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Impact of Soil-Applied Microbial Inoculant and Fertilizer on Fungal and Bacterial Communities in the Rhizosphere of Robinia Sp

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Impact of Soil-Applied Microbial Inoculant and Fertilizer on Fungal and Bacterial Communities in the Rhizosphere of Robinia Sp Article Impact of Soil-Applied Microbial Inoculant and Fertilizer on Fungal and Bacterial Communities in the Rhizosphere of Robinia sp. and Populus sp. Plantations Zoltán Mayer 1, Andrea Gógán Csorbainé 2, Ákos Juhász 1, Attila Ombódi 2, Antal Pápai 3, Boglárka Kisgyörgy Némethné 3 and Katalin Posta 1,* 1 Department of Microbiology and Applied Biotechnology, Institute of Genetics and Biotechnology, Hungarian University of Agriculture and Life Sciences, Páter Károly Street 1, 2100 Gödöll˝o,Hungary; [email protected] (Z.M.); [email protected] (Á.J.) 2 Institute of Horticulture, Hungarian University of Agriculture and Life Sciences, Páter Károly Street 1, 2100 Gödöll˝o,Hungary; [email protected] (A.G.C.); [email protected] (A.O.) 3 National Food Chain Safety Office, Agricultural Genetic Resources Directorate, Forestry Reproductive Material Department, Kis Rókus Street 15/A, I.19, 1024 Budapest, Hungary; [email protected] (A.P.); [email protected] (B.K.N.) * Correspondence: [email protected] Abstract: The impact of chemical fertilization on rhizosphere soil communities is a growing concern due to the changes they cause on microbes in soil ecosystems. The present study aims to compare my- corrhizal inoculation and fertilizer applications on bacterial and fungal communities in rhizosphere soil of intensively cultivated Robinia pseudoacacia and Populus × euramericana plantations using the Illumina Miseq sequencing platform. Our results revealed that the different host plants and applied Citation: Mayer, Z.; Csorbainé, A.G.; treatments did not significantly affect soil bacterial diversity, but interfered with native rhizosphere Juhász, Á.; Ombódi, A.; Pápai, A.; Némethné, B.K.; Posta, K. Impact of bacterial communities in plantation sites. In contrast, host plants and inorganic fertilizer had a strong Soil-Applied Microbial Inoculant and effect at the family and genus level on the composition of soil fungal communities. In conclusion, our Fertilizer on Fungal and Bacterial findings suggest that the structure and composition of the fungal community are more sensitive to Communities in the Rhizosphere of the nutrient sources in soil than bacteria. Robinia sp. and Populus sp. Plantations. Forests 2021, 12, 1218. Keywords: bacterial community; fungal community; mycorrhizal fungi; black locust; poplar https://doi.org/10.3390/f12091218 Academic Editor: Tiehang Wu 1. Introduction Received: 12 August 2021 Black locust (Robinia pseudoacacia L.) is widely distributed through arid and semiarid Accepted: 5 September 2021 Published: 7 September 2021 regions of North America, Europe and Asia; it is used for high-quality firewood and timber production around the world [1]. In 2019, it was the most used tree species on the continent and covered an area of more than 454,531 hectares from the 1,867,557 hectares of forest Publisher’s Note: MDPI stays neutral 3 with regard to jurisdictional claims in surface in Hungary, this represents 54,676 thousand m of living timber. Black locust is published maps and institutional affil- present in 24.33% of the domestic forest area, but only represents 13.89% of living timber iations. biomass [2]. It was declared as Hungaricum in 2014. The main advantage of black locust plantations is their fast and intensive growth. Nevertheless, it produces different growth intensities in different nutrient-supplied soils. As a result of cultivation on less favourable, i.e., moderately good quality or eroded soils it is only able to produce firewood quality. The species can provide high-quality timber on nutrient-rich and well-aerated soils [3]. Copyright: © 2021 by the authors. Due to these characteristics, it is the most important tree species cultivated in Hungary. Licensee MDPI, Basel, Switzerland. This article is an open access article With its outstandingly intensive pace of development, the black locust reaches its peak distributed under the terms and height in 5 years, while it needs 10 years to reach its maximum in diameter [4,5]. World- conditions of the Creative Commons wide, black locust contributes greatly to soil quality by changing the biodiversity of soil, Attribution (CC BY) license (https:// improving soil chemical properties and fertility [6–10], restoring degraded soils [11,12], creativecommons.org/licenses/by/ increasing the root biomass, and sequestering the organic carbon in soil [13,14]. Biodi- 4.0/). versity enhancement and soil improvement are the results of its ability to form symbiotic Forests 2021, 12, 1218. https://doi.org/10.3390/f12091218 https://www.mdpi.com/journal/forests Forests 2021, 12, 1218 2 of 15 associations with both nitrogen-fixing rhizobia and phosphorus-acquiring mycorrhizal fungi. Binding 75–150 kg ha−1 of atmospheric nitrogen year−1 can significantly increase the available nitrogen content of the soil and affect pH [15,16]. Rising costs of fertilizers and environmental efforts are contributing to a reduction in