Microbial “hotspots” of organic matter decomposition in temperate peatlands are driven by local spatial heterogeneity in abiotic conditions and not by vegetation structure

https://doi.org/10.1016/j.soilbio.2021.108501Get rights and content

Highlights

  • Peat microbial communities were more strongly linked to microclimatic conditions than to vegetation.

  • More aerobic and warmer soils under shrubs accelerated fungal driven decomposition and CO2 emissions.

  • Decreases in Gram-negative bacteria under grasses promoted C losses as DOC.

  • In the absence of abiotic stress, more C was retained (i.e. under mosses and sedges).

  • We propose temperate peatlands as ‘ecosystem sentinels’ for climate-mediated impacts on the C cycle.

Abstract

Climate change is triggering rapid shifts in plant communities and alterations in soil abiotic conditions in peatlands, with cascading effects on belowground decomposers and ecosystem C turnover. However, elucidating the dominant causal relationships between plant communities, soil biota and C fluxes in these vulnerable ecosystems requires a better understanding of the spatio-temporal variability of abiotic and biotic drivers. In this study we investigated the effects of biotic (plant functional types, PFTs) and abiotic factors (soil temperature and soil moisture) in determining dynamic patterns of soil microbial community structure and C cycling. Four representative temperate peatland habitats were selected based on their peat forming vegetation – an Atlantic wet heathland, two active blanket bogs with herbaceous plants (Molinia caerulea and Eriophorum angustifolium), and a transition mire dominated by Sphagnum mosses located along an altitudinal gradient to include the natural variations in soil temperature and water content regimes. We found that peat microbial communities were more strongly linked to local abiotic conditions than to the dominant above-ground vegetation. Aerobic conditions and warmer temperatures accelerated fungal driven decomposition and CO2 emissions under shrubs, whereas decreases in Gram−negative bacteria promoted increased C losses under Molinia. These findings suggest that small spatial differences in abiotic conditions can create local “hotspots” of organic matter decomposition. We propose that temperate peatlands should be considered as ‘ecosystem sentinels’ for climate change, acting as early-warning indicators of climate-carbon feedbacks.

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)

  • M.J. Kwon et al.

    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

    (2013)
  • P.H. Lunt et al.

    Role of recent climate change on carbon sequestration in peatland systems

    The Science of the Total Environment

    (2019)
  • K. Peltoniemi et al.

    Response of fungal and actinobacterial communities to water-level drawdown in boreal peatland sites

    Soil Biology and Biochemistry

    (2009)
  • A.G. Seifert et al.

    Variable effects of labile carbon on the carbon use of different microbial groups in black slate degradation

    Geochimica et Cosmochimica Acta

    (2011)
  • C.J. Trinder et al.

    Contribution of plant photosynthate to soil respiration and dissolved organic carbon in a naturally recolonising cutover peatland

    Soil Biology and Biochemistry

    (2008)
  • M.P. Waldrop et al.

    Bacterial and enchytraeid abundance accelerate soil carbon turnover along a lowland vegetation gradient in interior Alaska

    Soil Biology and Biochemistry

    (2012)
  • A. Armstrong et al.

    Biotic and abiotic factors interact to regulate northern peatland carbon cycling

    Ecosystems

    (2015)
  • W.K. Balasooriya et al.

    Translocation and turnover of rhizodeposit carbon within soil microbial communities of an extensive grassland ecosystem

    Plant and Soil

    (2014)
  • W.K. Balasooriya et al.

    Vegetation composition and soil microbial community structural changes along a wetland hydrological gradient

    Hydrology and Earth System Sciences

    (2008)
  • R.D. Bardgett et al.

    Belowground biodiversity and ecosystem functioning

    Nature

    (2014)
  • G. Borjesson et al.

    Soil microbial community structure affected by 53 years of nitrogen fertilisation and different organic amendments

    Biology and Fertility of Soils

    (2012)
  • L. Bragazza et al.

    Linking soil microbial communities to vascular plant abundance along a climate gradient

    New Phytologist

    (2015)
  • L. Bragazza et al.

    Biogeochemical plant-soil microbe feedback in response to climate warming in peatlands

    Nature Climate Change

    (2013)
  • M.J.I. Briones et al.

