Elsevier

Applied Soil Ecology

Volume 156, December 2020, 103702
Applied Soil Ecology

Microbial community size is a potential predictor of nematode functional group in limed grasslands

https://doi.org/10.1016/j.apsoil.2020.103702Get rights and content

Highlights

  • Liming had a limited effect on nematode and microbial community structures.

  • Bacterial 16S rRNA gene copy number was a proxy for nematode functional group.

  • Bacterial 16S rRNA gene copy number increased with predacious nematode abundance.

Abstract

Agronomic management practices can impose structural change within soil biotic communities that may negatively impact soil processes including function and biodiversity. Thus, optimizing sustainable crop production that confers minimal impacts on the structure and function of soil biota is an imperative to deliver healthy, functional and resilient production systems. Liming is a management intervention to mitigate soil acidification with a generally positive effect on crop biomass. The application of lime changes soil pH, a known driver of microbial community composition, but it is unknown whether pH derived shifts in bacterial communities result in altered nematode communities. In this study we used qPCR, next generation sequencing and nematode directed T-RFLP to characterise microbial and nematode communities in a liming field trial with a control and three liming applications to incrementally increase pH by 0.5, 0.75 and 1 pH unit. We demonstrate over a 14-month experimental period an interaction between microbial and nematode communities in managed grasslands. Liming had a limited effect on nematode and microbial community structures. However bacterial and archaeal abundance as measured by 16S rRNA gene copy number was found to be a potential predictor of nematode functional group, based on recognized trophic strategies, with increased abundance of omnivorous and predatory nematodes, that are known to prey upon bacterivorous nematodes, with a concomitant increase of 16S rRNA gene copy number. Thus, indirectly suggesting suppression of the bacterial and archaeal community in the presence of bacterivorous nematodes. Where populations of bacterivorous nematodes were highest the relative abundance of both predatory and omnivorous nematodes was lowest. Thus, this study demonstrates clear connectivity between soil microbial and nematode communities in grassland soil.

Introduction

The provision of sufficient nutritious food to underpin a burgeoning population is a well-recognized global imperative (Godfray et al., 2010) compounded by the overarching impact of a changing climate (Hoegh-Guldberg et al., 2018). However, a myriad of barriers to efficient and effective agricultural production exist; an increasing yield gap for many staple crops since the 1980s (Grassini et al., 2013, Grassini et al., 2015), global land degradation and reduced fertility resulting from intensive agriculture (Banwart, 2011; Powlson et al., 2011), and increased urbanisation that has resulted in a smaller global footprint for agricultural production (Lambin and Meyfroidt, 2011; Gibbs and Salmon, 2014). Thus, sustainable approaches to agricultural production need to be adopted (Tilman et al., 2011) though trade-offs and conflicts throughout the production system are inherent (Hawes et al., 2019), for example, the need to balance intensification in grasslands with mitigation of greenhouse gas emissions (Bengtsson et al., 2019).

Notwithstanding the need to sustainably increase production from agricultural systems, there is a concomitant need to mitigate greenhouse gas emissions (GHG) with the agricultural sector being a significant contributor to global greenhouse gas emissions (Hoegh-Guldberg et al., 2018). Grasslands can potentially play an important role in mitigating GHG through sequestering C within the soil, and non-intensively managed grasslands are currently recognized as a globally important C store (Conant et al., 2017). Soil biota drive key soil processes (Bardgett and van der Putten, 2014) delivering multiple societal benefits (Wall et al., 2015). Such benefits include C sequestration and nutrient cycling that provide bioavailable micro- and macronutrients to plants, in both cases the complexity and composition of the biological community may be highly relevant, as has been found for the management of soil P (Mezeli et al., 2020). However, agronomic management can have wide ranging impacts on soil processes including altering the structure of eukaryotic, bacterial and archaeal components of soil communities that may impact soil function and biodiversity and thus soil health (Gardi et al., 2013; Tsiafouli et al., 2015). Therefore, identifying how agronomic practices can impact the structure and function of microorganisms is an imperative to maintaining healthy soil communities, productive crops and thus resilient societies (Bender et al., 2016; Kremen and Merenlender, 2018; El Mujtar et al., 2019; Garibaldi et al., 2019).

One such sustainable agronomic management approach is the application of lime to mitigate the effects of soil acidification (Goulding, 2016) though with potential disbenefits in terms of increased net GHG emissions (Gibbons et al., 2014). In general, it is well established that liming has a positive but inconsistent impact on crop yield biomass (Goulding, 2016) though the relationship is complex and in an arable context potentially crop specific (Holland et al., 2019). This inconsistency of effect is also reflected in grasslands with liming having both positive short and long-term effects (Davies, 1987; Stevens and Laughlin, 1996) typically related to sward composition at species level (Davies, 1987; Bailey, 1997) and no effect (Cregan et al., 1989).