their use for improving plant growth and yields. Populus x euramericana L. represents the majority of poplar plantations in European countries [17,18]. Part of the European Union’s policy is to produce energy through the use of biomass to mitigate the effects of climate change by reducing greenhouse gas emissions and securing energy supply through diversification of energy sources [19]. Agroforestry has been proposed as an alternative land-use system and is earmarked as a target area for the productive growth of trees such as poplar. In their natural habitats, as well as in plantations, poplars are colonized by ectomycorrhizal fungi, this interaction is important for tree nutrition and can profoundly modulate plant responses to unfavourable environmental conditions [20–22]. Previous studies discussed the mechanism of plant– microbe interactions which affects plant health and soil fertility [23,24]. Mycorrhizal fungal inoculation has the potential to be a useful biotechnological tool that benefits plant devel- opment and health, that increases plant defence mechanisms and alleviates different stress effects [25–33]. In this study, we established black locust and poplar plantation at the same study site in Hungary, to explore the response of the rhizosphere soil bacterial and fungal community after mycorrhizal inoculation and inorganic fertilization. 2. Materials and Methods 2.1. Study Site The plantation study was conducted in Monorierd˝o,Pest County, Hungary (N 47◦300, E 19◦480) (Figure1). The study of the plantation field experiments area has a moderately cold–dry continental climate with 10.5 ◦C annual mean temperature and 500–750 mm annual mean precipitation [34]. Figure 1. Study site of black locust (A) and poplar plantation (B)(https://earth.google.com/web/ @47.30475687,19.48656325,140.81392265a,1194.88813009d,35y,0.00005561h,0.1766107t,-0r, accessed on 29 August 2021). 2.2. Intensively Cultivated Plantations Experiment Setup Black locust and poplar plantation experiments were conducted in two separate parcels with the same soil properties and climate. The parcels were used for experimenta- tion with forestry varieties over the past 20 years. Black locust (one-year-old R. pseudoacacia L. cuttings; OBE01; OBE26; OBE34; OBE53; OBE54; OBE69 varieties) was inoculated at planting time (March 2018) with arbuscular my- corrhizal fungi inoculant labelled in the experiment as ‘III’ (50 g plant−1, 80 propagules g−1 Forests 2021, 12, 1218 3 of 15 Symbivit® produced by Symbiom Ltd., Lanskroun, Czech Republic; www.symbiom.cz, accessed on 4 September 2017), fertilized labelled ‘II’ (70 g plant−1, Osmocote OSM, NPK, 14-7-21, Israel Chemicals, Tel-Aviv, Israel, Pétisó (27% N, 7% CaO, 5% MgO), Superphos- −1 phate (18% P2O5); NPK 9-6-7.5 g plant ) and non-treated plants were used as control ‘I’. We used a randomized block design of three treatments (840 plants treatment−1). Poplar (one-year-old P. x euramericana L. cuttings; SV-778; SV-879; SV-890; I-214; AF-13; AF-28 varieties) was inoculated at planting time (October 2017) with ectomycorrhizal fungi inoculant, labelled as ‘C’ (3 g plant−1, Tuber brumale L.) and fertilized ‘B’ (278 g plant−1, Pétisó (27% N, 7% CaO, 5% MgO)) and non-treated control plants labelled in the experi- ment as ‘A’. The plantation experiment was arranged in a randomized block design with 450 plants treatment−1. One hundred grams of soil sample in five replications of each treatment was collected (soil cores of 5 cm diameter and 25 cm length were collected. The top 5 cm of the cores was removed and the rest was mixed thoroughly) and were used to determine the microbiome of the soil. Sampling was conducted on 12 October 2020 (Figure S1). The height and stem diameter of trees were measured (9 October 2020) (Figure S1). 2.3. Metagenomic Sequencing For a total of 30 soil samples (two plantations × three treatments × five soil samples), DNA was extracted using the Quick DNA Fecal/Soil Microbe Miniprep (ZymoResearch, Irvine, CA, USA) following the manufacturer’s instructions. The quality of the DNA extracted was determined using a nanospectrophotometer (Nanophotometer 2210, Implen, Germany). For sequencing, the DNA extractions from each treatment (five samples) were pooled into one sample. Thus, three pooled samples were sequenced for each plantation (six samples in total). The abundance of the bacterial and fungal communities of soil samples was estimated using high-throughput sequencing of the 16S rRNA gene on the Illumina Miseq platform at UD-GenoMed Ltd. (Debrecen, Hungary). The V3–V4 region of bacterial 16S rRNA gene and the fungal ITS1 region was amplified using universal primers 16S and ITS Amplicon PCR universal primers (Sigma-Aldrich, St. Louis, MI, USA) (Table S1), following the recommendations of the 16S and Fungal Metagenomic Sequencing Library Preparation guides (Illumina, San Diego, CA, USA). The KAPA HiFi Hot Start Ready Mix (KAPA Biosystems, Wilmington, MA, USA; Roche AG, Basel, Switzerland) was used to perform PCR amplification. These samples were denatured at 95 ◦C for 3 min and then amplification was performed using three steps of PCR for 25 cycles, denaturing at 95 ◦C for 30 s, annealing at 55 ◦C for 30 s, extending at 72 ◦C for 30 s.
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