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