Sulfur speciation in Sphagnum peat moss modified by mutualistic interactions with cyanobacteria.

Peat moss (Sphagnum spp.) develops mutualistic interactions with cyanobacteria by providing carbohydrates and S compounds in exchange for N-rich compounds, potentially facilitating N inputs into peatlands. Here, we evaluate how colonization of Sphagnum angustifolium hyaline cells by Nostoc muscorum modifies S abundance and speciation at the scales of individual cells and across whole leaves. For the first time, S K-edge X-ray Absorption Spectroscopy was used to identify bulk and micron-scale S speciation across isolated cyanobacteria colonies, and in colonized and uncolonized leaves. Uncolonized leaves contained primarily reduced organic S and oxidized sulfonate- and sulfate-containing compounds. Increasing Nostoc colonization resulted in an enrichment of S and changes in speciation, with increases in sulfate relative to reduced S and sulfonate. At the scale of individual hyaline cells, colonized cells exhibited localized enrichment of reduced S surrounded by diffuse sulfonate, similar to observations of cyanobacteria colonies cultured in the absence of leaves. We infer that colonization stimulates plant S uptake and the production of sulfate-containing metabolites that are concentrated in stem tissues. Sulfate compounds that are produced in response to colonization become depleted in colonized cells where they may be converted into reduced S metabolites by cyanobacteria.

Variations in water economy traits in two Sphagnum species across their distribution boundaries.

PREMISE: We assessed changes in traits associated with water economy across climatic gradients in the ecologically similar peat mosses Sphagnum cuspidatum and Sphagnum lindbergii. These species have parapatric distributions in Europe and have similar niches in bogs. Sphagnum species of bogs are closely related, with a large degree of microhabitat niche overlap between many species that can be functionally very similar. Despite this, ecologically similar species do have different distributional ranges along climatic gradients that partly overlap. These gradients may favor particular Sphagnum traits, especially in relation to water economy, which can be hypothesized to drive species divergence by character displacement. METHODS: We investigated traits relevant for water economy of two parapatric bryophytes (Sphagnum cuspidatum and S. lindbergii) across the border of their distributional limits. We included both shoot traits and canopy traits, i.e., collective traits of the moss surface, quantified by photogrammetry. RESULTS: The two species are ecologically similar and occur at similar positions along the hydrological gradient in bogs. The biggest differences between the species were expressed in the variations of their canopy surfaces, particularly surface roughness and in the responses of important traits such as capitulum mass to climate. We did not find support for character displacement, because traits were not more dissimilar in sympatric than in allopatric populations. CONCLUSIONS: Our results suggest that parapatry within Sphagnum can be understood from just a few climatic variables and that climatic factors are stronger drivers than competition behind trait variation within these species of Sphagnum.

Linkages between Sphagnum metabolites and peatland CO2 uptake are sensitive to seasonality in warming trends.

Plants produce a wide diversity of metabolites. Yet, our understanding of how shifts in plant metabolites as a response to climate change feedback on ecosystem processes remains scarce. Here, we test to what extent climate warming shifts the seasonality of metabolites produced by Sphagnum mosses, and what are the consequences of these shifts for peatland C uptake. We used a reciprocal transplant experiment along a climate gradient in Europe to simulate climate change. We evaluated the responses of primary and secondary metabolites in five Sphagnum species and related their responses to gross ecosystem productivity (GEP). When transplanted to a warmer climate, Sphagnum species showed consistent responses to warming, with an upregulation of either their primary or secondary metabolite according to seasons. Moreover, these shifts were correlated to changes in GEP, especially in spring and autumn. Our results indicate that the Sphagnum metabolome is very plastic and sensitive to warming. We also show that warming-induced changes in the seasonality of Sphagnum metabolites have consequences on peatland GEP. Our findings demonstrate the capacity for plant metabolic plasticity to impact ecosystem C processes and reveal a further mechanism through which Sphagnum could shape peatland responses to climate change.

