Diversity of Active Viral Infections within the Sphagnum Microbiome.
ABSTRACT: Sphagnum-dominated peatlands play an important role in global carbon storage and represent significant sources of economic and ecological value. While recent efforts to describe microbial diversity and metabolic potential of the Sphagnum microbiome have demonstrated the importance of its microbial community, little is known about the viral constituents. We used metatranscriptomics to describe the diversity and activity of viruses infecting microbes within the Sphagnum peat bog. The vegetative portions of six Sphagnum plants were obtained from a peatland in northern Minnesota, and the total RNA was extracted and sequenced. Metatranscriptomes were assembled and contigs were screened for the presence of conserved virus marker genes. Using bacteriophage capsid protein gp23 as a marker for phage diversity, we identified 33 contigs representing undocumented phages that were active in the community at the time of sampling. Similarly, RNA-dependent RNA polymerase and the nucleocytoplasmic large DNA virus (NCLDV) major capsid protein were used as markers for single-stranded RNA (ssRNA) viruses and NCLDV, respectively. In total, 114 contigs were identified as originating from undescribed ssRNA viruses, 22 of which represent nearly complete genomes. An additional 64 contigs were identified as being from NCLDVs. Finally, 7 contigs were identified as putative virophage or polinton-like viruses. We developed co-occurrence networks with these markers in relation to the expression of potential-host housekeeping gene rpb1 to predict virus-host relationships, identifying 13 groups. Together, our approach offers new tools for the identification of virus diversity and interactions in understudied clades and suggests that viruses may play a considerable role in the ecology of the Sphagnum microbiome.IMPORTANCE Sphagnum-dominated peatlands play an important role in maintaining atmospheric carbon dioxide levels by modifying conditions in the surrounding soil to favor the growth of Sphagnum over that of other plant species. This lowers the rate of decomposition and facilitates the accumulation of fixed carbon in the form of partially decomposed biomass. The unique environment produced by Sphagnum enriches for the growth of a diverse microbial consortia that benefit from and support the moss's growth, while also maintaining the hostile soil conditions. While a growing body of research has begun to characterize the microbial groups that colonize Sphagnum, little is currently known about the ecological factors that constrain community structure and define ecosystem function. Top-down population control by viruses is almost completely undescribed. This study provides insight into the significant viral influence on the Sphagnum microbiome and identifies new potential model systems to study virus-host interactions in the peatland ecosystem.
Project description:Viruses impact microbial activity and carbon cycling in various environments, but their diversity and ecological importance in Sphagnum-peatlands are unknown. Abundances of viral particles and prokaryotes were monitored bi-monthly at a fen and a bog at two different layers of the peat surface. Viral particle abundance ranged from 1.7 x 10(6) to 5.6 x 10(8) particles mL(-1), and did not differ between fen and bog but showed seasonal fluctuations. These fluctuations were positively correlated with prokaryote abundance and dissolved organic carbon, and negatively correlated with water-table height and dissolved oxygen. Using shotgun metagenomics we observed a shift in viral diversity between winter/spring and summer/autumn, indicating a seasonal succession of viral communities, mainly driven by weather-related environmental changes. Based on the seasonal asynchrony between viral and microbial diversity, we hypothesize a seasonal shift in the active microbial communities associated with a shift from lysogenic to lytic lifestyles. Our results suggest that temporal variations of environmental conditions rather than current habitat differences control the dynamics of virus-host interactions in Sphagnum-dominated peatlands.
Project description:The thawing of ice-rich permafrost soils in northern peatlands leads to the formation of thermokarst ponds, surrounded by organic-rich soils. These aquatic ecosystems are sites of intense microbial activity, and CO2 and CH4 emissions. Many of the pond systems in northern landscapes and their surrounding peatlands are hydrologically contiguous, but little is known about the microbial connectivity of concentric habitats around the thermokarst ponds, or the effects of peat accumulation and infilling on the microbial communities. Here we investigated microbial community structure and abundance in a thermokarst pond-peatland system in subarctic Canada. Several lineages were ubiquitous, supporting a prokaryotic continuum from the thermokarst pond to surrounding peatlands. However, the microbial community structure shifted from typical aerobic freshwater microorganisms (Betaproteobacteria and Alphaproteobacteria) in the pond towards acidophilic and anaerobic lineages (Acidobacteria and Choroflexi) in the connected peatland waters, likely selected by the acidification of the water by Sphagnum mosses. Marked changes in abundance and community composition of methane cycling microorganisms were detected along the thermokarst pond-peatland transects, suggesting fine tuning of C-1 carbon cycling within a highly connected system, and warranting the need for higher spatial resolution across the thermokarst landscape to accurately predict net greenhouse gas emissions from northern peatlands.
