skip to main content


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

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 twoSphagnumspecies:S. divinumandS. angustifolium.Sphagnumgenomes show no gene colinearity with any other reference genome to date, demonstrating thatSphagnumrepresents 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 ofSphagnumto sequester carbon in acidic peat bogs is mediated by interactions between sex, autosomes and environment.

 
more » « less
Award ID(s):
1928514
NSF-PAR ID:
10478248
Author(s) / Creator(s):
; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; more » ; ; ; ; ; ; ; ; ; « less
Publisher / Repository:
Nature
Date Published:
Journal Name:
Nature Plants
Volume:
9
Issue:
2
ISSN:
2055-0278
Page Range / eLocation ID:
238 to 254
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract

    The relative importance of global versus local environmental factors for growth and thus carbon uptake of the bryophyte genusSphagnum—the main peat‐former and ecosystem engineer in northern peatlands—remains unclear.

    We measured length growth and net primary production (NPP) of two abundantSphagnumspecies across 99 Holarctic peatlands. We tested the importance of previously proposed abiotic and biotic drivers for peatland carbon uptake (climate, N deposition, water table depth and vascular plant cover) on these two responses. Employing structural equation models (SEMs), we explored both indirect and direct effects of drivers onSphagnumgrowth.

    Variation in growth was large, but similar within and between peatlands. Length growth showed a stronger response to predictors than NPP. Moreover, the smaller and denserSphagnum fuscumgrowing on hummocks had weaker responses to climatic variation than the larger and looserSphagnum magellanicumgrowing in the wetter conditions. Growth decreased with increasing vascular plant cover within a site. Between sites, precipitation and temperature increased growth forS. magellanicum. The SEMs indicate that indirect effects are important. For example, vascular plant cover increased with a deeper water table, increased nitrogen deposition, precipitation and temperature. These factors also influencedSphagnumgrowth indirectly by affecting moss shoot density.

    Synthesis. Our results imply that in a warmer climate,S. magellanicumwill increase length growth as long as precipitation is not reduced, whileS. fuscumis more resistant to decreased precipitation, but also less able to take advantage of increased precipitation and temperature. Such species‐specific sensitivity to climate may affect competitive outcomes in a changing environment, and potentially the future carbon sink function of peatlands.

     
    more » « less
  2. Abstract Background and Aims

    Sphagnum (peatmoss) comprises a moss (Bryophyta) clade with ~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. We assess clonality and gametophyte sex ratios and test hypotheses about the local-scale distribution of clones and sexes in 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.

    Methods

    Four hundred and five samples of the four species, representing 57 populations, were subjected to restriction site-associated DNA sequencing (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. Difference in fitness between genets was estimated as the numbers of ramets each genet comprised. Degrees 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.

    Key Results

    All four species appear to engage in a mixture of sexual and asexual (clonal) reproduction. A single ramet represents most genets but two to eight ramets were dsumbers ansd text etected 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 harboured two to three times the number of microbial taxa as males.

    Conclusions

    These four Sphagnum species all exhibit 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 result 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.

     
    more » « less
  3. Abstract

    Peat mosses (Sphagnumspp.) are keystone species in boreal peatlands, where they dominate net primary productivity and facilitate the accumulation of carbon in thick peat deposits.Sphagnummosses harbor a diverse assemblage of microbial partners, including N2‐fixing (diazotrophic) and CH4‐oxidizing (methanotrophic) taxa that support ecosystem function by regulating transformations of carbon and nitrogen. Here, we investigate the response of theSphagnumphytobiome (plant + constituent microbiome + environment) to a gradient of experimental warming (+0°C to +9°C) and elevated CO2(+500 ppm) in an ombrotrophic peatland in northern Minnesota (USA). By tracking changes in carbon (CH4, CO2) and nitrogen (NH4‐N) cycling from the belowground environment up toSphagnumand its associated microbiome, we identified a series of cascading impacts to theSphagnumphytobiome triggered by warming and elevated CO2. Under ambient CO2, warming increased plant‐available NH4‐N in surface peat, excess N accumulated inSphagnumtissue, and N2fixation activity decreased. Elevated CO2offset the effects of warming, disrupting the accumulation of N in peat andSphagnumtissue. Methane concentrations in porewater increased with warming irrespective of CO2treatment, resulting in a ~10× rise in methanotrophic activity withinSphagnumfrom the +9°C enclosures. Warming's divergent impacts on diazotrophy and methanotrophy caused these processes to become decoupled at warmer temperatures, as evidenced by declining rates of methane‐induced N2fixation and significant losses of keystone microbial taxa. In addition to changes in theSphagnummicrobiome, we observed ~94% mortality ofSphagnumbetween the +0°C and +9°C treatments, possibly due to the interactive effects of warming on N‐availability and competition from vascular plant species. Collectively, these results highlight the vulnerability of theSphagnumphytobiome to rising temperatures and atmospheric CO2concentrations, with significant implications for carbon and nitrogen cycling in boreal peatlands.

     
    more » « less
  4. Abstract

    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 ofSphagnumwas 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 inSphagnum(inferred from microsatellite heterozygosity) does not appear to be biased with regard to geographic region nor intrageneric clade. The inference thatSphagnumdiversified 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.

     
    more » « less
  5. Premise

    TheSphagnum recurvumcomplex comprises a group of closely related peat mosses that are dominant components of many northern wetland ecosystems. Taxonomic hypotheses for the group range from interpreting the whole complex as one polymorphic species to distinguishing 6–10 species. The complex occurs throughout the Northern Hemisphere, and some of the putative species have intercontinental ranges. Our goals were to delimit the complex and assess its phylogenetic structure in relation to morphologically defined species and intercontinental geography.

    Methods

    RADseq analyses were applied to a sample of 384 collections from Europe, North America, and Asia. The data were subjected to maximum likelihood phylogenetic analyses and analyses of genetic structure using the software STRUCTURE and multivariate ordination approaches.

    Results

    TheS. recurvumcomplex includesS. angustifolium,S. fallax,S. flexuosum,S. pacificum, andS. recurvumas clades with little evidence of admixture. We also resolved an unnamed clade that is referred to here asS. “pseudopacificum.” We confirm thatS. balticumandS. obtusumare nested within the complex. Species with bluntly acute to obtuse stem leaf apices are sister to those with acute to apiculate leaves. Most of the species exhibit some differentiation between intraspecific population systems disjunct on different continents.

    Conclusions

    We recognize seven species in the amendedS. recurvumcomplex, includingS. balticumandS. obtusum, in addition to the informal cladeS. “pseudopacificum.” Although we detected some geographically correlated phylogenetic structure within widespread morphospecies, our RADseq data support the interpretation that these species have intercontinental geographic ranges.

     
    more » « less