ABSTRACT
Plant-mediated CH4 transport (PMT) is the dominant pathway through which soil-produced CH4 can escape into the atmosphere and thus plays an important role in controlling ecosystem CH4 emission. PMT is affected by abiotic and biotic factors simultaneously, and the effects of biotic factors, such as the dominant plant species and their traits, can override the effects of abiotic factors. Increasing evidence shows that plant-mediated CH4 fluxes include not only PMT, but also within-plant CH4 production and oxidation due to the detection of methanogens and methanotrophs attached to the shoots. Despite the inter-species and seasonal differences, and the probable contribution of within-plant microbes to total plant-mediated CH4 exchange (PME), current process-based ecosystem models only estimate PMT based on the bulk biomass or leaf area index of aerenchymatous plants. We highlight five knowledge gaps to which more research efforts should be devoted. First, large between-species variation, even within the same family, complicates general estimation of PMT, and calls for further work on the key dominant species in different types of wetlands. Second, the interface (rhizosphere-root, root-shoot, or leaf-atmosphere) and plant traits controlling PMT remain poorly documented, but would be required for generalizations from species to relevant functional groups. Third, the main environmental controls of PMT across species remain uncertain. Fourth, the role of within-plant CH4 production and oxidation is poorly quantified. Fifth, the simplistic description of PMT in current process models results in uncertainty and potentially high errors in predictions of the ecosystem CH4 flux. Our review suggest that flux measurements should be conducted over multiple growing seasons and be paired with trait assessment and microbial analysis, and that trait-based models should be developed. Only then we are capable to accurately estimate plant-mediated CH4 emissions, and eventually ecosystem total CH4 emissions at both regional and global scales.
Subject(s)
Ecosystem , Wetlands , Plants/metabolism , Biomass , Methane/analysis , Carbon Dioxide/analysis , SoilABSTRACT
Methane emissions from plant foliage may play an important role in the global methane cycle, but their size and the underlying source processes remain poorly understood. Here, we quantify methane fluxes from the shoots of Scots pine trees, a dominant tree species in boreal forests, to identify source processes and environmental drivers, and we evaluate whether these fluxes can be constrained at the ecosystem-level by eddy covariance flux measurements. We show that shoot-level measurements conducted in forest, garden, or greenhouse settings; on mature trees and saplings; manually and with an automated CO2-, temperature-, and water-controlled chamber system; and with multiple methane analyzers all resulted in comparable daytime fluxes (0.144 ± 0.019 to 0.375 ± 0.074 nmol CH4 g-1 foliar d.w. h-1). We further find that these emissions exhibit a pronounced diurnal cycle that closely follows photosynthetically active radiation and is further modulated by temperature. These diurnal patterns indicate that methane production is associated with diurnal cycle of sunlight, indicating that this production is either a byproduct of photosynthesis-associated biochemical reactions (e.g., the methionine cycle) or produced through nonenzymatic photochemical reactions in plant biomass. Moreover, we identified a light-dependent component in stand-level methane fluxes, which showed order-of-magnitude agreement with shoot-level measurements (0.968 ± 0.031 nmol CH4 g-1 h-1) and which provides an upper limit for shoot methane emissions.
Subject(s)
Ecosystem , Pinus sylvestris , Temperature , Methane , Soil , Forests , Trees , Carbon DioxideABSTRACT
Aerenchymatic transport is an important mechanism through which plants affect methane (CH4 ) emissions from peatlands. Controlling environmental factors and the effects of plant phenology remain, however, uncertain. We identified factors controlling seasonal CH4 flux rate and investigated transport efficiency (flux rate per unit of rhizospheric porewater CH4 concentration). We measured CH4 fluxes through individual shoots of Carex rostrata, Menyanthes trifoliata, Betula nana and Salix lapponum throughout growing seasons in 2020 and 2021 and Equisetum fluviatile and Comarum palustre in high summer 2021 along with water-table level, peat temperature and porewater CH4 concentration. CH4 flux rate of C. rostrata was related to plant phenology and peat temperature. Flux rates of M. trifoliata and shrubs B. nana and S. lapponum were insensitive to the investigated environmental variables. In high summer, flux rate and efficiency were highest for C. rostrata (6.86 mg m-2 h-1 and 0.36 mg m-2 h-1 (µmol l-1 )-1 , respectively). Menyanthes trifoliata showed a high flux rate, but limited efficiency. Low flux rates and efficiency were detected for the remaining species. Knowledge of the species-specific CH4 flux rate and their different responses to plant phenology and environmental factors can significantly improve the estimation of ecosystem-scale CH4 dynamics in boreal peatlands.
