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  1. Host Species–Microbiome Interactions Contribute to Sphagnum Moss Growth Acclimation to Warming

    Sphagnum moss is the dominant plant genus in northern peatlands responsible for long-term carbon accumulation. Sphagnum hosts diverse microbial communities (microbiomes), and its phytobiome (plant host + constituent microbiome + environment) plays a key role in nutrient acquisition along with carbon cycling. Climate change can modify the Sphagnum-associated microbiome, resulting in enhanced host growth and thermal acclimation as previously shown in warming experiments. However, the extent of microbiome benefits to the host and the influence of host–microbe specificity on Sphagnum thermal acclimation remain unclear. Here, we extracted Sphagnum microbiomes from five donor species of four peatland warming experiments across amore » latitudinal gradient and applied those microbiomes to three germ-free Sphagnum species grown across a range of temperatures in the laboratory. Using this experimental system, we test if Sphagnum's growth response to warming depends on the donor and/or recipient host species, and we determine how the microbiome's growth conditions in the field affect Sphagnum host growth across a range of temperatures in the laboratory. After 4 weeks, we found that the highest growth rate of recipient Sphagnum was observed in treatments of matched host–microbiome pairs, with rates approximately 50% and 250% higher in comparison to maximum growth rates of non-matched host–microbiome pairs and germ-free Sphagnum, respectively. We also found that the maximum growth rate of host–microbiome pairs was reached when treatment temperatures were close to the microbiome's native temperatures. Our study shows that Sphagnum's growth acclimation to temperature is partially controlled by its constituent microbiome. Strong Sphagnum host–microbiome species specificity indicates the existence of underlying, unknown physiological mechanisms that may drive Sphagnum's ability to acclimatize to elevated temperatures. Together with rapid acclimation of the microbiome to warming, these specific microbiome–plant associations have the potential to enhance peatland resilience in the face of climate change.« less
  2. Divergent selection and climate adaptation fuel genomic differentiation between sister species of Sphagnum (peat moss)

    Abstract Background and Aims New plant species can evolve through the reinforcement of reproductive isolation via local adaptation along habitat gradients. Peat mosses (Sphagnaceae) are an emerging model system for the study of evolutionary genomics and have well-documented niche differentiation among species. Recent molecular studies have demonstrated that the globally distributed species Sphagnum magellanicum is a complex of morphologically cryptic lineages that are phylogenetically and ecologically distinct. Here, we describe the architecture of genomic differentiation between two sister species in this complex known from eastern North America: the northern S. diabolicum and the largely southern S. magniae. Methods We sampledmore » plant populations from across a latitudinal gradient in eastern North America and performed whole genome and restriction-site associated DNA sequencing. These sequencing data were then analyzed computationally. Key Results Using sliding-window population genetic analyses we find that differentiation is concentrated within ‘islands’ of the genome spanning up to 400 kb that are characterized by elevated genetic divergence, suppressed recombination, reduced nucleotide diversity and increased rates of non-synonymous substitution. Sequence variants that are significantly associated with genetic structure and bioclimatic variables occur within genes that have functional enrichment for biological processes including abiotic stress response, photoperiodism and hormone-mediated signalling. Demographic modelling demonstrates that these two species diverged no more than 225 000 generations ago with secondary contact occurring where their ranges overlap. Conclusions We suggest that this heterogeneity of genomic differentiation is a result of linked selection and reflects the role of local adaptation to contrasting climatic zones in driving speciation. This research provides insight into the process of speciation in a group of ecologically important plants and strengthens our predictive understanding of how plant populations will respond as Earth’s climate rapidly changes.« less
  3. Clonality, local population structure, and gametophyte sex ratios in cryptic species of the Sphagnum magellanicum complex

    Sphagnum (peatmoss) comprises a moss (Bryophyta) clade with approximately 300-500 species. The genus has unparalleled ecological importance because Sphagnum-dominated peatlands store almost a third of the terrestrial carbon pool and peatmosses engineer the formation and microtopography of peatlands. Genomic resources for Sphagnum are being actively expanded, but many aspects of their biology are still poorly known. Among these are the degree to which Sphagnum species reproduce asexually, and the relative frequencies of male and female gametophytes in these haploid-dominant plants. Here, we assess clonality and gametophyte sex ratios and test hypotheses about the local-scale distribution of clones and sexes inmore » four North American species of the S. magellanicum complex. These four species are difficult to distinguish morphologically and are very closely related. We also assess microbial communities associated with Sphagnum host plant clones and sexes at two sites. 405 samples of the four species, representing 57 populations, were subjected to RADseq. Analyses of population structure and clonality based on the molecular data utilized both phylogenetic and phenetic approaches. Multi-locus genotypes (genets) were identified using the RADseq data. Sexes of sampled ramets were determined using a molecular approach that utilized coverage of loci on the sex chromosomes after the method was validated using a sample of plants that expressed sex phenotypically. Sex ratios were estimated for each species, and populations within species. Differences in fitness between genets was estimated as the numbers of ramets each genet comprised. Degree of clonality (numbers of genets/numbers of ramets [samples]) within species, among sites, and between gametophyte sexes were estimated. Sex ratios were estimated for each species, and populations within species. Sphagnum-associated microbial communities were assessed at two sites in relation to Sphagnum clonality and sex. All four species appear to engage in a mixture of sexual and asexual (clonal) reproduction. A single ramet represents most genets but 2-8 ramets were detected for some genets. Only one genet is represented by ramets in multiple populations; all other genets are restricted to a single population. Within populations ramets of individual genets are spatially clustered, suggesting limited dispersal even within peatlands. Sex ratios are male-biased in S. diabolicum but female-biased in the other three species, although significantly so only in S. divinum. Neither species nor males/females differ in levels of clonal propagation. At St. Regis Lake (NY) and Franklin Bog (VT), microbial community composition is strongly differentiated between the sites, but differences between species, genets, and sexes were not detected. Within S. divinum, however, female gametophytes harbored 2-3 times the number oi of microbial taxa as males. These four Sphagnum species all exhibit a similar reproductive patterns that result from a mixture of sexual and asexual reproduction. The spatial patterns of clonally replicated ramets of genets suggest that these species fall between the so-called phalanx patterns where genets abut one another but do not extensively mix, because of limited ramet fragmentation, and the guerrilla patterns where extensive genet fragmentation and dispersal results in greater mixing of different genets. Although sex ratios in bryophytes are most often female-biased, both male and female biases occur in this complex of closely related species. The association of far greater microbial diversity for female gametophytes in S. divinum, which has a female-biased sex ratio, suggests additional research to determine if levels of microbial diversity are consistently correlated with differing patterns of sex ratio biases.« less
  4. Viral infections likely mediate microbial controls on ecosystem responses to global warming

