Host-linked soil viral ecology along a permafrost thaw gradient

Climate change threatens to release abundant carbon that is sequestered at high latitudes, but the constraints on microbial metabolisms that mediate the release of methane and carbon dioxide are poorly understood1,2,3,4,5,6,7. The role of viruses, which are known to affect microbial dynamics, metabolism and biogeochemistry in the oceans8,9,10, remains largely unexplored in soil. Here, we aimed to investigate how viruses influence microbial ecology and carbon metabolism in peatland soils along a permafrost thaw gradient in Sweden. We recovered 1,907 viral populations (genomes and large genome fragments) from 197 bulk soil and size-fractionated metagenomes, 58% of which were detected in metatranscriptomes and presumed to be active. In silico predictions linked 35% of the viruses to microbial host populations, highlighting likely viral predators of key carbon-cycling microorganisms, including methanogens and methanotrophs. Lineage-specific virus/host ratios varied, suggesting that viral infection dynamics may differentially impact microbial responses to a changing climate. Virus-encoded glycoside hydrolases, including an endomannanase with confirmed functional activity, indicated that viruses influence complex carbon degradation and that viral abundances were significant predictors of methane dynamics. These findings suggest that viruses may impact ecosystem function in climate-critical, terrestrial habitats and identify multiple potential viral contributions to soil carbon cycling

Controls on Soil Organic Matter Degradation and Subsequent Greenhouse Gas Emissions Across a Permafrost Thaw Gradient in Northern Sweden

Warming-induced permafrost thaw could enhance microbial decomposition of previously stored soil organic matter (SOM) to carbon dioxide (CO2) and methane (CH4), one of the most significant potential feedbacks from terrestrial ecosystems to the atmosphere in a changing climate. The environmental parameters regulating microbe-organic matter interactions and greenhouse gas (GHG) emissions in northern permafrost peatlands are however still largely unknown. The objective of this work is to understand controls on SOM degradation and its impact on porewater GHG concentrations across the Stordalen Mire, a thawing peat plateau in Northern Sweden. Here, we applied high-resolution mass spectrometry to characterize SOM molecular composition in peat soil samples from the active layers of a Sphagnum-dominated bog and rich fen sites in the Mire. Microbe-organic matter interactions and porewater GHG concentrations across the thaw gradient were controlled by aboveground vegetation and soil pH. An increasingly high abundance of reduced organic compounds experiencing greater humification rates due to enhanced microbial activity were observed with increasing thaw, in parallel with higher CH(4)and CO(2)porewater concentrations. Bog SOM however contained more Sphagnum-derived phenolics, simple carbohydrates, and organic- acids. The low degradation of bog SOM by microbial communities, the enhanced SOM transformation by potentially abiotic mechanisms, and the accumulation of simple carbohydrates in the bog sites could be attributed in part to the low pH conditions of the system associated with Sphagnum mosses. We show that Gibbs free energy of C half reactions based on C oxidation state for OM can be used as a quantifiable measure for OM decomposability and quality to enhance current biogeochemical models to predict C decomposition rates. We found a direct association between OM chemical diversity and delta C-13-CH(4)in peat porewater; where higher substrate diversity was positively correlated with enriched delta C-13-CH(4)in fen sites. Oxidized sulfur-containing compounds, produced by Sphagnum, were further hypothesized to control GHG emissions by acting as electron acceptors for a sulfate-reducing electron transport chain, inhibiting methanogenesis in peat bogs. These results suggest that warming-induced permafrost thaw might increase organic matter lability, in subset of sites that become wetlands, and shift biogeochemical processes toward faster decomposition with an increasing proportion of carbon released as CH4.Department of Energy and Climate ChangeOpen access journalThis item from the UA Faculty Publications collection is made available by the University of Arizona with support from the University of Arizona Libraries. If you have questions, please contact us at [email protected]

Microbial community analyses inform geochemical reaction network models for predicting pathways of greenhouse gas production