Habitat-adapted microbial communities mediate Sphagnum peatmoss resilience to warming.

Sphagnum peatmosses are fundamental members of peatland ecosystems, where they contribute to the uptake and long-term storage of atmospheric carbon. Warming threatens Sphagnum mosses and is known to alter the composition of their associated microbiome. Here, we use a microbiome transfer approach to test if microbiome thermal origin influences host plant thermotolerance. We leveraged an experimental whole-ecosystem warming study to collect field-grown Sphagnum, mechanically separate the associated microbiome and then transfer onto germ-free laboratory Sphagnum for temperature experiments. Host and microbiome dynamics were assessed with growth analysis, Chla fluorescence imaging, metagenomics, metatranscriptomics and 16S rDNA profiling. Microbiomes originating from warming field conditions imparted enhanced thermotolerance and growth recovery at elevated temperatures. Metagenome and metatranscriptome analyses revealed that warming altered microbial community structure in a manner that induced the plant heat shock response, especially the HSP70 family and jasmonic acid production. The heat shock response was induced even without warming treatment in the laboratory, suggesting that the warm-microbiome isolated from the field provided the host plant with thermal preconditioning. Our results demonstrate that microbes, which respond rapidly to temperature alterations, can play key roles in host plant growth response to rapidly changing environments.

Will climate change cause the global peatland to expand or contract? Evidence from the habitat shift pattern of Sphagnum mosses.

Peatlands play a crucial role in the global carbon cycle. Sphagnum mosses (peat mosses) are considered to be the peatland ecosystem engineers and contribute to the carbon accumulation in the peatland ecosystems. As cold-adapted species, the dominance of Sphagnum mosses in peatlands will be threatened by climate warming. The response of Sphagnum mosses to climate change is closely related to the future trajectory of carbon fluxes in peatlands. However, the impact of climate change on the habitat suitability of Sphagnum mosses on a global scale is poorly understood. To predict the potential impact of climate change on the global distribution of Sphagnum mosses, we used the MaxEnt model to predict the potential geographic distribution of six Sphagnum species that dominate peatlands in the future (2050 and 2070) under two greenhouse gas emission scenarios (SSP1-2.6 and SSP5-8.5). The results show that the mean temperature of the coldest quarter, precipitation of the driest month, and topsoil calcium carbonate are the main factors affecting the habitat availability of Sphagnum mosses. As the climate warms, Sphagnum mosses tend to migrate northward. The suitable habitat and abundance of Sphagnum mosses increase extensively in the high-latitude boreal peatland (north of 50°N) and decrease on a large scale beyond the high-latitude boreal peatland. The southern edge of boreal peatlands would experience the greatest decline in the suitable habitat and richness of Sphagnum mosses with the temperature rising and would be a risk area for the transition from carbon sink to carbon source. The spatial-temporal pattern changes of Sphagnum mosses simulated in this study provide a reference for the development of management and conservation strategies for Sphagnum bogs.

CO2 fertilization of Sphagnum peat mosses is modulated by water table level and other environmental factors.

Sphagnum mosses account for most accumulated dead organic matter in peatlands. Therefore, understanding their responses to increasing atmospheric CO2 is needed for estimating peatland C balances under climate change. A key process is photorespiration: a major determinant of net photosynthetic C assimilation that depends on the CO2 to O2 ratio. We used climate chambers to investigate photorespiratory responses of Sphagnum fuscum hummocks to recent increases in atmospheric CO2 (from 280 to 400 ppm) under different water table, temperature, and light intensity levels. We tested the photorespiratory variability using a novel method based on deuterium isotopomers (D6S /D6R ratio) of photosynthetic glucose. The effect of elevated CO2 on photorespiration was highly dependent on water table. At low water table (-20 cm), elevated CO2 suppressed photorespiration relative to C assimilation, thus substantially increasing the net primary production potential. In contrast, a high water table (~0 cm) favored photorespiration and abolished this CO2 effect. The response was further tested for Sphagnum majus lawns at typical water table levels (~0 and -7 cm), revealing no effect of CO2 under those conditions. Our results indicate that hummocks, which typically experience low water table levels, benefit from the 20th century's increase in atmospheric CO2 .

