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.

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.

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.

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.

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.

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.

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.

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 .

Impact of warming and reduced precipitation on morphology and chlorophyll concentration in peat mosses (Sphagnum angustifolium and S. fallax).

Peatlands are one of the most important ecosystems due to their biodiversity and abundant organic compounds; therefore, it is important to observe how different plant species in peatlands react to changing environmental conditions. Sphagnum spp. are the main component of peatlands and are considered as the creator of conditions favorable for carbon storage in the form of peat. Sphagnum angustifolium and Sphagnum fallax are taxonomically very close species. To examine their adaptability to climate change, we studied the morphology and pigment content of these two species from environmental manipulation sites in Poland, where the environment was continuously manipulated for temperature and precipitation. The warming of peat was induced by using infrared heaters, whereas total precipitation was reduced by a curtain that cuts the nighttime precipitation. Morphology of S. angustifolium stayed under climate manipulation relatively stable. However, the main morphological parameters of S. fallax were significantly affected by precipitation reduction. Thus, this study indicates S. angustifolium is better adapted in comparison to S. fallax for drier and warmer conditions.

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.

Taxonomic and functional turnover are decoupled in European peat bogs.

In peatland ecosystems, plant communities mediate a globally significant carbon store. The effects of global environmental change on plant assemblages are expected to be a factor in determining how ecosystem functions such as carbon uptake will respond. Using vegetation data from 56 Sphagnum-dominated peat bogs across Europe, we show that in these ecosystems plant species aggregate into two major clusters that are each defined by shared response to environmental conditions. Across environmental gradients, we find significant taxonomic turnover in both clusters. However, functional identity and functional redundancy of the community as a whole remain unchanged. This strongly suggests that in peat bogs, species turnover across environmental gradients is restricted to functionally similar species. Our results demonstrate that plant taxonomic and functional turnover are decoupled, which may allow these peat bogs to maintain ecosystem functioning when subject to future environmental change.

Sphagnum palustre clone vs native Pseudoscleropodium purum: A first trial in the field to validate the future of the moss bag technique.

Although a large body of literature exists on the use of transplanted mosses for biomonitoring of air pollution, no article has addressed so far the use and the accumulation performance of a cloned moss for this purpose. In this work, a direct comparison of metal accumulation between bags filled with a Sphagnum palustre L. clone or with native Pseudoscleropodium purum Hedw., one of the most used moss species in biomonitoring surveys, was investigated. The test was performed in sites with different atmospheric contamination levels selected in urban, industrial, agricultural and background areas of Italy and Spain. Among the eighteen elements investigated, S. palustre was significantly enriched in 10 elements (Al, Ba, Cr, Cu, Fe, Hg, Pb, Sr, V and Zn), while P. purum was enriched only in 6 elements (Al, Ba, Cu, Hg, Pb and Sr), and had a consistently lower uptake capacity than S. palustre. The clone proved to be more sensitive in terms of metal uptake and showed a better performance as a bioaccumulator, providing a higher accumulation signal and allowing a finer distinction among the different land uses and levels of pollution. The excellent uptake performance of the S. palustre clone compared to the native P. purum and its low and stable baseline elemental content, evidenced in this work, are key features for the improvement of the moss bag approach and its large scale application.

Nitrogen deposition does not enhance Sphagnum decomposition.

Long-term additions of nitrogen (N) to peatlands have altered bryophyte growth, species dominance, N content in peat and peat water, and often resulted in enhanced Sphagnum decomposition rate. However, these results have mainly been derived from experiments in which N was applied as ammonium nitrate (NH4NO3), neglecting the fact that in polluted areas, wet deposition may be dominated either by NO3(-) or NH4(+). We studied effects of elevated wet deposition of NO3(-) vs. NH4(+) alone (8 or 56kgNha(-1)yr(-1) over and above the background of 8kgNha(-1)yr(-1) for 5 to 11years) or combined with phosphorus (P) and potassium (K) on Sphagnum quality for decomposers, mass loss, and associated changes in hummock pore water in an ombrotrophic bog (Whim). Adding N, especially as NH4(+), increased N concentration in Sphagnum, but did not enhance mass loss from Sphagnum. Mass loss seemed to depend mainly on moss species and climatic factors. Only high applications of N affected hummock pore water chemistry, which varied considerably over time. Overall, C and N cycling in this N treated bog appeared to be decoupled. We conclude that moss species, seasonal and annual variation in climatic factors, direct negative effects of N (NH4(+) toxicity) on Sphagnum production, and indirect effects (increase in pH and changes in plant species dominance under elevated NO3(-) alone and with PK) drive Sphagnum decomposition and hummock C and N dynamics at Whim.