The mechanisms, pathways, and rates of CO2 and CH4 production are central to understanding carbon cycling and greenhouse gas flux in wetlands. Thawing permafrost regions are of particular interest because they are disproportionally affected by climate warming and store large reservoirs of organic C that may be readily converted to CO2 and CH4 upon thaw. This conversion is accomplished by a community of microorganisms interacting in complex ways to transform large organic compounds into fatty acids and ultimately CO2 and CH4. While the central role of microbes in this process is well-known, geochemical rate models rarely integrate microbiological information. Herein, we expanded the geochemical rate model of Neumann et al., (2016, Biogeochemistry 127: 57-87) to incorporate a Bayesian probability analysis and applied the result to quantifying rates of CO2, CH4, and acetate production in closed-system incubations of peat collected from three habitats along a permafrost thaw gradient. The goals of this analysis were twofold. First, we integrated microbial community analyses with geochemical rate modeling by using microbial data to inform the best model choice among equally mathematically feasible model variants. Second, based on model results, we described changes in organic carbon transformation among habitats to understand the changing pathways of greenhouse gas production along the permafrost thaw gradient. We found that acetoclasty, hydrogenotrophy, CO2 production, and homoacetogenesis were the important reactions in this system, with little evidence for anaerobic CH4 oxidation. There was a distinct transition in the reactions across the thaw gradient. The collapsed palsa stage presents an initial disequilibrium where the abrupt (physically and temporally) change in elevation introduces freshly fixed carbon into anoxic conditions then fermentation products build up over time as the system transitions through the acid phase and electron acceptors are depleted. In the bog, fermentation slows, while methanogenesis increases. In the fully thawed fen, most of the terminal electron acceptors are depleted and the system becomes increasingly methanogenic. This suggests that as permafrost regions thaw and dry palsas transition into wet fens, CH4 emissions will rise, increasing the warming potential of these systems and accelerating climate warming feedbacks

Latitude, Elevation, and Mean Annual Temperature Predict Peat Organic Matter Chemistry at a Global Scale

Peatlands contain a significant fraction of global soil carbon, but how these reservoirs will respond to the changing climate is still relatively unknown. A global picture of the variations in peat organic matter chemistry will aid our ability to gauge peatland soil response to climate. The goal of this research is to test the hypotheses that (a) peat carbohydrate content, an indicator of soil organic matter reactivity, will increase with latitude and decrease with mean annual temperatures, (b) while peat aromatic content, an indicator of recalcitrance, will vary inversely, and (c) elevation will have a similar effect to latitude. We used Fourier Transform Infrared Spectroscopy to examine variations in the organic matter functional groups of 1034 peat samples collected from 10 to 20, 30–40, and 60–70 cm depths at 165 individual sites across a latitudinal gradient of 79°N–65°S and from elevations of 0–4,773 m. Carbohydrate contents of high latitude peat were significantly greater than peat originating near the equator, while aromatic content showed the opposite trend. For peat from similar latitudes but different elevations, the carbohydrate content was greater and aromatic content was lower at higher elevations. Higher carbohydrate content at higher latitudes indicates a greater potential for mineralization, whereas the chemical composition of low latitude peat is consistent with their apparent relative stability in the face of warmer temperatures. The combination of low carbohydrates and high aromatics at warmer locations near the equator suggests the mineralization of high latitude peat until reaching recalcitrance under a new temperature regime.Estación Experimental Agropecuaria BarilocheFil: Verbeke, Brittany A. Florida State University. Department of Earth, Ocean, and Atmospheric Science; Estados UnidosFil: Lamit, Louis J. Syracuse University. Department of Biology, Department of Environmental and Forest Biology; Estados UnidosFil: Lilleskov, Erik A. USDA Forest Service; Estados UnidosFil: Hodgkins, Suzanne B. Florida State University. Department of Chemistry and Biochemistry; Estados UnidosFil: Basiliko, Nathan. Laurentian University. Department of Biology and the Vale Living with Lakes Centre; CanadaFil: Kane, Evan S. USDA Forest Service; Estados UnidosFil: Andersen, Roxane. University of the Highlands and Islands. Environmental Research Institute; Reino UnidoFil: Artz, Rebekka R. E. Ecological Sciences, James Hutton Institute; Reino UnidoFil: Benavides, Juan Carlos. Pontificia Universidad Javeriana. Departmento de Ecología y Territorio; ColombiaFil: Enriquez, Andrea Soledad. Instituto Nacional de Tecnologia Agropecuaria (INTA). Estación Experimental Agropecuaria Bariloche. Área de Recursos Naturales; ArgentinaFil: Enriquez, Andrea Soledad. Consejo Nacional de Investigaciones Cientificas y Tecnicas. Instituto de Investigaciones Forestales y Agropecuarias Bariloche; ArgentinaFil: Chanton, Jeffrey P. Florida State University. Department of Earth, Ocean, and Atmospheric Science; Estados Unido