Development of a method for protonema proliferation of peat moss (Sphagnum squarrosum) through regeneration analysis.

The moss Sphagnum (peat moss) is ecologically and economically important. There is a paucity of physiological and developmental studies on Sphagnum because of the lack of an axenic culture system for its whole life cycle. A culture system has been established for the Sphagnum gametophore, but not the protonema (juvenile vegetative stage after spore germination). Therefore, the aim of this study was to develop a protonema culture system for Sphagnum. Sphagnum squarrosum gametophore tissue was disrupted and then cultured in liquid Knop medium. The regeneration of protonemata from the gametophore fragments was analyzed in detail by microscopy. We observed a developmental balance between filamentous and thalloid protonemata, and growth competition between the thalloid protonema and the gametophore. On the basis of these findings, we established a relatively stable peat moss protonema proliferation method. Using this method, all the developmental stages of peat moss vegetative growth could be obtained through differentiation or regeneration. The method can provide abundant homogeneous Sphagnum materials at desired stages for physiological and developmental studies, and will be useful for large-scale Sphagnum vegetative proliferation. The regeneration analysis method will be useful for establishing protonema proliferation systems for other mosses.

Range change evolution of peat mosses (Sphagnum) within and between climate zones.

Peat mosses (Sphagnum) hold exceptional importance in the control of global carbon fluxes and climate because of the vast stores of carbon bound up in partially decomposed biomass (peat). This study tests the hypothesis that the early diversification of Sphagnum was in the Northern Hemisphere, with subsequent range expansions to tropical latitudes and the Southern Hemisphere. A phylogenetic analysis of 192 accessions representing the moss class Sphagnopsida based on four plastid loci was conducted in conjunction with biogeographic analyses using BioGeoBEARS to investigate the tempo and mode of geographic range evolution. Analyses support the hypothesis that the major intrageneric clades of peat-forming species accounting for >90% of peat moss diversity originated and diversified at northern latitudes. The genus underwent multiple range expansions into tropical and Southern Hemisphere regions. Range evolution in peat mosses was most common within latitudinal zones, attesting to the relative difficulty of successfully invading new climate zones. Allopolyploidy in Sphagnum (inferred from microsatellite heterozygosity) does not appear to be biased with regard to geographic region nor intrageneric clade. The inference that Sphagnum diversified in cool-or cold-climate regions and repeatedly expanded its range into tropical regions makes the genus an excellent model for studying morphological, physiological, and genomic traits associated with adaptation to warming climates.

The Sphagnome Project: enabling ecological and evolutionary insights through a genus-level sequencing project.

Considerable progress has been made in ecological and evolutionary genetics with studies demonstrating how genes underlying plant and microbial traits can influence adaptation and even 'extend' to influence community structure and ecosystem level processes. Progress in this area is limited to model systems with deep genetic and genomic resources that often have negligible ecological impact or interest. Thus, important linkages between genetic adaptations and their consequences at organismal and ecological scales are often lacking. Here we introduce the Sphagnome Project, which incorporates genomics into a long-running history of Sphagnum research that has documented unparalleled contributions to peatland ecology, carbon sequestration, biogeochemistry, microbiome research, niche construction, and ecosystem engineering. The Sphagnome Project encompasses a genus-level sequencing effort that represents a new type of model system driven not only by genetic tractability, but by ecologically relevant questions and hypotheses.

The effects of quantitative fecundity in the haploid stage on reproductive success and diploid fitness in the aquatic peat moss Sphagnum macrophyllum.

