surrounding dwarf shrubs responded to Sphagnum phenolics. We evaluated the phenolic profiles of aqueous extracts of Sphagnum fallax and Sphagnum magellanicum over a 6-month period in two microhabitats (wet lawns versus dry hummocks) in a French peatland. Phenolic profiles of water-soluble extracts were measured by UHPLC-QTOF-MS. Andromeda polifolia mycorrhizal colonization was quantified by assessing the intensity of global root cortex colonization. Phenolic profiles of both Sphagnum mosses were species-, season- and microhabitat- dependant. Sphagnum-derived acids were the phenolics mostly recovered; relative quantities were 2.5-fold higher in S. fallax than in S. magellanicum. Microtopography and vascular plant cover strongly influenced phenolic profiles, especially for minor metabolites present in low abundance. Higher mycorrhizal colonization of A. polifolia was found in lawns as compared to hummocks. Mycorrhizal abundance, in contrast to environmental parameters, was correlated with production of minor phenolics in S. fallax. Our results highlight the close interaction between mycorrhizae such as those colonizing A. polifolia and the release of Sphagnum phenolic metabolites and suggest that Sphagnum-derived acids and minor phenolics play different roles in this interaction. This work provides new insight into the ecological role of Sphagnum phenolics by proposing a strong association with mycorrhizal colonization of shrubs.
Similar content being viewed by others
References
Appel HM, Governo HL, Siska E, Schultz JC (2001) Limitations of Folin assays of foliar phenolics in ecological studies. J Chem Ecol 27:761–778
Arndal MF, Merrild MP, Michelsen A, Schmidt IK, Mikkelsen TN, Beier C (2013) Net growth and nutrient acquisition in response to predicted climate change in two contrasting heathland species. Plant Soil 369:615–629
Asplund J, Bokhorst S, Wardle DA (2013) Secondary compounds can reduce the soil micro-arthropod effect on lichen decomposition. Soil Biol Biochem 66:10–16
Binet P, Rouifed S, Jassey VEJ, Toussaint ML, Chiapusio G (2017) Experimental climate warming alters the relationship between fungal root symbiosis and Sphagnum litter phenolics in two peatland microhabitats. Soil Biol Biochem 105:153–161
Braggazza L, Freeman C (2007) High nitrogen availability reduces polyphenol content in Sphagnum peat. Sci Total Environ 377:439–343
Buttler A, Robroek BM, Laggoun-Defarge F, Jassey VEJ, Pochelon C, Bernard G, Delarue F, Gogo S, Mariotte P, Mitchell EAD, Bragazza L (2015) Experimental warming interacts with soil moisture to discriminate plant responses in an ombrotrophic peatland. J Veg Sci 26:964–974
Chiapusio G, Jassey V, Hussain MI, Binet P (2013) Evidences of bryophyte allelochemical interactions: the case of Sphagnum. In: Cheema ZA, Faroq M, Wahid A (eds) Allelopathy: Current trends and future applications. Springer, Verlag Berlin, pp 39–54
Cipollini D, Rigsby CM, Barto EK (2012) Microbes as targets and mediators of allelopathy in plants. J Chem Ecol 38:714–727
Delarue F, Laggoun-Défarge F, Buttler A, Gogo S, Jassey VEJ, Disnar JR (2011) Effects of short-term ecosystem experimental warming on water-extractable organic matter in an ombrotrophic Sphagnum peatland (Le Forbonnet, France). Org Geochem 42:1016–1024
Dieleman CM, Branfireun BA, McLaughlin JW, Lindo Z (2016) Enhanced carbon release under future climate conditions in a peatland mesocosm experiment: the role of phenolic compounds. Plant Soil 400:81–91
Dray S, Dufour AB (2007) The ade4 package: implementing the duality diagram for ecologists. J Stat Softw 22:1–20
Fenner N, Freeman C (2011) Drought-induced carbon loss in peatlands. Nat Geosci 4:895–900
Finlay RD (2008) Ecological aspects of mycorrhizal symbiosis: with special emphasis on the functional diversity of interactions involving the extraradical mycelium. J Exp Bot 59:1115–1126