Subject(s)
Ecosystem , Soil , Seasons , Temperature , Methane , Carbon Dioxide , WetlandsABSTRACT
Methane (CH4 ) exchange in tree stems and canopies and the processes involved are among the least understood components of the global CH4 cycle. Recent studies have focused on quantifying tree stems as sources of CH4 and understanding abiotic CH4 emissions in plant canopies, with the role of microbial in situ CH4 formation receiving less attention. Moreover, despite initial reports revealing CH4 consumption, studies have not adequately evaluated the potential of microbial CH4 oxidation within trees. In this paper, we discuss the current level of understanding on these processes. Further, we demonstrate the potential of novel metagenomic tools in revealing the involvement of microbes in the CH4 exchange of plants, and particularly in boreal trees. We detected CH4 -producing methanogens and novel monooxygenases, potentially involved in CH4 consumption, in coniferous plants. In addition, our field flux measurements from Norway spruce (Picea abies) canopies demonstrate both net CH4 emissions and uptake, giving further evidence that both production and consumption are relevant to the net CH4 exchange. Our findings, together with the emerging diversity of novel CH4 -producing microbial groups, strongly suggest microbial analyses should be integrated in the studies aiming to reveal the processes and drivers behind plant CH4 exchange.
Subject(s)
Methane , Trees , Metagenomics , Methane/analysis , NorwayABSTRACT
Boreal forest soils store significant amounts of carbon and are cohabited by saprotrophic and ectomycorrhizal fungi (ECM). The 'Gadgil effect' implies antagonistic interactions between saprotrophic fungi and ECM. Plant photosynthates support the competitive fitness of the ECM, and may also shape the soil bacterial communities. Many 'Gadgil effect' experiments have focused on litter layer (OL) or have litter and root-fragments present, and thus possibly favor the saprotrophs. We compared how the restriction of plant roots and exudates affect soil microbial community structures in organic soil (mixed OF and OH). For this, we established a 3-yr field experiment with 3 different mesh treatments affecting the penetration of plant roots and external fungal hyphae. Exclusion of plant photosynthates induced modest changes in both fungal and bacterial community structures, but not to potential functionality of the microbial community. The microbial community was resilient towards rather short-term disturbances. Contrary to the 'Gadgil effect', mesh treatments restricting the entrance of plant roots and external fungal hyphae did not favor saprotrophs that originally inhabited the soil. Thus, we propose that different substrate preferences (fresh litter vs. fermented or humified soil), rather than antagonism, maintain the spatial separation of saprotrophs and mycorrhizal fungi in boreal forest soils.
Subject(s)
Fungi/growth & development , Mycorrhizae/growth & development , Soil Microbiology , Carbon/metabolism , Fungi/classification , Fungi/genetics , Fungi/metabolism , Hyphae/classification , Hyphae/genetics , Hyphae/growth & development , Hyphae/metabolism , Microbiota , Mycorrhizae/classification , Mycorrhizae/genetics , Mycorrhizae/metabolism , Plant Roots/microbiology , Plants/metabolism , Plants/microbiology , Soil/chemistry , Taiga , Trees/microbiologyABSTRACT
Ombrotrophic peatlands are a recognized global carbon reservoir. Without restoration and peat regrowth, harvested peatlands are dramatically altered, impairing their carbon sink function, with consequences for methane turnover. Previous studies determined the impact of commercial mining on the physicochemical properties of peat and the effects on methane turnover. However, the response of the underlying microbial communities catalyzing methane production and oxidation have so far received little attention. We hypothesize that with the return of Sphagnum spp. postharvest, methane turnover potential and the corresponding microbial communities will converge in a natural and restored peatland. To address our hypothesis, we determined the potential methane production and oxidation rates in natural (as a reference), actively mined, abandoned, and restored peatlands over two consecutive years. In all sites, the methanogenic and methanotrophic population sizes were enumerated using quantitative PCR (qPCR) assays targeting the mcrA and pmoA genes, respectively. Shifts in the community composition were determined using Illumina MiSeq sequencing of the mcrA gene and a pmoA-based terminal restriction fragment length polymorphism (t-RFLP) analysis, complemented by cloning and sequence analysis of the mmoX gene. Peat mining adversely affected methane turnover potential, but the rates recovered in the restored site. The recovery in potential activity was reflected in the methanogenic and methanotrophic abundances. However, the microbial community composition was altered, being more pronounced for the methanotrophs. Overall, we observed a lag between the recovery of the methanogenic/methanotrophic activity and the return of the corresponding microbial communities, suggesting that a longer duration (>15 years) is needed to reverse mining-induced effects on the methane-cycling microbial communities.IMPORTANCE Ombrotrophic peatlands are a crucial carbon sink, but this environment is also a source of methane, an important greenhouse gas. Methane emission in peatlands is regulated by methane production and oxidation catalyzed by methanogens and methanotrophs, respectively. Methane-cycling microbial communities have been documented in natural peatlands. However, less is known of their response to peat mining and of the recovery of the community after restoration. Mining exerts an adverse impact on potential methane production and oxidation rates and on methanogenic and methanotrophic population abundances. Peat mining also induced a shift in the methane-cycling microbial community composition. Nevertheless, with the return of Sphagnum spp. in the restored site after 15 years, methanogenic and methanotrophic activity and population abundance recovered well. The recovery, however, was not fully reflected in the community composition, suggesting that >15 years are needed to reverse mining-induced effects.