A major question in evolutionary biology is how mating patterns affect the fitness of offspring. However, in animals and seed plants it is virtually impossible to investigate the effects of specific gamete genotypes. In bryophytes, haploid gametophytes grow via clonal propagation and produce millions of genetically identical gametes throughout a population. The main goal of this research was to test whether gamete identity has an effect on the fitness of their diploid offspring in a population of the aquatic peat moss Sphagnum macrophyllum. We observed a heavily male-biased sex ratio in gametophyte plants (ramets) and in multilocus microsatellite genotypes (genets). There was a steeper relationship between mating success (number of different haploid mates) and fecundity (number of diploid offspring) for male genets compared with female genets. At the sporophyte level, we observed a weak effect of inbreeding on offspring fitness, but no effect of brood size (number of sporophytes per maternal ramet). Instead, the identities of the haploid male and haploid female parents were significant contributors to variance in fitness of sporophyte offspring in the population. Our results suggest that intrasexual gametophyte/gamete competition may play a role in determining mating success in this population.

Sphagnum physiology in the context of changing climate: emergent influences of genomics, modelling and host-microbiome interactions on understanding ecosystem function.

Peatlands harbour more than one-third of terrestrial carbon leading to the argument that the bryophytes, as major components of peatland ecosystems, store more organic carbon in soils than any other collective plant taxa. Plants of the genus Sphagnum are important components of peatland ecosystems and are potentially vulnerable to changing climatic conditions. However, the response of Sphagnum to rising temperatures, elevated CO2 and shifts in local hydrology have yet to be fully characterized. In this review, we examine Sphagnum biology and ecology and explore the role of this group of keystone species and its associated microbiome in carbon and nitrogen cycling using literature review and model simulations. Several issues are highlighted including the consequences of a variable environment on plant-microbiome interactions, uncertainty associated with CO2 diffusion resistances and the relationship between fixed N and that partitioned to the photosynthetic apparatus. We note that the Sphagnum fallax genome is currently being sequenced and outline potential applications of population-level genomics and corresponding plant photosynthesis and microbial metabolic modelling techniques. We highlight Sphagnum as a model organism to explore ecosystem response to a changing climate and to define the role that Sphagnum can play at the intersection of physiology, genetics and functional genomics.

Climate change drives a shift in peatland ecosystem plant community: implications for ecosystem function and stability.

The composition of a peatland plant community has considerable effect on a range of ecosystem functions. Peatland plant community structure is predicted to change under future climate change, making the quantification of the direction and magnitude of this change a research priority. We subjected intact, replicated vegetated poor fen peat monoliths to elevated temperatures, increased atmospheric carbon dioxide (CO2 ), and two water table levels in a factorial design to determine the individual and synergistic effects of climate change factors on the poor fen plant community composition. We identify three indicators of a regime shift occurring in our experimental poor fen system under climate change: nonlinear decline of Sphagnum at temperatures 8 °C above ambient conditions, concomitant increases in Carex spp. at temperatures 4 °C above ambient conditions suggesting a weakening of Sphagnum feedbacks on peat accumulation, and increased variance of the plant community composition and pore water pH through time. A temperature increase of +4 °C appeared to be a threshold for increased vascular plant abundance; however the magnitude of change was species dependent. Elevated temperature combined with elevated CO2 had a synergistic effect on large graminoid species abundance, with a 15 times increase as compared to control conditions. Community analyses suggested that the balance between dominant plant species was tipped from Sphagnum to a graminoid-dominated system by the combination of climate change factors. Our findings indicate that changes in peatland plant community composition are likely under future climate change conditions, with a demonstrated shift toward a dominance of graminoid species in poor fens.

Evapotranspiration of tropical peat swamp forests.

