Effects of synthetic fertilizer and farm compost on soil nematode community in long-term crop rotation plots: A morphological and metabarcoding approach

PLOS ONE RESEARCH ARTICLE Effects of synthetic fertilizer and farm compost on soil nematode community in long-term crop rotation plots: A morphological and metabarcoding approach Gisèle L. Herren ID1*, Joos Habraken1, Lieven Waeyenberge ID2, Annelies Haegeman2, Nicole Viaene1,2, Mathias Cougnon3, Dirk Reheul3, Hanne Steel1, Wim Bert ID1 a1111111111 a1111111111 a1111111111 a1111111111 a1111111111 1 Nematology Research Unit, Department of Biology, Ghent University, Ghent, Belgium, 2 Plant Sciences Unit, ILVO – Flanders Research Institute for Agriculture, Fisheries and Food, Merelbeke, Belgium, 3 Research Unit Plant Breeding and Sustainable Crop Production, Department of Plants and Crops, Faculty of Bioscience and Engineering, Ghent University, Ghent, Belgium * Abstract OPEN ACCESS Citation: Herren GL, Habraken J, Waeyenberge L, Haegeman A, Viaene N, Cougnon M, et al. (2020) Effects of synthetic fertilizer and farm compost on soil nematode community in long-term crop rotation plots: A morphological and metabarcoding approach. PLoS ONE 15(3): e0230153. https://doi. org/10.1371/journal.pone.0230153 Editor: Remigio Paradelo Núñez, Universidade de Santiago de Compostela, SPAIN Received: December 2, 2019 Accepted: February 22, 2020 Published: March 17, 2020 Copyright: © 2020 Herren et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Data Availability Statement: All relevant data for morphological identification is within the manuscript and its Supporting Information files, and metabarcoding data submitted to the Sequence Read Archive (SRA) of NCBI under BioProject PRJNA607002. Soil biodiversity plays a key regulation role in the ecosystem services that underpin regenerative sustainable agriculture. It can be impacted by agricultural management techniques, both positively (through measures such as compost application) and negatively (through, for example, application of synthetic nitrogen). As one of the most numerous members of the soil biota, nematodes are well established as indicators for the soil food web. However, compost application also includes the addition of nematodes present in compost and their subsequent survival in soil is unknown. Nematode communities within the compost applied to soil, and nematode communities in the soil of a multi-year rotational cropping field trial in Melle (Belgium) were studied using morphological and metabarcoding techniques. Compost (C) and nitrogen fertilizer (NF) treated plots were compared. Three replicate plots were investigated for each of the following treatments: C application only; C and NF application; NF only; no C and no NF (control). Plots were sampled six times between 2015–2017, before and after C or NF were added each spring and after crop harvest (except for 2017). NF treatment resulted in a significant decrease of fungal feeding and predatory nematodes, while herbivorous nematodes were positively affected. Remarkably, we did not find compost addition to exert any noticeable effects on the soil nematode community. The morphological and metabarcoding data resulted in different results of the nematode community composition. However, trends and patterns in the two data sets were congruent when observed with NMDS plots and using the nematode maturity index. Metabarcoding of individual compost nematode taxa demonstrated that nematodes originating from compost did not persist in soil. Funding: G.L.H acknowledges FWO (the Research Foundation – Flanders)- for a PhD grant (11W0918N). https://www.fwo.be. Hanne Steel acknowledges special research fund UGent for her PLOS ONE | https://doi.org/10.1371/journal.pone.0230153 March 17, 2020 1 / 19 PLOS ONE post-doc grant. https://www.ugent.be The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing interests: The authors have declared that no competing interests exist. Effects of synthetic fertilizer and farm compost on soil nematode community in long-term crop rotation plots Introduction Soil biodiversity is known to play a key role in regulating the delivery of many ecosystem goods and services, including primary production, decomposition, water purification, erosion control, biological pest control, and plant disease [1–4]. A key component of soil biological health is the diversity of soil biota species within function classes performing these ecosystem services. The rates and magnitudes of these ecosystem services are determined by the composition and abundance of the diverse soil biota [5,6]. The assemblages of soil biota found in agricultural soils are known to be sensitive to management practices such as tillage, organic and inorganic amendments, pesticides and herbicides application and can be influenced by crop rotation since soil biota assemblages can be crop-specific [7–10]. It is also now well established that agricultural intensification of soils reduces soil biodiversity [11]. However, there is an intriguing suggestion that soil biota could be manipulated for certain desired outcomes in agricultural management, a process dubbed “soil ecological engineering” [12]. One potential method of soil ecological engineering involves the use of management practices such as mulching and compost application versus synthetic nitrogen application, additives that are known to have a direct impact on soil biota. The biological health of agricultural soils in particular has been shown to increase crop yields through farm compost amendments [13,14]. Soil nematodes are a crucial component of soil biota as they are among the most numerous and diverse organisms found in agricultural soils [15]. Nematodes are present on all trophic levels, ranging from primary consumers to specialist predators [16]. In addition to being ubiquitous, nematodes react measurably to disturbances, and furthermore are easily allocated to trophic groups and identified into functional groups, making them ideal indicators for the soil food web [15,17,18]. Nematode-based weighted indices incorporate functional roles and life history strategies, and as such provide information about the nematode community structure in stressed, enriched, stable, structured and decomposition environments, and provide important information on the dynamics of soil food webs [19–21]. Synthetic fertilizers have been shown to have a large impact on nematode community structure by decreasing fungivorous nematode abundance compared to manure application [22]. In compost-treated soil, total nematode density has been found to increase, with a particular increase of bacterivorous, fungivorous and predacious nematodes [22,23]. However, compost is usually treated as an organic material that benefits the soil, not as a complex matrix with its own biological properties. Thus, (...truncated)