Grace JB, Anderson TM, Olff H, Scheiner SM (2010) On the specification of structural equation models for ecological systems. Ecol Monogr 80:67–87
Grace JB, Schoolmaster DR Jr, Guntenspergen GR, Little AM, Mitchell BR, Miller KM, Schweiger EW (2012) Guidelines for a graph-theoretic implementation of structural equation modeling. Ecosphere 3(1–44):73. https://doi.org/10.1890/ES12-00048.1
Grace JB, Adler PB, Harpole WS, Borer ET, Seabloom EW (2014) Causal networks clarify productivity–richness interrelations, bivariate plots do not. Funct Ecol 28:787–798
Hájek T, Vicherová E (2014) Desiccation tolerance of Sphagnum revisited: a puzzle resolved. Plant Biol 16:765–773
Iason GR, Dick M, Hartley SE (2012) The integrative roles of plant secondary metabolites in natural systems: a synthesis. In: Iason GR, Dicke M, Hartley SE (eds) The ecology of plant secondary metabolites: from genes to global processes. Cambridge University Press, Cambridge, pp 1–9
Jacquemard AL (1998) Andromeda polifolia L. J Ecol 86:527–541
Jassey VEJ, Chiapusio G, Mitchell EAD, Binet P, Toussaint ML, Gilbert D (2011a) Fine-scale horizontal and vertical micro-distribution patterns of testate amoebae along a narrow fen/bog gradient. Microb Ecol 61:374–385
Jassey VEJ, Chiapusio G, Gilbert D, Buttler A, Toussaint ML, Binet P (2011b) Experimental climate effect on seasonal variability of polyphenol/phenoloxidase interplay along a narrow fen-bog ecological gradient. Glob Chang Biol 17:2945–2957
Jassey VEJ, Chiapusio G, Binet P, Buttler A, Laggoun Défarge F, Delarue F, Bernard N, Mitchell EAD, Toussaint ML, Francez AJ, Gilbert D (2013) Above- and belowground linkages in Sphagnum peatland:climate warming affects plant-microbial interactions. Glob Chang Biol 19:811–823
Johnson N, Angelard C, Sanders I, Kiers EK (2013) Predicting community and ecosystem outcomes of mycorrhizal responses to global change. Ecol Lett 16:140–153
Koske RE, Gemma JN (1989) A modified procedure for staining roots to detect VA-mycorrhizas. Mycol Res 92:486–505
Latif S, Chiapusio G, Weston LA (2017) Allelopathy and the role of Allelochemicals in plant defence. In: G Becard (ed) How plants communicate with their biotic environment. Adv Bot Res 82:19–54
Legendre P, Gallagher ED (2001) Ecologically meaningful transformations for ordination of species data. Oecologia 129:271–280
Limpens J, Bohlin E, Nilsson MD (2017) Phylogenic or environmental control on the elemental and organo-chemical composition of Sphagnum mosses ? Plant Soil 417:69–85
Michel P, Burritt DJ, Lee WG (2011) Bryophytes display allelopathic interactions with tree species in native forest ecosystem. Oikos 120:1272–1280
Oksanen J (2011) Multivariate analysis of ecological communities in R: vegan tutorial. R Package Version
Olsrud M, Melillo JM, Michelsen A, Wallander H, Olsson PA (2004) Response or ericoid mycorrhizal colonization and functioning to global change factors. New Phytol 162:459–469
Opelt K, Chobot V, Hadacek F, Schonmann S, Eberl L, Berg G (2007) Investigations of the structure and function of bacterial communities associated with Sphagnum mosses. Environ Microbiol 9:2795–2809
Pinheiro JC, Bates DM (2000) Mixed-effects models in S and S-PLUS. Springer, New York
R Development Core Team (2013) R: a language and environment for statistical computing. R Foundation for statistical computing, Vienna, Austria. ISBN 3-900051-00-3. http://www.R-project.org
Rasmussen S, Wolff C, Rudolph H (1995) Compartmentalization of phenolic constituents in sphagnum. Phytochemistry 38:35–39
Read DJ, Leake JR, Perez-Moreno J (2004) Mycorrhizal fungi as drivers of ecosystem processes in heathland and boreal forest biomes. Can J Bot 82:1243–1263