Mapping substrate use across a permafrost thaw gradient

Permafrost thaw in northern peatlands is likely to create a positive feedback to climate change, as microbes transform soil carbon (C) into carbon dioxide (CO2) or methane (CH4). While the microbiome's encoded C-processing potential changes with thaw, the impact on substrate utilization and gas emissions is less well characterized. We therefore examined microbial C-cycling dynamics from a partially thawed Sphagnum-dominated bog to a fully thawed sedge-dominated fen in Stordalen Mire (68.35°N, 19.05°E), Sweden. We profiled C substrate utilization diversity and extent by Biolog Ecoplates™, then tested substrate-specific hypotheses by targeted additions (of glucose, the short chain fatty acids (SCFAs) acetate and butyrate, and the organic acids galacturonic acid and p-hydroxybenzoic acid, all at field-relevant concentrations) under anaerobic conditions at 15 °C. In parallel we characterized microbiomes (via 16S rRNA amplicon sequencing and quantitative polymerase chain reaction) and C gas emissions. The fen exhibited a higher substrate use diversity and faster rate of overall substrate utilization than in the bog, based on Biolog Ecoplate™ incubations. Simple glucose additions (akin to a positive control) to peat microcosms fueled fermentation as expected (reflected in enriched fermenter lineages, their inferred metabolisms, and CO2 production), but also showed potential priming of anaerobic phenol degradation in the bog. Addition of SCFAs to bog and fen produced the least change in lineages and in CO2, and modest suppression of CH4 primarily in the fen, attributed to inhibition. Addition of both organic acids greatly increased the CO2:CH4 ratio in the deep peats but had distinct individual gas dynamics and impacts on microbiota. Both organic acids appeared to act as both C source and as a microbial inhibitor, with galacturonic acid also likely playing a role in electron transfer or acceptance. Collectively, these results support the importance of aboveground-belowground linkages - and in particular the role of Sphagnum spp.- in supplying substrates and inhibitors that drive microbiome assembly and C processing in these dynamically changing systems. In addition, they highlight an important temporal dynamic: responses on the short time scale of incubations (which would reflect transition conditions in the field) differ from those evident at the longer scales of habitat transition, in ways consequential to C gas emissions. In the short term, substrate addition response reflected microbiome legacy (e.g., bog communities were slower to process C and better tolerated inhibitors than fen communities) but led to little overall increase in C gas production (and a high skew to CO2). At the longer time scale of bog and fen thaw stages (which are used to represent these systems in models) the concomitant shifts in plants, hydrology and microbiota attenuate microbiome legacy impacts on substrate processing and C gas emissions over time. As habitat transition areas expand under accelerating change, we hypothesize an increased role of microbiome legacy in the landscape overall, leading to a lag in the increase of CH4 emissions expected from fen expansion.Open access articleThis item from the UA Faculty Publications collection is made available by the University of Arizona with support from the University of Arizona Libraries. If you have questions, please contact us at [email protected]

Methanotrophy across a natural permafrost thaw environment

The fate of carbon sequestered in permafrost is a key concern for future global warming as this large carbon stock is rapidly becoming a net methane source due to widespread thaw. Methane release from permafrost is moderated by methanotrophs, which oxidise 20-60% of this methane before emission to the atmosphere. Despite the importance of methanotrophs to carbon cycling, these microorganisms are under-characterised and have not been studied across a natural permafrost thaw gradient. Here, we examine methanotroph communities from the active layer of a permafrost thaw gradient in Stordalen Mire (Abisko, Sweden) spanning three years, analysing 188 metagenomes and 24 metatranscriptomes paired with in situ biogeochemical data. Methanotroph community composition and activity varied significantly as thaw progressed from intact permafrost palsa, to partially thawed bog and fully thawed fen. Thirteen methanotroph population genomes were recovered, including two novel genomes belonging to the uncultivated upland soil cluster alpha (USCα) group and a novel potentially methanotrophic Hyphomicrobiaceae. Combined analysis of porewater δC-CH isotopes and methanotroph abundances showed methane oxidation was greatest below the oxic-anoxic interface in the bog. These results detail the direct effect of thaw on autochthonous methanotroph communities, and their consequent changes in population structure, activity and methane moderation potential