Subject(s)
Methane/metabolism , Microbiota/physiology , Mining , Soil Microbiology , Soil , Bacterial Proteins/genetics , Bacterial Proteins/metabolism , Carbon/metabolism , Ecosystem , Euryarchaeota/genetics , Euryarchaeota/metabolism , Microbiota/genetics , Nitrogen Fixation , Oxidation-Reduction , Oxygenases , Phylogeny , Sphagnopsida/metabolism , WetlandsABSTRACT
Sphagnum-associated methanotrophs (SAM) are an important sink for the methane (CH4) formed in boreal peatlands. We aimed to reveal how peatland succession, which entails a directional change in several environmental variables, affects SAM and their activity. Based on the pmoA microarray results, SAM community structure changes when a peatland develops from a minerotrophic fen to an ombrotrophic bog. Methanotroph subtypes Ia, Ib, and II showed slightly contrasting patterns during succession, suggesting differences in their ecological niche adaptation. Although the direct DNA-based analysis revealed a high diversity of type Ib and II methanotrophs throughout the studied peatland chronosequence, stable isotope probing (SIP) of the pmoA gene indicated they were active mainly during the later stages of succession. In contrast, type Ia methanotrophs showed active CH4 consumption in all analyzed samples. SIP-derived (13)C-labeled 16S rRNA gene clone libraries revealed a high diversity of SAM in every succession stage including some putative Methylocella/Methyloferula methanotrophs that are not detectable with the pmoA-based approach. In addition, a high diversity of 16S rRNA gene sequences likely representing cross-labeled nonmethanotrophs was discovered, including a significant proportion of Verrucomicrobia-related sequences. These results help to predict the effects of changing environmental conditions on SAM communities and activity.
Subject(s)
Bacteria/classification , Methane/metabolism , Soil Microbiology , Sphagnopsida/microbiology , Wetlands , Bacteria/genetics , Bacteria/isolation & purification , Molecular Sequence Data , Phylogeny , RNA, Ribosomal, 16S/geneticsABSTRACT
It is known that Sphagnum associated methanotrophy (SAM) changes in relation to the peatland water table (WT) level. After drought, rising WT is able to reactivate SAM. We aimed to reveal whether this reactivation is due to activation of indigenous methane (CH(4)) oxidizing bacteria (MOB) already present in the mosses or to MOB present in water. This was tested through two approaches: in a transplantation experiment, Sphagna lacking SAM activity were transplanted into flark water next to Sphagna oxidizing CH(4). Already after 3 days, most of the transplants showed CH(4) oxidation activity. Microarray showed that the MOB community compositions of the transplants and the original active mosses had become more similar within 28 days thus indicating MOB movement through water between mosses. Methylocystis-related type II MOB dominated the community. In a following experiment, SAM inactive mosses were bathed overnight in non-sterile and sterile-filtered SAM active site flark water. Only mosses bathed with non-sterile flark water became SAM active, which was also shown by the pmoA copy number increase of over 60 times. Thus, it was evident that MOB present in the water can colonize Sphagnum mosses. This colonization could act as a resilience mechanism for peatland CH(4) dynamics by allowing the re-emergence of CH(4) oxidation activity in Sphagnum.
ABSTRACT
Northern peatlands play a major role in the global carbon cycle as sinks for CO(2) and as sources of CH(4). These diverse ecosystems develop through accumulation of partially decomposed plant material as peat. With increasing depth, peat becomes more and more recalcitrant due to its longer exposure to decomposing processes. Compared with surface peat, deeper peat sediments remain microbiologically poorly described. We detected active archaeal communities even in the deep bottom layers (-220/-280 cm) of two Finnish fen-type peatlands by 16S rRNA-based terminal restriction fragment length polymorphism analysis. In the sediments of the northern study site, all detected archaea were methanogens with Rice Cluster II (RC-II) and Methanosaetaceae as major groups. In southern peatland, Crenarchaeota of a rare unidentified cluster were present together with mainly RC-II methanogens. RNA profiles showed a larger archaeal diversity than DNA-based community profiles, suggesting that small but active populations were better visualized with rRNA. In addition, potential methane production measurements indicated methanogenic activity throughout the vertical peat profiles.