Project description:The fate of Northern peatlands under climate change is important because of their contribution to global carbon (C) storage. Peatlands are maintained via greater plant productivity (especially of Sphagnum species) than decomposition, and the processes involved are strongly mediated by climate. Although some studies predict that warming will relax constraints on decomposition, leading to decreased C sequestration, others predict increases in productivity and thus increases in C sequestration. We explored the lack of congruence between these predictions using single-species and integrated species distribution models as proxies for understanding the environmental correlates of North American Sphagnum peatland occurrence and how projected changes to the environment might influence these peatlands under climate change. Using Maximum entropy and BIOMOD modelling platforms, we generated single and integrated species distribution models for four common Sphagnum species in North America under current climate and a 2050 climate scenario projected by three general circulation models. We evaluated the environmental correlates of the models and explored the disparities in niche breadth, niche overlap, and climate suitability among current and future models. The models consistently show that Sphagnum peatland distribution is influenced by the balance between soil moisture deficit and temperature of the driest quarter-year. The models identify the east and west coasts of North America as the core climate space for Sphagnum peatland distribution. The models show that, at least in the immediate future, the area of suitable climate for Sphagnum peatland could expand. This result suggests that projected warming would be balanced effectively by the anticipated increase in precipitation, which would increase Sphagnum productivity.
Project description:Sphagnum-associated microbiomes are crucial to Sphagnum growth and peatland ecological functions. However, roles of rare species in bacterial communities across Sphagnum compartments are poorly understood. Here the structures of rare taxa (RT) and conditionally abundant and rare taxa (CART) from Sphagnum palustre peat (SP), S. palustre ectosphere (Ecto) and S. palustre endosphere (Endo) were investigated in the Dajiuhu Peatland, central China. Our results showed that plant compartment effects significantly altered the diversities and structures of bacterial communities. The Observed species and Simpson indices of RT and CART in alpha diversity significantly increased from Endo to SP, with those of Ecto in-between. The variations of community dissimilarities of RT and CART among compartments were consistent with those of whole bacterial communities (WBC). Network analysis indicated a non-random co-occurrence pattern of WBC and all keystone species are affiliated with RT and CART, indicating their important role in sustaining the WBC. Furthermore, the community structures of RT and CART in SP were significantly shaped by water table and total nitrogen content, which coincided with the correlations between WBC and environmental factors. Collectively, our results for the first time confirm the importance of rare species to bacterial communities through structural and predicted functional analyses, which expands our understanding of rare species in Sphagnum-associated microbial communities in subalpine peatlands.
Project description:Current projections suggest that climate warming will be accompanied by more frequent and severe drought events. Peatlands store ca. one third of the world's soil organic carbon. Warming and drought may cause peatlands to become carbon sources through stimulation of microbial activity increasing ecosystem respiration, with positive feedback effect on global warming. Micro-eukaryotes play a key role in the carbon cycle through food web interactions and therefore, alterations in their community structure and diversity may affect ecosystem functioning and could reflect these changes. We assessed the diversity and community composition of <i>Sphagnum</i>-associated eukaryotic microorganisms inhabiting peatlands and their response to experimental drought and warming using high throughput sequencing of environmental DNA. Under drier conditions, micro-eukaryotic diversity decreased, the relative abundance of autotrophs increased and that of osmotrophs (including Fungi and Peronosporomycetes) decreased. Furthermore, we identified climate change indicators that could be used as early indicators of change in peatland microbial communities and ecosystem functioning. The changes we observed indicate a shift towards a more "terrestrial" community in response to drought, in line with observed changes in the functioning of the ecosystem.
Project description:Peatland ecosystem services include drinking water provision, flood mitigation, habitat provision and carbon sequestration. Dissolved organic carbon (DOC) removal is a key treatment process for the supply of potable water downstream from peat-dominated catchments. A transition from peat-forming Sphagnum moss to vascular plants has been observed in peatlands degraded by (a) land management, (b) atmospheric deposition and (c) climate change. Here within we show that the presence of vascular plants with higher annual above-ground biomass production leads to a seasonal addition of labile plant material into the peatland ecosystem as litter recalcitrance is lower. The net effect will be a smaller litter carbon pool due to higher rates of decomposition, and a greater seasonal pattern of DOC flux. Conventional water treatment involving coagulation-flocculation-sedimentation may be impeded by vascular plant-derived DOC. It has been shown that vascular plant-derived DOC is more difficult to remove via these methods than DOC derived from Sphagnum, whilst also being less susceptible to microbial mineralisation before reaching the treatment works. These results provide evidence that practices aimed at re-establishing Sphagnum moss on degraded peatlands could reduce costs and improve efficacy at water treatment works, offering an alternative to 'end-of-pipe' solutions through management of ecosystem service provision.