In Southeast Asia, peatland is widely distributed and has accumulated a massive amount of soil carbon, coexisting with peat swamp forest (PSF). The peatland, however, has been rapidly degraded by deforestation, fires, and drainage for the last two decades. Such disturbances change hydrological conditions, typically groundwater level (GWL), and accelerate oxidative peat decomposition. Evapotranspiration (ET) is a major determinant of GWL, whereas information on the ET of PSF is limited. Therefore, we measured ET using the eddy covariance technique for 4-6 years between 2002 and 2009, including El Niño and La Niña events, at three sites in Central Kalimantan, Indonesia. The sites were different in disturbance degree: a PSF with little drainage (UF), a heavily drained PSF (DF), and a drained burnt ex-PSF (DB); GWL was significantly lowered at DF, especially in the dry season. The ET showed a clear seasonal variation with a peak in the mid-dry season and a large decrease in the late dry season, mainly following seasonal variation in net radiation (Rn ). The Rn drastically decreased with dense smoke from peat fires in the late dry season. Annual ET forced to close energy balance for 4 years was 1636 ± 53, 1553 ± 117, and 1374 ± 75 mm yr(-1) (mean ± 1 standard deviation), respectively, at UF, DF, and DB. The undrained PSF (UF) had high and rather stable annual ET, independently of El Niño and La Niña events, in comparison with other tropical rainforests. The minimum monthly-mean GWL explained 80% of interannual variation in ET for the forest sites (UF and DF); the positive relationship between ET and GWL indicates that drainage by a canal decreased ET at DF through lowering GWL. In addition, ET was decreased by 16% at DB in comparison with UF chiefly because of vegetation loss through fires.

Newly identified sex chromosomes in the Sphagnum (peat moss) genome alter carbon sequestration and ecosystem dynamics.

Peatlands are crucial sinks for atmospheric carbon but are critically threatened due to warming climates. Sphagnum (peat moss) species are keystone members of peatland communities where they actively engineer hyperacidic conditions, which improves their competitive advantage and accelerates ecosystem-level carbon sequestration. To dissect the molecular and physiological sources of this unique biology, we generated chromosome-scale genomes of two Sphagnum species: S. divinum and S. angustifolium. Sphagnum genomes show no gene colinearity with any other reference genome to date, demonstrating that Sphagnum represents an unsampled lineage of land plant evolution. The genomes also revealed an average recombination rate an order of magnitude higher than vascular land plants and short putative U/V sex chromosomes. These newly described sex chromosomes interact with autosomal loci that significantly impact growth across diverse pH conditions. This discovery demonstrates that the ability of Sphagnum to sequester carbon in acidic peat bogs is mediated by interactions between sex, autosomes and environment.

High genetic diversity in a remote island population system: sans sex.

It has been proposed that long-distance dispersal of mosses to the Hawaiian Islands rarely occurs and that the Hawaiian population of the allopolyploid peat moss Sphagnum palustre probably resulted from a single dispersal event. Here, we used microsatellites to investigate whether the Hawaiian population of the dioicous S. palustre had a single founder and to compare its genetic diversity to that found in populations of S. palustre in other regions. The genetic diversity of the Hawaiian population is comparable to that of larger population systems. Several lines of evidence, including a lack of sporophytes and an apparently restricted natural distribution, suggest that sexual reproduction is absent in the Hawaiian plants. In addition, all samples of Hawaiian S. palustre share a genetic trait rare in other populations. Time to most recent ancestor (TMRCA) analysis indicates that the Hawaiian population was probably founded 49-51 kyr ago. It appears that all Hawaiian plants of S. palustre descend from a single founder via vegetative propagation. The long-term viability of this clonal population coupled with the development of significant genetic diversity suggests that vegetative propagation in a moss does not necessarily preclude evolutionary success in the long term.

Bioaccumulation and glutathione-mediated detoxification of copper and cadmium in Sphagnum squarrosum Crome Samml.

Physiological and biochemical responses, metal bioaccumulation and tolerance potential of Sphagnum squarrosum Crome Samml. to Cu and Cd were studied to determine its bioindication and bioremediation potential. Results suggest that glutathione treatment increases the metal accumulation potential and plays a definite role in heavy metal scavenging. High abundance of Sphagnum in metal-rich sites strongly suggests its high metal tolerance capabilities. This experiment demonstrates that S. squarrosum is able to accumulate and tolerate a high amount of metals and feasibility of its application as bioindicator and remediator test species of metal-contaminated environment.

