Microbial “hotspots” of organic matter decomposition in temperate peatlands are driven by local spatial heterogeneity in abiotic conditions and not by vegetation structure
Introduction
The majority of the world's peatlands occur in boreal and temperate parts of the Northern Hemisphere where they cover around 3.5 million km2 of land and store about 455 Gt of carbon (C), representing around 25% of all the soil C stored on earth (Moore, 2002). They are complex ecosystems, consisting of habitat mosaics containing plant species that form peat under high precipitation-low temperature climatic regimes that restrict decomposition, leading to carbon accumulation. Their plant communities are dominated by different functional types (PFTs) as defined by their growth forms (e.g. vascular woody plants, herbaceous forbs and graminoids and non-vacular plants including bryophytes; Dorrepaal, 2007). The PFTs supply a wide range of food sources (as litter and root exudates) to below-ground decomposers with cascading effects on ecosystem C turnover (De Deyn et al., 2008; Ward et al., 2015; Chen et al., 2016). In addition to nutrient inputs, the abiotic conditions are also key abiotic regulators of decomposer activities, with soil temperature and moisture determining anaerobic and aerobic processes (Cobb et al., 2017; Morton and Heinemeyer, 2019), and temperature defining the activation energy of biochemical reactions (Davidson and Janssens, 2006).
Consequently, climate change is expected to cause profound alterations in peatland hydrology that will increase rates of decomposition (Ise et al., 2008; Waddington et al., 2015). In addition, some projections forecast a functional shift in peatland plant communities to favour vascular plants over mosses (e.g., Gallego-Sala and Prentice, 2013; Dieleman et al., 2015), which could exacerbate C losses (Walker et al., 2016; Robroek et al., 2016; Malhotra et al., 2020). As a result, concerns have risen about the potential for these critical C reservoirs to become significant global sources of C, with temperate peatlands likely to have a greater greenhouse gas contribution than their northern counterparts due to their longer and warmer growing seasons (Limpens et al., 2008; Teh et al., 2011).
When analysing the temperature sensitivity of peat C decomposition and potential feedbacks to climate change, the interactions between abiotic and biotic factors have been recognised as regulators of C cycling in these ecosystems (Briones et al., 2014; Armstrong et al., 2015; Juan-Ovejero et al., 2020). However, linking abiotic and biotic drivers of peatland C dynamics is challenged by the variability in plant-soil interactions even a small spatial scales. For example, in peatlands, decomposition rates vary through acrotelm and catotelm layers (Lunt et al., 2019), and as a result, the above- and below-ground phenologies are often unparallel (Schwieger et al., 2019). This could explain the contradictory responses reported in the literature, where certain PFTs have been found to strongly influence carbon dioxide (CO2) fluxes (Ward et al., 2013; Armstrong et al., 2015), whereas other studies concluded that abiotic factors are the main drivers of CO2 production irrespective of PFTs (Preston et al., 2012; Haynes et al., 2015). Similarly, while some studies have detected correlative relationships between different PFTs and DOC (Armstrong et al., 2012), others have concluded that plant control on DOC release is indirect through their influence on soil fauna (Carrera et al., 2009; Juan-Ovejero et al., 2020).
Therefore, elucidating the dominant causal relationships between PFTs, soil biota and C fluxes in these ecosystems requires spatially and temporally extensive assessments of biotic and abiotic factors in field environments. Previous studies have shown that temporal variations of soil abiotic conditions across different PFTs result in profound alterations of soil mesofauna community structure as a consequence of their different ecophysiological adaptations to water table drawdown (Juan-Ovejero et al., 2019). However, there is a distinct lack of data on similar temporal changes in microbial community responses in such microhabitats, and the potential implications for the C sink/source function (see review by Zhong et al., 2020).
