Experimental warming alters the community composition, diversity, and N2 fixation activity of peat moss (Sphagnum fallax) microbiomes.
ABSTRACT: Sphagnum-dominated peatlands comprise a globally important pool of soil carbon (C) and are vulnerable to climate change. While peat mosses of the genus Sphagnum are known to harbor diverse microbial communities that mediate C and nitrogen (N) cycling in peatlands, the effects of climate change on Sphagnum microbiome composition and functioning are largely unknown. We investigated the impacts of experimental whole-ecosystem warming on the Sphagnum moss microbiome, focusing on N2 fixing microorganisms (diazotrophs). To characterize the microbiome response to warming, we performed next-generation sequencing of small subunit (SSU) rRNA and nitrogenase (nifH) gene amplicons and quantified rates of N2 fixation activity in Sphagnum fallax individuals sampled from experimental enclosures over 2 years in a northern Minnesota, USA bog. The taxonomic diversity of overall microbial communities and diazotroph communities, as well as N2 fixation rates, decreased with warming (p < 0.05). Following warming, diazotrophs shifted from a mixed community of Nostocales (Cyanobacteria) and Rhizobiales (Alphaproteobacteria) to predominance of Nostocales. Microbiome community composition differed between years, with some diazotroph populations persisting while others declined in relative abundance in warmed plots in the second year. Our results demonstrate that warming substantially alters the community composition, diversity, and N2 fixation activity of peat moss microbiomes, which may ultimately impact host fitness, ecosystem productivity, and C storage potential in peatlands.
Project description:Biological nitrogen (N) fixation is an important process supporting primary production in ecosystems, especially in those where N availability is limiting growth, such as peatlands and boreal forests. In many peatlands, peat mosses (genus Sphagnum) are the prime ecosystem engineers, and like feather mosses in boreal forests, they are associated with a diverse community of diazotrophs (N2-fixing microorganisms) that live in and on their tissue. The large variation in N2 fixation rates reported in literature remains, however, to be explained. To assess the potential roles of habitat (including nutrient concentration) and species traits (in particular litter decomposability and photosynthetic capacity) on the variability in N2 fixation rates, we compared rates associated with various Sphagnum moss species in a bog, the surrounding forest and a fen in Sweden. We found appreciable variation in N2 fixation rates among moss species and habitats, and showed that both species and habitat conditions strongly influenced N2 fixation. We here show that higher decomposition rates, as explained by lower levels of decomposition-inhibiting compounds, and higher phosphorous (P) levels, are related with higher diazotrophic activity. Combining our findings with those of other studies, we propose a conceptual model in which both species-specific traits of mosses (as related to the trade-off between rapid photosynthesis and resistance to decomposition) and P availability, explain N2 fixation rates. This is expected to result in a tight coupling between P and N cycling in peatlands.
Project description:Biological nitrogen fixation is an important source of bioavailable nitrogen in Sphagnum dominated peatlands. Sphagnum mosses harbor a diverse microbiome including nitrogen-fixing and methane (CH4) oxidizing bacteria. The inhibitory effect of oxygen on microbial nitrogen fixation is documented for many bacteria. However, the role of nitrogen-fixing methanotrophs in nitrogen supply to Sphagnum peat mosses is not well explored. Here, we investigated the role of both oxygen and methane on nitrogen fixation in subarctic Sphagnum peat mosses. Five species of Sphagnum mosses were sampled from two mesotrophic and three oligotrophic sites within the Lakkasuo peatland in Orivesi, central Finland. Mosses were incubated under either ambient or low oxygen conditions in the presence or absence of methane. Stable isotope activity assays revealed considerable nitrogen-fixing and methane-assimilating rates at all sites (1.4?±?0.2 µmol 15N-N2 g-1 DW day-1 and 12.0?±?1.1 µmol 13C-CH4 g-1 DW day-1, respectively). Addition of methane did not stimulate incorporation of 15N-nitrogen into biomass, whereas oxygen depletion increased the activity of the nitrogen-fixing community. Analysis of the 16S rRNA genes at the bacterial community level showed a very diverse microbiome that was dominated by Alphaproteobacteria in all sites. Bona fide methane-oxidizing taxa were not very abundant (relative abundance less than 0.1%). Based on our results we conclude that methanotrophs did not contribute significantly to nitrogen fixation in the investigated peatlands.