Sphagnum can 'filter' N deposition, but effects on the plant and pore water depend on the N form.

The ability of Sphagnum moss to efficiently intercept atmospheric nitrogen (N) has been assumed to be vulnerable to increased N deposition. However, the proposed critical load (20kgNha(-1)yr(-1)) to exceed the capacity of the Sphagnum N filter has not been confirmed. A long-term (11years) and realistic N manipulation on Whim bog was used to study the N filter function of Sphagnum (Sphagnum capillifolium) in response to increased wet N deposition. On this ombrotrophic peatland where ambient deposition was 8kgNha(-1)yr(-1), an additional 8, 24, and 56kgNha(-1)yr(-1) of either ammonium (NH4(+)) or nitrate (NO3(-)) has been applied for 11years. Nutrient status of Sphagnum and pore water quality from the Sphagnum layer were assessed. The N filter function of Sphagnum was still active up to 32kgNha(-1)yr(-1) even after 11years. N saturation of Sphagnum and subsequent increases in dissolved inorganic N (DIN) concentration in pore water occurred only for 56kgNha(-1)yr(-1) of NH4(+) addition. These results indicate that the Sphagnum N filter is more resilient to wet N deposition than previously inferred. However, functionality will be more compromised when NH4(+) dominates wet deposition for high inputs (56kgNha(-1)yr(-1)). The N filter function in response to NO3(-) uptake increased the concentration of dissolved organic N (DON) and associated organic anions in pore water. NH4(+) uptake increased the concentration of base cations and hydrogen ions in pore water though ion exchange. The resilience of the Sphagnum N filter can explain the reported small magnitude of species change in the Whim bog ecosystem exposed to wet N deposition. However, changes in the leaching substances, arising from the assimilation of NO3(-) and NH4(+), may lead to species change.

Sphagnum-dominated bog systems are highly effective yet variable sources of bio-available iron to marine waters.

Iron is a micronutrient of particular interest as low levels of iron limit primary production of phytoplankton and carbon fluxes in extended regions of the world's oceans. Sphagnum-peatland runoff is extraordinarily rich in dissolved humic-bound iron. Given that several of the world's largest wetlands are Sphagnum-dominated peatlands, this ecosystem type may serve as one of the major sources of iron to the ocean. Here, we studied five near-coastal creeks in North Scotland using freshwater/seawater mixing experiments of natural creek water and synthetic seawater based on a (59)Fe radiotracer technique combined with isotopic characterization of dissolved organic carbon by Accelerator Mass Spectrometry. Three of the creeks meander through healthy Sphagnum-dominated peat bogs and the two others through modified peatlands which have been subject to artificial drainage for centuries. The results revealed that, at the time of sampling (August 16-24, 2014), the creeks that run through modified peatlands delivered 11-15µg iron per liter creek water to seawater, whereas the creeks that run through intact peatlands delivered 350-470µg iron per liter creek water to seawater. To find out whether this humic-bound iron is bio-available to marine algae, we performed algal growth tests using the unicellular flagellated marine prymnesiophyte Diacronema lutheri and the unicellular marine green alga Chlorella salina, respectively. In both cases, the riverine humic material provided a highly bio-available source of iron to the marine algae. These results add a new item to the list of ecosystem services of Sphagnum-peatlands.

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.

Factors affecting re-vegetation dynamics of experimentally restored extracted peatland in Estonia.

Increasing human activity continues to threaten peatlands, and as the area of natural mires declines, our obligation is to restore their ecosystem functions. Several restoration strategies have been developed for restoration of extracted peatlands, including "The moss layer transfer method", which was initiated on the Tässi extracted peatland in central Estonia in May 2012. Three-year study shows that despite the fluctuating water table, rainfall events can compensate for the insufficient moisture for mosses. Total plant cover on the restoration area attained 70 %, of which ~60 % is comprised of target species-Sphagnum mosses. From restoration treatments, spreading of plant fragments had a significant positive effect on the cover of bryophyte and vascular plants. Higher water table combined with higher plant fragments spreading density and stripping of oxidised peat layer affected positively the cover of targeted Sphagnum species. The species composition in the restoration area became similar to that in the donor site in a natural bog. Based on results, it was concluded that the method approved for restoration in North America gives good results also in the restoration of extracted peatland towards re-establishment of bog vegetation under northern European conditions.