In this study, we aimed to disentangle the effects biotic (PFTs) and abiotic drivers (soil microclimatic conditions) on temperate peatland microbial community structure and C cycling. We selected four representative temperate peatland habitats based on their peat forming vegetation: Atlantic wet heathland (Erica mackayana and Calluna vulgaris), two active blanket bogs with herbaceous plants (Molinia caerulea and Eriophorum angustifolium), and a transition mire dominated by Sphagnum mosses. These peatlands were located at different elevations to capture the natural altitudinal gradient in soil temperature and water content (Bragazza et al., 2015). We hypothesized that distinct microbial communities will be associated with different PFTs (i.e., vascular vs. non-vascular), irrespective of their spatial location, in agreement with other studies linking peatland habitats to specific microbial taxa (Chroňáková et al., 2019). However, based on microbial responses to abiotic factors (e.g., Bragazza et al., 2015; Kumar et al., 2019), we also hypothesized that greater seasonal variations in temperature and moisture will determine changes in microbial community structure over time despite PFT. Finally, in addition to microclimatic conditions, litter quality differences among PFTs also drive microbial decomposition processes and accordingly, we expected a higher C turnover with a greater supply of more decomposable plant litter. Sphagnum mosses and shrubs have large concentrations of high molecular weight polyphenolic compounds they are very resistant to microbial attack (Hattenschwiler and Vitousek, 2000; Fenner and Freeman, 2011). Similarly, the cotton-grass Eriophorum angustifolium produces litter that is lower in nutrient content than other vascular species and hence, its decomposition rates are similar to those of shrubs (Trinder et al., 2008). In contrast, the graminoid Molinia caerulea is a fast growing grass that produces nutrient-rich litter (Certini et al., 2015; Kaštovská et al., 2018), providing a greater supply of labile C to decomposers. Since previous modelling exercises have shown that C exports in these systems are abiotically mediated via direct and indirect effects on peat mesofauna populations (Juan-Ovejero et al., 2020), we assessed whether abiotic factors are the major drivers of microbial decomposition, while above-ground vegetation composition acts as secondary modifier.
Section snippets
Peatland habitats
The study area is located in “Serra do Xistral’’ (NW of the Iberian Peninsula) within the Atlantic Biogeographical Region. Data from the nearest meteorological station (Fragavella 43° 27″ 16.56′' N, 7° 26″ 46.5′' W; 710 m a.s.l.) indicate that the area is characterised by an oceanic climate, with a mean annual temperature of 10.5 °C (ranging from 6.0 °C in February to 16.0 °C in August) and annual rainfall of 1533 mm in the 17 years prior to sampling. Similar temperature records were observed
Microbial community structure under different PFTs
Total PLFA biomarker abundance was significantly higher in the peat samples from the Atlantic wet heathland and the Sphagnum site (152.8 ± 5.3 and 140.6 ± 5.4 μg g−1, respectively) than from the two blanket bogs (Eriophorum: 108.7 ± 3.7 and Molinia: 105.4 ± 4.2 μg g−1; Table 1 and Fig. 1).
However, microbial community structure was very similar across habitats, with bacteria being the most dominant group relative to total abundance (79–80%; Fig. 1), and fungi representing the smallest proportion
Linking habitat properties to below-ground microbial community structure
This two-year field study showed that microbial communities were more strongly linked to local soil abiotic conditions than to the dominant above-ground vegetation types. These results contradict previous studies concluding that different vascular plants are inhabited by unique microbial communities (Chroňáková et al., 2019), but agree with observations in tropical peatlands where contrasting plant communities supported similar microbial communities (Girkin et al., 2020).
The four peat soils
Conclusions
Research to find common mechanisms that shape the diversity of above- and below-ground plant-soil organisms have shown that community structure is governed by many interacting factors (Bardgett and Van Der Putten, 2014). In temperate peatlands, local abiotic factors (such as microtopography, soil temperature and pH, water and pore space availability, etc.) and differences in local plant communities are expected to have a strong influence on soil communities and C cycling. Despite the high
Declaration of competing interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Acknowledgements
We are very grateful to Dr Annette Ryan (Lancaster University) for her valuable support with PLFAs procedures and to Kelly Mason (UKCEH) for her advice on microbial biomarkers assignation. This work was funded by a MINECO research grant (Ref. CGL2014-54861-R) and R. Juan-Ovejero was supported by a PhD fellowship (FPI Programme, Ref. BES-2015-074461). MJIB would also like to thank Xunta de Galicia (Ref. 10 PXIB 310 142 PR and CITACA Strategic Partnership ED431E 2018/07) for funding the research
References (81)
- et al.
Microbial communities in natural and disturbed peatlands: a review
Soil Biology and Biochemistry
(2013) - et al.
A soil microcosm system and its application to measurements of respiration and nutrient leaching
Soil Biology and Biochemistry
(1982) - et al.