    Interactive biotic and abiotic regulators of soil carbon cycling: evidence from controlled climate experiments on peatland and boreal soils

    Global Change Biology

    (2014)
  • N. Carrera et al.

    Soil invertebrates control peatland C fluxes in response to warming

    Functional Ecology

    (2009)
  • G. Certini et al.

    Litter decomposition rate and soil organic matter quality in a patchwork heathland of southern Norway

    Soils

    (2015)
  • D. Chen et al.

    Effects of plant functional group loss on soil biota and net ecosystem exchange: a plant removal experiment in the Mongolian grassland

    Journal of Ecology

    (2016)
  • A. Chroňáková et al.

    Spatial heterogeneity of belowground microbial communities linked to peatland microhabitats with different plant dominants

    FEMS Microbiology Ecology

    (2019)
  • C. Cillero et al.

    Assessment of anthropogenic pressures on South European Atlantic bogs (NW Spain) based on hydrochemical data

    Hydrobiologia

    (2016)
  • A.R. Cobb et al.

    How temporal patterns in rainfall determine the geomorphology and carbon fluxes of tropical peatlands

    Proceedings of the National Academy of Sciences

    (2017)
  • E.A. Davidson et al.

    Temperature sensitivity of soil carbon decomposition and feedbacks to climate change

    Nature

    (2006)
  • G.B. De Deyn et al.

    Plant functional traits and soil carbon sequestration in contrasting biomes

    Ecology Letters

    (2008)
  • C.M. Dieleman et al.

    Northern peatland carbon dynamics driven by plant growth form — the role of graminoids

    Plant and Soil

    (2017)
  • C.M. Dieleman et al.

    Climate change drives a shift in peatland ecosystem plant community: implications for ecosystem function and stability

    Global Change Biology

    (2015)
  • E. Dorrepaal

    Are plant growth-form-based classifications useful in predicting northern ecosystem carbon cycling feedbacks to climate change?

    Journal of Ecology

    (2007)
  • N. Fenner et al.

    Drought-induced carbon loss in peatlands

    Nature Geoscience

    (2011)
  • C. Freeman et al.

    Export of dissolved organic carbon from peatlands under elevated carbon dioxide levels

    Nature

    (2004)
  • C. Freeman et al.

    An enzymic 'latch' on a global carbon store - a shortage of oxygen locks up carbon in peatlands by restraining a single enzyme

    Nature

    (2001)
  • A.V. Gallego-Sala et al.

    Blanket peat biome endangered by climate change

    Nature Climate Change

    (2013)
  • N.T. Girkin et al.

    Peat properties, dominant vegetation type and microbial community structure in a tropical peatland

    Wetlands

    (2020)
  • Cited by (10)

    • Alder encroachment alters subsoil organic carbon pool and chemical structure in a boreal peatland of Northeast China

      2022, Science of the Total Environment
      Citation Excerpt :

      This huge organic C pool is primarily ascribed to the extremely slow organic matter decomposition rate because plant productivity is low in boreal peatlands (Page and Baird, 2016). In general, microbial decomposition of organic matter is believed to be predominantly suppressed by the cool temperature, high water table levels, and acidic, anoxic, and nutrient-poor conditions (Bragazza et al., 2012; Briones et al., 2022; Da Silva et al., 2022). Recently, there has been a growing recognition that plant community composition is a key factor controlling soil organic C pool and stability through the quantity and quality of plant litter inputs (Dorrepaal et al., 2005; Ward et al., 2014; Antala et al., 2022).

    • Evaluation of the wider applications of the alkanol index BNA<inf>15</inf> as temperature proxy in a broad distribution of peat deposits

      2022, Organic Geochemistry
      Citation Excerpt :

      In peatlands, there are diverse micro-habitats, including hummocks, hollows, lawns, and pools (Lehmann et al., 2016). Peat-forming plants and microbes and the associated biogeochemical cycles are also micro-habitat dependent (e.g., Lehmann et al., 2016; Chroňáková et al., 2019; Briones et al., 2022; Chen et al., 2022). In this context, it is reasonable to assume that the source and preservation of alkan-1-ols will change on micro-habitat scales and likely drives the observed heterogeneity in biomarker distribution.

    View all citing articles on Scopus
    View full text