Vascular plants regulate responses of boreal peatland Sphagnum to climate warming and nitrogen addition.

Boreal peatland Sphagnum may be affected by climate warming and elevated nitrogen availability directly and indirectly via altering vascular plant interaction. Here, we used a field experiment of nitrogen addition, warming, and vascular plant removal to investigate the effects of these factors on Sphagnum in a Canadian blanket boreal peatland. We revealed that significant effects of warming and nitrogen addition on Sphagnum were regulated by vascular plant interaction. The intense competition of vascular plants accelerated an adverse effect of warming on Sphagnum, while facilitation of vascular plants reduced detrimental losses of the Sphagnum due to high dose of nitrogen addition and both warming and the nitrogen addition. These findings indicate the crucial role of vascular plants in regulating the effects of environmental changes on existing Sphagnum in boreal peatlands.

Climatic modifiers of the response to nitrogen deposition in peat-forming Sphagnum mosses: a meta-analysis.

Peatlands in the northern hemisphere have accumulated more atmospheric carbon (C) during the Holocene than any other terrestrial ecosystem, making peatlands long-term C sinks of global importance. Projected increases in nitrogen (N) deposition and temperature make future accumulation rates uncertain. Here, we assessed the impact of N deposition on peatland C sequestration potential by investigating the effects of experimental N addition on Sphagnum moss. We employed meta-regressions to the results of 107 field experiments, accounting for sampling dependence in the data. We found that high N loading (comprising N application rate, experiment duration, background N deposition) depressed Sphagnum production relative to untreated controls. The interactive effects of presence of competitive vascular plants and high tissue N concentrations indicated intensified biotic interactions and altered nutrient stochiometry as mechanisms underlying the detrimental N effects. Importantly, a higher summer temperature (mean for July) and increased annual precipitation intensified the negative effects of N. The temperature effect was comparable to an experimental application of almost 4 g N m(-2) yr(-1) for each 1°C increase. Our results indicate that current rates of N deposition in a warmer environment will strongly inhibit C sequestration by Sphagnum-dominated vegetation.

Interploidal hybridization and mating patterns in the Sphagnum subsecundum complex.

Polyploidization is thought to result in instant sympatric speciation, but several cases of hybrid zones between one of the parental species and its polyploid derivative have been documented. Previous work showed that diploid Sphagnum lescurii is an allopolyploid derived from the haploids S. lescurii (maternal progenitor) and S. subsecundum (paternal progenitor). Here, we report the results from analyses of a population where allodiploid and haploid S. lescurii co-occur and produce sporophytes. We tested (i) whether haploids and diploids form hybrid triploid sporophytes; (ii) how hybrid and nonhybrid sporophytes compare in fitness; (iii) whether hybrid sporophytes form viable spores; (iv) the ploidy of any viable gametophyte offspring from hybrid sporophytes; (v) the relative viability of sporelings derived from hybrid and nonhybrid sporophytes; and (vi) if interploidal hybridization results in introgression between the allopolyploid and its haploid progenitor. We found that triploid hybrid sporophytes do occur and are larger than nonhybrid sporophytes, but exhibit very low germination percentages and produce sporelings that develop more slowly than those from nonhybrid sporophytes. All sporophytes attached to haploid gametophytes were triploid and were sired by diploid males, but all sporophytes attached to diploid gametophytes were tetraploid. This asymmetric pattern of interploidal hybridization is related to an absence of haploid male gametophytes in the population. Surprisingly, all sporelings from triploid sporophytes were triploid, yet were genetically variable, suggesting some form of aberrant meiosis that warrants further study. There was limited (but some) evidence of introgression between allodiploid and haploid S. lescurii.