Discovery of a novel methanogen prevalent in thawing permafrost

Thawing permafrost promotes microbial degradation of cryo-sequestered and new carbon leading to the biogenic production of methane, creating a positive feedback to climate change. Here we determine microbial community composition along a permafrost thaw gradient in northern Sweden. Partially thawed sites were frequently dominated by a single archaeal phylotype, Candidatus ‘Methanoflorens stordalenmirensis’ gen. nov. sp. nov., belonging to the uncultivated lineage ‘Rice Cluster II’ (Candidatus ‘Methanoflorentaceae’ fam. nov.). Metagenomic sequencing led to the recovery of its near-complete genome, revealing the genes necessary for hydrogenotrophic methanogenesis. These genes are highly expressed and methane carbon isotope data are consistent with hydrogenotrophic production of methane in the partially thawed site. In addition to permafrost wetlands, ‘Methanoflorentaceae’ are widespread in high methane-flux habitats suggesting that this lineage is both prevalent and a major contributor to global methane production. In thawing permafrost, Candidatus ‘M. stordalenmirensis’ appears to be a key mediator of methane-based positive feedback to climate warming

Carbon accumulation, flux, and fate in Stordalen Mire, a permafrost peatland in transition

Author Posting. © American Geophysical Union, 2022. This article is posted here by permission of American Geophysical Union for personal use, not for redistribution. The definitive version was published in Global Biogeochemical Cycles 36(1), (2022): e2021GB007113, https://doi.org/10.1029/2021GB007113.Stordalen Mire is a peatland in the discontinuous permafrost zone in arctic Sweden that exhibits a habitat gradient from permafrost palsa, to Sphagnum bog underlain by permafrost, to Eriophorum-dominated fully thawed fen. We used three independent approaches to evaluate the annual, multi-decadal, and millennial apparent carbon accumulation rates (aCAR) across this gradient: seven years of direct semi-continuous measurement of CO2 and CH4 exchange, and 21 core profiles for 210Pb and 14C peat dating. Year-round chamber measurements indicated net carbon balance of −13 ± 8, −49 ± 15, and −91 ± 43 g C m−2 y−1 for the years 2012–2018 in palsa, bog, and fen, respectively. Methane emission offset 2%, 7%, and 17% of the CO2 uptake rate across this gradient. Recent aCAR indicates higher C accumulation rates in surface peats in the palsa and bog compared to current CO2 fluxes, but these assessments are more similar in the fen. aCAR increased from low millennial-scale levels (17–29 g C m−2 y−1) to moderate aCAR of the past century (72–81 g C m−2 y−1) to higher recent aCAR of 90–147 g C m−2 y−1. Recent permafrost collapse, greater inundation and vegetation response has made the landscape a stronger CO2 sink, but this CO2 sink is increasingly offset by rising CH4 emissions, dominated by modern carbon as determined by 14C. The higher CH4 emissions result in higher net CO2-equivalent emissions, indicating that radiative forcing of this mire and similar permafrost ecosystems will exert a warming influence on future climate.We would like to acknowledge the following funding in support of this project: Swedish Research Council (Vetenskapsrådet, VR) grants (NT 2007-4547 and NT 2013-5562 to P. Crill), U.S. Department of Energy grants (DE-SC0004632 and DE-SC0010580 to V. Rich and S. Saleska), and U.S. National Science Foundation MacroSystems Biology grant (NSF EF #1241037, PI Varner). This work was supported by the U.S. Department of Energy, Office of Science, Office of Biological and Environmental Research under the Genomic Science program. We also acknowledge funding from the National Science Foundation for the EMERGE Biology Integration Institute, NSF Award #2022070.2022-07-0