Multi-scale relationship between peatland vegetation type and dissolved organic carbon concentration
Ecological Engineering
(2012) - et al.
The role of molecular weight in the enzyme-inhibiting effect of phenolics: the significance in peatland carbon sequestration
Ecological Engineering
(2018) - et al.
The ratio of Gram-positive to Gram-negative bacterial PLFA markers as an indicator of carbon availability in organic soils
Soil Biology and Biochemistry
(2019) - et al.
Use and misuse of PLFA measurements in soils
Soil Biology and Biochemistry
(2011) - et al.
Microbial diversity in Sphagnum peatlands
- et al.
The role of polyphenols in terrestrial ecosystem nutrient cycling
Trends in Ecology & Evolution
(2000) - et al.
Tolerance to fluctuating water regimes drives changes in mesofauna community structure and vertical stratification in peatlands
Pedobiologia
(2019) - et al.
The interplay between abiotic factors and below-ground biological interactions regulates carbon exports from peatlands
Geoderma
(2020)
Long-term water regime differentiates changes in decomposition and microbial properties in tropical peat soils exposed to the short-term drought
Soil Biology and Biochemistry
Role of recent climate change on carbon sequestration in peatland systems
The Science of the Total Environment
Response of fungal and actinobacterial communities to water-level drawdown in boreal peatland sites
Soil Biology and Biochemistry
Variable effects of labile carbon on the carbon use of different microbial groups in black slate degradation
Geochimica et Cosmochimica Acta
Contribution of plant photosynthate to soil respiration and dissolved organic carbon in a naturally recolonising cutover peatland
Soil Biology and Biochemistry
Bacterial and enchytraeid abundance accelerate soil carbon turnover along a lowland vegetation gradient in interior Alaska
Soil Biology and Biochemistry
Biotic and abiotic factors interact to regulate northern peatland carbon cycling
Ecosystems
Translocation and turnover of rhizodeposit carbon within soil microbial communities of an extensive grassland ecosystem
Plant and Soil
Vegetation composition and soil microbial community structural changes along a wetland hydrological gradient
Hydrology and Earth System Sciences
Belowground biodiversity and ecosystem functioning
Nature
Soil microbial community structure affected by 53 years of nitrogen fertilisation and different organic amendments
Biology and Fertility of Soils
Linking soil microbial communities to vascular plant abundance along a climate gradient
New Phytologist
Biogeochemical plant-soil microbe feedback in response to climate warming in peatlands
Nature Climate Change
Interactive biotic and abiotic regulators of soil carbon cycling: evidence from controlled climate experiments on peatland and boreal soils
Global Change Biology
Soil invertebrates control peatland C fluxes in response to warming
Functional Ecology
Litter decomposition rate and soil organic matter quality in a patchwork heathland of southern Norway
Soils
Effects of plant functional group loss on soil biota and net ecosystem exchange: a plant removal experiment in the Mongolian grassland
Journal of Ecology
Spatial heterogeneity of belowground microbial communities linked to peatland microhabitats with different plant dominants
FEMS Microbiology Ecology
Assessment of anthropogenic pressures on South European Atlantic bogs (NW Spain) based on hydrochemical data
Hydrobiologia
How temporal patterns in rainfall determine the geomorphology and carbon fluxes of tropical peatlands
Proceedings of the National Academy of Sciences
Temperature sensitivity of soil carbon decomposition and feedbacks to climate change
Nature
Plant functional traits and soil carbon sequestration in contrasting biomes
Ecology Letters
Northern peatland carbon dynamics driven by plant growth form — the role of graminoids
Plant and Soil
Climate change drives a shift in peatland ecosystem plant community: implications for ecosystem function and stability
Global Change Biology
Are plant growth-form-based classifications useful in predicting northern ecosystem carbon cycling feedbacks to climate change?
Journal of Ecology
Drought-induced carbon loss in peatlands
Nature Geoscience
Export of dissolved organic carbon from peatlands under elevated carbon dioxide levels
Nature
An enzymic 'latch' on a global carbon store - a shortage of oxygen locks up carbon in peatlands by restraining a single enzyme
Nature
Blanket peat biome endangered by climate change
Nature Climate Change
Peat properties, dominant vegetation type and microbial community structure in a tropical peatland
Wetlands
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