Project description:Climate warming is predicted to increase heterotrophic metabolism in northern peatland soils leading to enhanced greenhouse gas emissions. However, the specific relationships between temperature and the greenhouse gas producing microbial communities are poorly understood. Thus, in this study, the temperature dependence of carbon dioxide (CO2) and methane (CH4) production rates along with abundance and composition of microbial communities were investigated in peat from a Sphagnum-dominated peatland, S1 bog (Minnesota, United States). Whereas CH4 production rates increased with temperature up to 30°C, CO2 production did not, resulting in a lower CO2:CH4 ratio with increasing temperature. CO2 production showed both psychrophilic and mesophilic maxima at 4 and 20°C, respectively, and appears to be mediated by two anaerobic microbial communities, one that operates under psychrophilic conditions that predominate for much of the year, and another that is more active under warmer conditions during the growing season. In incubations at 10°C above the ambient range, members of the Clostridiaceae and hydrogenotrophic methanogens of the Methanobacteriaceae dominated. Moreover, a significant negative correlation between temperature and microbial diversity was observed. Results indicate that the potential consequences of warming surface peat in northern peatlands include a large stimulation in CH4 production and a significant loss of microbial diversity.
Project description:Mid- to high-latitude peatlands are a major terrestrial carbon stock but become carbon sources during droughts, which are increasingly frequent as a result of climate warming. A critical question within this context is the sensitivity to drought of peatland microbial food webs. Microbiota drive key ecological and biogeochemical processes, but their response to drought is likely to impact these processes. Peatland food webs have, however, been little studied, especially the response of microbial predators. We studied the response of microbial predators (testate amoebae, ciliates, rotifers, and nematodes) living in Sphagnum moss carpet to droughts, and their influence on lower trophic levels and on related microbial enzyme activity. We assessed the impact of reduced water availability on microbial predators in two peatlands using experimental (Linje mire, Poland) and natural (Forbonnet mire, France) water level gradients, reflecting a sudden change in moisture regime (Linje), and a typically drier environment (Forbonnet). The sensitivity of different microbial groups to drought was size dependent; large sized microbiota such as testate amoebae declined most under dry conditions (-41% in Forbonnet and -80% in Linje). These shifts caused a decrease in the predator-prey mass ratio (PPMR). We related microbial enzymatic activity to PPMR; we found that a decrease in PPMR can have divergent effects on microbial enzymatic activity. In a community adapted to drier conditions, decreasing PPMR stimulated microbial enzyme activity, while in extreme drought experiment, it reduced microbial activity. These results suggest that microbial enzymatic activity resulting from food web structure is optimal only within a certain range of PPMR, and that different trophic mechanisms are involved in the response of peatlands to droughts. Our findings confirm the importance of large microbial consumers living at the surface of peatlands on the functioning of peatlands, and illustrate their value as early warning indicators of change.
Project description:Sphagnum mosses dominate peatlands by employing harsh ecosystem tactics to prevent vascular plant growth and microbial degradation of these large carbon stores. Knowledge about Sphagnum-produced metabolites, their structure and their function, is important to better understand the mechanisms, underlying this carbon sequestration phenomenon in the face of climate variability. It is currently unclear which compounds are responsible for inhibition of organic matter decomposition and the mechanisms by which this inhibition occurs. Metabolite profiling of Sphagnum fallax was performed using two types of mass spectrometry (MS) systems and 1H nuclear magnetic resonance spectroscopy (1H NMR). Lipidome profiling was performed using LC-MS/MS. A total of 655 metabolites, including one hundred fifty-two lipids, were detected by NMR and LC-MS/MS-329 of which were novel metabolites (31 unknown lipids). Sphagum fallax metabolite profile was composed mainly of acid-like and flavonoid glycoside compounds, that could be acting as potent antimicrobial compounds, allowing Sphagnum to control its environment. Sphagnum fallax metabolite composition comparison against previously known antimicrobial plant metabolites confirmed this trend, with seventeen antimicrobial compounds discovered to be present in Sphagnum fallax, the majority of which were acids and glycosides. Biological activity of these compounds needs to be further tested to confirm antimicrobial qualities. Three fungal metabolites were identified providing insights into fungal colonization that may benefit Sphagnum. Characterizing the metabolite profile of Sphagnum fallax provided a baseline to understand the mechanisms in which Sphagnum fallax acts on its environment, its relation to carbon sequestration in peatlands, and provide key biomarkers to predict peatland C store changes (sequestration, emissions) as climate shifts.
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.