Project description:Peatlands have acted as C-sinks for millennia, storing large amounts of carbon, of which a significant amount is yearly released as methane (CH4). Sphagnum mosses are a key genus in many peat ecosystems and these mosses live in close association with methane-oxidizing and nitrogen-fixing microorganisms. To disentangle mechanisms which may control Sphagnum-associated methane-oxidation and nitrogen-fixation, we applied four treatments to Sphagnum mosses from a pristine peatland in Finland: nitrogen fertilization, phosphorus fertilization, CH4 addition and light. N and P fertilization resulted in nutrient accumulation in the moss tissue, but did not increase Sphagnum growth. While net CO2 fixation rates remained unaffected in the N and P treatment, net CH4 emissions decreased because of enhanced CH4 oxidation. CH4 addition did not affect Sphagnum performance in the present set-up. Light, however, clearly stimulated the activity of associated nitrogen-fixing and methane-oxidizing microorganisms, increasing N2 fixation rates threefold and CH4 oxidation rates fivefold. This underlines the strong connection between Sphagnum and associated N2 fixation and CH4 oxidation. It furthermore indicates that phototrophy is a strong control of microbial activity, which can be directly or indirectly.
Project description:Biological N2 fixation (BNF) in the rhizosphere of Podocarpaceae is currently attributed to unspecific diazotrophs with negligible impact on N acquisition. Here, we report specific and high associative BNF in dead cells of root nodules of Lepidothamnus fonkii distributed in ombrotrophic peatlands of Patagonia. BNF of nodulated roots, intact plants of L. fonkii and rhizospheric peat was assessed by 15N2 and acetylene reduction. Diazotrophs were identified by electron microscopy, analysis of nitrogenase encoding genes (nifH) and transcripts, and 16S rRNA. Nitrogenase encoding nifH transcripts from root nodules point to Beijerinckiaceae (Rhizobiales), known as free-living diazotrophs. Electron microscopy and 16S rRNA analysis likewise identified active Beijerinckiaceae in outer dead cells of root nodules. NifH transcripts from the rhizopshere peat revealed diverse active diazotrophs including Beijerinckiaceae. Both methods revealed high activity of nitrogenase rates in cut roots of L. fonkii (2.5??mol N g-1 d.w. d-1 based on 15N2 assay; 2.4??mol C2H4 g-1 d.w. d-1 based on acetylene reduction assay). The data suggest that (i) nodules recruit diazotrophic Beijerinckiaceae from peat, (ii) dead nodule cells provide an exclusive habitat for Beijerinckiaceae, and (iii) BNF in L. fonkii is one potent pathway to overcome N deficiency in ombrotrophic peatlands of Patagonia.
Project description:Nitrogen (N) fixation by diazotrophic plankton is the primary source of this crucial nutrient to the ocean, but the factors limiting its rate and distribution are controversial. According to one view, the ecological niche of diazotrophs is primarily controlled by the ocean through internally generated N deficits that suppress the growth of their competitors. A second view posits an overriding limit from the atmosphere, which restricts diazotrophs to regions where dust deposition satisfies their high iron (Fe) requirement, thus separating N sources from sinks at a global scale. Here we use multiple geochemical signatures of N2 fixation to show that the Fe limitation of diazotrophs is strong enough to modulate the regional distribution of N2 fixation within ocean basins--particularly the Fe-poor Pacific--but not strong enough to influence its partition between basins, which is instead governed by rates of N loss. This scale-dependent limitation of N2 fixation reconciles local observations of Fe stress in diazotroph communities with an inferred spatial coupling of N sources and sinks. Within this regime of intermediate Fe control, the oceanic N reservoir would respond only weakly to enhanced dust fluxes during glacial climates, but strongly to the reduced fluxes hypothesized under anthropogenic climate warming.
Project description: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.
Project description:Nitrogen (N) accumulation rates in peatland ecosystems indicate significant biological atmospheric N2 fixation associated with Sphagnum mosses. Here, we show that the linkage between methanotrophic carbon cycling and N2 fixation may constitute an important mechanism in the rapid accumulation of N during the primary succession of peatlands. In our experimental stable isotope enrichment study, previously overlooked methane-induced N2 fixation explained more than one-third of the new N input in the younger peatland stages, where the highest N2 fixation rates and highest methane oxidation activities co-occurred in the water-submerged moss vegetation.
