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.

Habitat‐adapted microbial communities mediate Sphagnum peatmoss resilience to warming

“…In addition to N metabolism, recent studies have identified a role for sulfur exchange within feathermossand Sphagnumcyanobacterial symbioses (Warshan et al, 2017;Stuart et al, 2020;Carrell et al, 2021). For example, Stuart et al (2020) found that targeted mutatgenesis of the cyanobacterial alkane sulfonate monooxygenase resulted in an inability to colonize feathermoss.…”

“…For example, Stuart et al (2020) found that targeted mutatgenesis of the cyanobacterial alkane sulfonate monooxygenase resulted in an inability to colonize feathermoss. In addition, Carrell et al (2021) used metabolic cross-feeding and spatial metabolite profiling to discover that Sphagnum provided sulfur-rich choline-O-sulfate, taurine and sulfoacetate, which were subsequently depleted by the Nostoc symbiont. Within the current study, the warm-microbiome showed enrichment for bacterially related sulfur metabolism regardless of treatment temperature.…”

“…In addition to N metabolism, recent studies have identified a role for sulfur exchange within feathermoss – and Sphagnum – cyanobacterial symbioses (Warshan et al ., 2017; Stuart et al ., 2020; Carrell et al ., 2021). For example, Stuart et al .…”

Biotic and abiotic controls of nitrogen fixation in cyanobacteria–moss associations

“…What the cyanobacteria gain remains even more elusive. It could be protection from desiccation and predation, and/or supply of a C source – as N 2 fixation is an energy costly process (Stuart et al ., 2020; Carrell et al ., 2022). However, cyanobacterial photosynthesis is not downregulated when associating with a moss host (Warshan et al ., 2017).…”

Viral infections mediate microbial controls on ecosystem responses to global warming

“…While Sphagnum plays a primary role in carbon dynamics (Slate, Sullivan and Callaway 2019), it serves a secondary role by insulating permafrost, thus dampening the impacts of rising temperatures on vast amounts of carbon stored in the arctic tundra (Camill and Clark 1998). Peatland microbial food webs are uniquely well-suited systems for studying ecosystem responses to global change due to 1) their net impact on the global carbon cycle (Gorham 1991;Dorrepaal et al 2009;Yu et al 2010;Bu et al 2011), 2) the functional diversity of their constituent microbial taxa (Gilbert et al 1998;Trap et al 2016;Geisen et al 2018;Thakur and Geisen 2019), 3) their vulnerability to changes in temperature (Richardson et al 2018;Norby et al 2019;Geisen et al 2021), and 4) the ability to grow and study Sphagnum moss and associated microbial communities in the laboratory (Altermatt et al 2015;Geisen et al 2018;Carrell et al 2019Carrell et al , 2022b) Doing so, however, will require a multifaceted approachincluding characterization of microbial communities in the field, microbial experiments in the laboratory, -omics approaches, and mathematical modeling (Singh et al 2010;Geisen et al 2017), all of which can benefit from cross-scale integration.…”