    Abstract Climate change is affecting how energy and matter flow through ecosystems, thereby altering global carbon and nutrient cycles. Microorganisms play a fundamental role in carbon and nutrient cycling and are thus an integral link between ecosystems and climate. Here, we highlight a major black box hindering our ability to anticipate ecosystem climate responses: viral infections within complex microbial food webs. We show how understanding and predicting ecosystem responses to warming could be challenging—if not impossible—without accounting for the direct and indirect effects of viral infections on different microbes (bacteria, archaea, fungi, protists) that together perform diverse ecosystem functions. Importantly,more » understanding how rising temperatures associated with climate change influence viruses and virus-host dynamics is crucial to this task, yet is severely understudied. In this perspective, we (i) synthesize existing knowledge about virus-microbe-temperature interactions and (ii) identify important gaps to guide future investigations regarding how climate change might alter microbial food web effects on ecosystem functioning. To provide real-world context, we consider how these processes may operate in peatlands—globally significant carbon sinks that are threatened by climate change. We stress that understanding how warming affects biogeochemical cycles in any ecosystem hinges on disentangling complex interactions and temperature responses within microbial food webs.« less
  5. Sphagnum diabolicum sp. nov. and S. magniae sp. nov.; morphological variation and taxonomy of the “S. magellanicum complex”

    Until a few years ago, Sphagnum magellanicum was understood to be a single widespread species with an intercontinental range. Recent work by Norwegian sphagnologists showed that S. magellanicum s.str. is restricted to southern South America and plants known as S. magellanicum in Europe should be referred to S. divinum and S. medium. In a separate publication, we showed that there are two additional major clades in eastern North America, and we describe them herein as S. diabolicum and S. magniae. These species are very hard to distinguish morphologically (and also from S. divinum and S. medium) but are distinct phylogenetically,more » ecologically and geographically, and are important units of biodiversity. Here, morphological variation within and between species is photographically documented.« less
  6. 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 ofmore » 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.« less
  7. Phylogenomic structure and speciation in an emerging model: the Sphagnum magellanicum complex (Bryophyta)

    Sphagnum magellanicum is one of two Sphagnum species for which a reference-quality genome exists to facilitate research in ecological genomics. Phylogenetic and comparative genomic analyses were conducted based on resequencing data from 48 samples and RADseq analyses based on 187 samples. Here, we report that there are four clades/species within the S. magellanicum complex in eastern North America and that the reference genome belongs to Sphagnum divinum. The species exhibit tens of thousands (RADseq) to millions (resequencing) of fixed nucleotide differences. Two species, however, referred to informally as S. diabolicum and S. magni because they have not been formally described,more » are differentiated by only 100 (RADseq) to 1000 (resequencing) of differences. Introgression among species in the complex is demonstrated using D-statistics and f4 ratios. One ecologically important functional trait, tissue decomposability, which underlies peat (carbon) accumulation, does not differ between segregates in the S. magellanicum complex, although previous research showed that many closely related Sphagnum species have evolved differences in decomposability/carbon sequestration. Phylogenetic resolution and more accurate species delimitation in the S. magellanicum complex substantially increase the value of this group for studying the early evolutionary stages of climate adaptation and ecological evolution more broadly.« less
  8. Draft Metagenome Sequences of the Sphagnum (Peat Moss) Microbiome from Ambient and Warmed Environments across Europe

    We present 49 metagenome assemblies of the microbiome associated with Sphagnum (peat moss) collected from ambient, artificially warmed, and geothermally warmed conditions across Europe. These data will enable further research regarding the impact of climate change on plant-microbe symbiosis, ecology, and ecosystem functioning of northern peatland ecosystems.
  9. 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-assistedmore » 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.« less
  10. Habitat‐adapted microbial communities mediate Sphagnum peatmoss resilience to warming

    Summary 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, Chl a fluorescence imaging, metagenomics, metatranscriptomics and 16S rDNA profiling. Microbiomesmore » 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.« less
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"Shaw, A. Jonathan"

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