Project description:Discrepancies between bioavailable nitrogen (N) concentrations and phytoplankton growth rates in the oligotrophic waters of the Great Barrier Reef (GBR) suggest that undetermined N sources must play a significant role in supporting primary productivity. One such source could be biological dinitrogen (N2) fixation through the activity of "diazotrophic" bacterioplankton. Here, we investigated N2 fixation and diazotroph community composition over 10° S of latitude within GBR surface waters. Qualitative N2 fixation rates were found to be variable across the GBR but were relatively high in coastal, inner and outer GBR waters, reaching 68 nmol L-1 d-1. Diazotroph assemblages, identified by amplicon sequencing of the nifH gene, were dominated by the cyanobacterium Trichodesmium erythraeum, ?-proteobacteria from the Gamma A clade, and ?-proteobacterial phylotypes related to sulfate-reducing genera. However, diazotroph communities exhibited significant spatial heterogeneity, correlated with shifts in dissolved inorganic nutrient concentrations. Specifically, heterotrophic diazotrophs generally increased in relative abundance with increasing concentrations of phosphate and N, while Trichodesmium was proportionally more abundant when concentrations of these nutrients were low. This study provides the first in-depth characterization of diazotroph community composition and N2 fixation dynamics within the oligotrophic, N-limited surface waters of the GBR. Our observations highlight the need to re-evaluate N cycling dynamics within oligotrophic coral reef systems, to include diverse N2 fixing assemblages as a potentially significant source of dissolved N within the water column.
Project description:Sphagnum mosses are keystone components of peatland ecosystems. They facilitate the accumulation of carbon in peat deposits, but climate change is predicted to expose peatland ecosystem to sustained and unprecedented warming leading to a significant release of carbon to the atmosphere. Sphagnum responses to climate change, and their interaction with other components of the ecosystem, will determine the future trajectory of carbon fluxes in peatlands. We measured the growth and productivity of Sphagnum in an ombrotrophic bog in northern Minnesota, where ten 12.8-m-diameter plots were exposed to a range of whole-ecosystem (air and soil) warming treatments (+0 to +9°C) in ambient or elevated (+500 ppm) CO2. The experiment is unique in its spatial and temporal scale, a focus on response surface analysis encompassing the range of elevated temperature predicted to occur this century, and consideration of an effect of co-occurring CO2 altering the temperature response surface. In the second year of warming, dry matter increment of Sphagnum increased with modest warming to a maximum at 5°C above ambient and decreased with additional warming. Sphagnum cover declined from close to 100% of the ground area to <50% in the warmest enclosures. After three years of warming, annual Sphagnum productivity declined linearly with increasing temperature (13-29 g C/m2 per °C warming) due to widespread desiccation and loss of Sphagnum. Productivity was less in elevated CO2 enclosures, which we attribute to increased shading by shrubs. Sphagnum desiccation and growth responses were associated with the effects of warming on hydrology. The rapid decline of the Sphagnum community with sustained warming, which appears to be irreversible, can be expected to have many follow-on consequences to the structure and function of this and similar ecosystems, with significant feedbacks to the global carbon cycle and climate change.
Project description:Nitrogen fixing plankton provide nitrogen to fuel marine ecosystems and biogeochemical cycles but the factors that constrain their growth and habitat remain poorly understood. Here we investigate the importance of metabolic specialization in unicellular diazotroph populations, using laboratory experiments and model simulations. In clonal cultures of Crocosphaera watsonii and Cyanothece sp. spiked with 15N2, cellular 15N enrichment developed a bimodal distribution within colonies, indicating that N2 fixation was confined to a subpopulation. In a model of population metabolism, heterogeneous nitrogen (N2) fixation rates substantially reduce the respiration rate required to protect nitrogenase from O2. The energy savings from metabolic specialization is highest at slow growth rates, allowing populations to survive in deeper waters where light is low but nutrients are high. Our results suggest that heterogeneous N2 fixation in colonies of unicellular diazotrophs confers an energetic advantage that expands the ecological niche and may have facilitated the evolution of multicellular diazotrophs.