Renault H, Alber A, Horst NA, Basilio Lopes A, Fich EA, Kriegshauser L, Wiedemann G, Ullmann P, Herrgott L, Erhardt M, Pineau E, Ehlting J, Schmitt M, Rose JKC, Reski R, Werck-Reichhart D (2017) A phenol-enriched cuticle is ancestral to lignin evolution in land plants. Nat Commun 8. https://doi.org/10.1038/ncomms14713
Rudolph H, Samland (1985) Occurrence and metabolism of sphagnum acid in the cell wall of bryophytes. Phytochemistry 24:745–749
Skoneczny D, Weston PA, Weston LA (2018) Metabolomics and metabolic profiling – investigation of dynamic plant-environment interactions at the functional level. In: Reigosa MJ, Sanchez AM (eds) Advances in plant ecophysiology techniques, 1st edn. Springer, Verlag Berlin, pp 375–400
Slack NG (2011) The ecological value of Bryophytes as indicators of climate change. In: Tuban Z, Slack NG, Stark LR (eds) Bryophyte Ecology and climate change. Cambridge University Press, Cambridge, pp 5–12
Smith SE, Read DJ (2008) Mycorrhizal symbiosis. Academic Press, New York
Soudzilovskaia NA, Graae BJ, Douma JC, Grau O, Milbau A, Shevtsova A (2011) How do bryophytes govern generative recruitment of vascular plants? New Phytol 190:1019–1031
Tan BC, Pocs T (2000) Bryogeography and conservation of bryophytes. In: Shaw AJ, Goffinet B (eds) Bryophyte biology. Cambridge University Press, Cambridge, pp 403–448
Trouvelot A, Kough JL, Gianinazzi-Pearson V (1985) Mesure du taux de mycorhization VA d'un système radiculaire. Recherche de méthodes d'estimation ayant Une signification fonctionnelle. Physiological and genetical aspects of mycorrhizae, Proceedings of the 1st European Symposium on Mycorrhizae, INRA, Paris, pp 217–221
Van Breemen N (1995) How Sphagnum bogs down other plants. Trends Ecol Evol 10:270–275
Van der Putten WH, Bardgett RD, Bever JD, Bezemer TM, Casper BB, Fukami T, Kardoi P, Klironomos JN, Kulmatiski A, Schweitzer JA, Suding KN, Van de Voorde TFJ, Wardle DA (2013) Plant-soil feedbacks : the past, the present and the futures challenges. J Ecol 101:265–276
Wang H, Richardson CJ, Ho M (2015) Dual controls on carbon loss during drought in peatlands. Nat Clim Chang 5:584–587
Weng JK, Chapple C (2010) The origin and evolution of lignin biosynthesis. New Phytol 187:273–285
Weston LA, Skoneczny D, Weston PA, Weidenhamer JD (2015) Metabolic profiling: an overview – new approaches for the detection and functional analysis of biologically active secondary plant products. J Allelelochemical Interactions 2:15–27
Weston DJ, Turetsky MR, Johnson MG, Granath G, Lindo Z, Belyea LR, Rice SK, Hanson DT, Engelhardt KAM,Schmutz J, Dorrepaal E, Euskirchen ES, Stenøien HK, Szövényi P, Jackson M, Piatkowski BT, Muchero W, Norby RJ, Kostka JE, Glass JB, Rydin H, Limpens J, Tuittila ES, Ullrich KK, Carrell A, Benscoter BW, Chen JG, Oke TA, Nilsson MB, Ranjan P, Jacobson D, Lilleskov EA, Clymo RS, Shaw AJ (2018) The Sphagnome project: enabling ecological and evolutionary insights through a genus-level sequencing project. New Phytol 217(1):16–25
Wilschke J, Sprengel B, Wolff C, Rudolph H (1989) A hydroxybutenolide from Sphagnum species. Phytochemistry 28:1725–1727
Zeng RS (2014) Allelopathy: the solution is indirect. J Chem Ecol 40:515–516
Acknowledgements
This research was supported by the French National Agency for the ANR PeatWarm project (ANR-07-VUL-010) and the Pays Montbéliard Agglomération (France) and Nathalie Islam-Frénoy (Translator, University Hospital of Besançon, France) for her fruitful comments on the manuscript and English edits.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Chiapusio, G., Jassey, V.E.J., Bellvert, F. et al. Sphagnum Species Modulate their Phenolic Profiles and Mycorrhizal Colonization of Surrounding Andromeda polifolia along Peatland Microhabitats. J Chem Ecol 44, 1146–1157 (2018). https://doi.org/10.1007/s10886-018-1023-4
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10886-018-1023-4