In a recent review of the impact of liming in the UK, Holland et al. (2018) outlined a qualitative framework overlaying a chronological scale and suggested that impacts of the application of liming on “biota” were manifest in weeks/months whereas impacts on “biodiversity” were observed over years/decades. However, the soil microbial community is a high diversity system which encompasses multiple trophic levels each of which will respond to liming both directly and indirectly making it difficult to generalise the response of the soil microbial community.

Nematodes are the most abundant soil biota on earth (van den Hoogen et al., 2019, van den Hoogen et al., 2020) which Holland et al. (2018) postulated based only on four studies to respond, “strongly to liming”, through increased abundance and altered community composition. However, a more comprehensive review of the published literature (Table 1, this study) revealed that nematode abundance responds inconsistently, whereas nematode community composition is consistently altered with the application of liming. What is less well understood is how lime induced changes in bacterial composition can impact other trophic levels in this case nematode composition.

While it is recognized that liming may have effects on nematode community composition through altering soil environmental conditions, liming may also affect nematodes by altering the composition of microbial communities (bacteria and archaea). Liming alters pH, which is known to be a key determinant of microbial community composition (Fierer and Jackson, 2006; Herold et al., 2018) however, it is not known whether pH derived shifts in microbial communities can result in altered nematode communities. Little is known about the explicit (rather than inferred) interactions between multiple trophic levels in the soil microbiome (Neilson et al., 2002; Nielsen et al., 2010; Paterson et al., 2011; Wang et al., 2019) however, it has been suggested that nematodes may show a preference for particular prey (Thakur and Geisen, 2019) leading to the possibility that liming may exert indirect controls on nematode communities. The objectives of this study were therefore to characterise both the soil nematode and microbial (bacterial and archaeal) communities under four different liming treatments in an upland grassland and to determine if changes in nematode community structure were associated with changes in microbial community structure.

We hypothesize that there will be greater divergence between nematode communities as the concentration of lime applied is increased. This will be caused by a mixture of direct pH effects and indirect effects caused by the impacts of pH on the structure of the microbial community.

Section snippets

Experimental design

Twenty-four 5 × 10 m plots were established (August 2017) at the Glensaugh Research Station (operated by the James Hutton Institute), Scotland (latitude: longitude 56.9013: −2.5553, 193 m a.s.l.) on a permanent pasture which last received lime and fertilizer inputs during autumn 2002 and spring 2009, respectively.

The soil was a humus iron podzol (Strichen series), free draining with a stony layer between 10 and 15 cm below the surface, average soil pH across the site was 5.2 (in 0.1 M calcium

Results

Soil pH varied by amount of lime applied (p < 0.001), year (p < 0.001) and days after liming (p < 0.001) (Fig. 1). With pH increasing with increasing amounts of lime, an interactive effect between treatment and days after liming (p < 0.001) was also noted (Fig. 1).

Liming treatment had no impact on the structure of the nematode community as measured by the Basal, Enrichment, Maturity and Structural indices (Fig. 2a–d). However, pH significantly decreased the Enrichment (p < 0.01) and increased

Discussion

Typically, when exploring soil communities, different trophic levels are studied in isolation overlooking the complex and multiple interactions between soil micro-organisms. This study demonstrated an interaction between microbial and nematode communities in a managed grassland subjected to liming. The abundance of bacteria (16S rRNA gene copy numbers) was a predictor of nematode functional group composition with higher 16S rRNA gene copy numbers where omnivorous and predatory nematodes, that

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

This work was funded by the Scottish Government Rural and Environment Science and Analytical Services (RESAS) division through its Strategic Research Programme (RD1.1.1 and RD1.1.2). We thank colleagues of the James Hutton Institute sequencing team for generating nematode T-RFs and bacterial Illumina sequences and Clare Cameron for soil analyses.

References (103)

  • H. Ferris et al.

    A framework for soil food web diagnostics: extension of the nematode faunal analysis concept

    Appl. Soil Ecol.

    (2001)
  • L.A. Garibaldi et al.

    Policies for ecological intensification of crop production

    Trends Ecol. Evol.

    (2019)
  • J.M. Gibbons et al.

    Sustainable nutrient management at field, farm and regional level: soil testing, nutrient budgets and the trade-off between lime application and greenhouse gas emissions

    Agric. Ecosyst. Environ.

    (2014)
  • P. Grassini et al.

    How good is good enough? Data requirements for reliable crop yield simulations and yield-gap analysis

    Field Crops Res.

    (2015)
  • J. Haimi et al.

    Soil decomposer animal community in heavy-metal contaminated coniferous forest with and without liming

    Euro. J. Soil Biol.

    (2002)
  • J.E. Holland et al.

    Liming impacts on soils, crops and biodiversity in the UK: a review

    Sci. Tot. Environ.

    (2018)
  • J.E. Holland et al.

    Yield responses of arable crops to liming – an evaluation of relationships between yields and soil pH from a long-term liming experiment

    Eur. J. Agron.

    (2019)
  • R. Hyvönen et al.

    Effects of lime, ash and nitrogen fertilizers on nematode populations in Scots pine forest soils

    Pedobiologia

    (1989)
  • A. Langarica-Fuentes et al.

    Effect of model root exudate on denitrifier community dynamics and activity at different water-filled pore space levels in a fertilised soil

    Soil Biol. Biochem.

    (2018)
  • P.J. Murray et al.

    Interactions between fertilizer addition, plants and the soil environment: implications for soil faunal structure and diversity

    Appl. Soil Ecol.

    (2006)
  • R. Neilson et al.

    Above-ground grazing affects floristic composition and modifies soil trophic interactions

    Soil Biol. Biochem.

    (2002)
  • H. Okada et al.

    Fungal-feeding habits of six nematode isolates in the genus Filenchus

    Soil Biol. Biochem.

    (2005)
  • E. Paterson et al.

    Altered food web structure and C-flux pathways associated with mineralisation of organic amendments to agricultural soil

    Appl. Soil Ecol.

    (2011)
  • I. Popovici et al.

    Diversity and distribution of nematode communities in grasslands from Romania in relation to vegetation and soil characteristics

    Appl. Soil Ecol.

    (2000)
  • D.S. Powlson et al.

    Soil management in relation to sustainable agriculture and ecosystem services

    Food Policy

    (2011)
  • B. Sieriebriennikov et al.

    NINJA: an automated calculation system for nematode-based biological monitoring

    Eur. J. Soil Biol.

    (2014)
  • D. Stone et al.

    Using nematode communities to test a European scale soil biological monitoring programme for policy development

    Appl. Soil Ecol.

    (2016)
  • L. Su et al.

    Novel soil fumigation strategy suppressed plant-parasitic nematodes associated with soil nematode community alterations in the field

    Appl. Soil Ecol.

    (2017)
  • M.P. Thakur et al.

    Trophic regulations of the soil microbiome

    Trends Microbiol.

    (2019)
  • L. Wiesel et al.

    Determination of the optimal soil sample size to accurately characterise nematode communities in soil

    Soil Biol. Biochem.

    (2015)
  • A. Apprill et al.

    Minor revision to V4 region SSU rRNA 806R gene primer greatly increases detection of SAR11 bacterioplankton

    Aquat. Microb. Ecol.

    (2015)
  • J.S. Bailey

    Some influences of initial sward botanical composition on the responsiveness of Irish grassland to liming

    Irish J. Agr. Res.

    (1997)
  • S.A. Banwart

    Save our soils

    Nature

    (2011)
  • R.D. Bardgett et al.

    Belowground biodiversity and ecosystem functioning

    Nature

    (2014)
  • W. Bassus

    Die nematodenfauna des fichtenrohhumus unter dem einflug der kalkdiingung

    Nematologica

    (1960)
  • J. Bengtsson et al.

    Grasslands - more important for ecosystem services than you might think

    Ecosphere

    (2019)
  • C.B. Blackwood et al.

    Terminal restriction fragment length polymorphism data analysis for quantitative comparison of microbial communities

    Appl. Environ. Microb.

    (2003)
  • N.A. Bokulich et al.

    Optimizing taxonomic classification of marker-gene amplicon sequences with QIIME 2’s q2-feature-classifier plugin

    Microbiome

    (2018)
  • E. Bolyen et al.

    Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2

    Nat. Biotechnol.

    (2019)
  • T. Bongers

    The maturity index: an ecological measure of environmental disturbance based on nematode species composition

    Oecologia

    (1990)
  • M.A. Bradford et al.

    A test of the hierarchical model of litter decomposition

    Nat. Ecol. Evol.

    (2017)
  • D.J.F. Brown et al.

    An examination of methods used to extract virus-vector nematodes (Nematoda: Longidoridae and Trichodoridae) from soil samples

    Nematol. Medit.

    (1988)
  • B.J. Callahan et al.

    DADA2: high-resolution sample inference from Illumina amplicon data

    Nat. Methods

    (2016)
  • R.T. Conant et al.

    Grassland management impacts on soil carbon stocks: a new synthesis

    Ecol. Appl.

    (2017)
  • D. Davies

    Long-term effects of improvement methods on Molinia caerula dominant rough grazing on wet hill land. 1. Pasture production, quality and botanical composition

    J. Agr. Sci.

    (1987)
  • P.C.E.M. de Rooij-van der Goes et al.

    Analysis of nematodes and soil-borne fungi from Ammophila arenaria (Marram grass) in Dutch coastal foredunes by multivariate techniques

    Eur. J. Plant Pathol.

    (1995)
  • H. Deng et al.

    Long-term effect of re-vegetation on the microbial community of a severely eroded soil in sub-tropical China

    Plant Soil

    (2010)
  • S. Donn et al.

    Greater coverage of the phylum Nematoda in SSU rDNA studies

    Biol. Fert. Soils

    (2011)
  • S. Donn et al.

    A novel molecular approach for rapid assessment of soil nematode assemblages – variation, validation and potential applications

    Methods Ecol. Evol.

    (2012)
  • N. Fierer et al.

    The diversity and biogeography of soil bacterial communities

    P. Natl. Acad. Sci. USA

    (2006)
  • Cited by (0)

    View full text