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Root-Associated Bacterial Community Shifts in Hydroponic Lettuce Cultured with Urine-Derived Fertilizer

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Root-Associated Bacterial Community Shifts in Hydroponic Lettuce Cultured with Urine-Derived Fertilizer microorganisms Article Root-Associated Bacterial Community Shifts in Hydroponic Lettuce Cultured with Urine-Derived Fertilizer Thijs Van Gerrewey 1,2 , Christophe El-Nakhel 1,3 , Stefania De Pascale 3 , Jolien De Paepe 2, Peter Clauwaert 2, Frederiek-Maarten Kerckhof 2 , Nico Boon 2 and Danny Geelen 1,* 1 Horticell Lab, Department of Plants and Crops, Ghent University, Coupure Links 653, B-9000 Gent, Belgium; [email protected] (T.V.G.); [email protected] (C.E.-N.) 2 Center for Microbial Ecology and Technology (CMET), Ghent University, Coupure Links 653, B-9000 Gent, Belgium; [email protected] (J.D.P.); [email protected] (P.C.); [email protected] (F.-M.K.); [email protected] (N.B.) 3 Department of Agricultural Sciences, University of Naples Federico II, 80055 Portici, Italy; [email protected] * Correspondence: [email protected] Abstract: Recovery of nutrients from source-separated urine can truncate our dependency on syn- thetic fertilizers, contributing to more sustainable food production. Urine-derived fertilizers have been successfully applied in soilless cultures. However, little is known about the adaptation of the plant to the nutrient environment. This study investigated the impact of urine-derived fertilizers on plant performance and the root-associated bacterial community of hydroponically grown lettuce (Lactuca sativa L.). Shoot biomass, chlorophyll, phenolic, antioxidant, and mineral content were Citation: Van Gerrewey, T.; associated with shifts in the root-associated bacterial community structures. K-struvite, a high- El-Nakhel, C.; De Pascale, S.; De performing urine-derived fertilizer, supported root-associated bacterial communities that overlapped Paepe, J.; Clauwaert, P.; Kerckhof, most strongly with control NPK fertilizer. Contrarily, lettuce performed poorly with electrodialysis F.-M.; Boon, N.; Geelen, D. (ED) concentrate and hydrolyzed urine and hosted distinct root-associated bacterial communities. Root-Associated Bacterial Comparing the identified operational taxonomic units (OTU) across the fertilizer conditions revealed Community Shifts in Hydroponic strong correlations between specific bacterial genera and the plant physiological characteristics, Lettuce Cultured with Urine-Derived salinity, and NO −/NH + ratio. The root-associated bacterial community networks of K-struvite Fertilizer. Microorganisms 2021, 9, 3 4 1326. https://doi.org/10.3390/ and NPK control fertilized plants displayed fewer nodes and node edges, suggesting that good microorganisms9061326 plant growth performance does not require highly complex ecological interactions in hydroponic growth conditions. Academic Editor: José David Flores-Félix Keywords: waste streams; source-separated urine; urine-derived fertilizer; organic fertilizer; nutrient cycling; soilless culture; plant holobiont; microbial community; rhizosphere; PGPR Received: 26 May 2021 Accepted: 15 June 2021 Published: 18 June 2021 1. Introduction Publisher’s Note: MDPI stays neutral Up to half of the world’s food supply depends on the input of mineral fertilizers [1]. with regard to jurisdictional claims in Moreover, a growing population will increase our dependency on fertilizer inputs. Syn- published maps and institutional affil- thetic fertilizer production is scrutinized for its use of non-renewable resources. Phosphorus iations. and potassium fertilizers are mined. The depletion of geological materials and spiking prices jeopardizes the long-term security of P and K [2,3]. The production of N fertilizers starts with the Haber–Bosch synthesis of ammonia. This process requires hydrogen (H2), which is mainly derived from natural gas and is responsible for approximately 1.2% of Copyright: © 2021 by the authors. global energy use [4]. In addition, anthropogenically driven deposition of P and N in Licensee MDPI, Basel, Switzerland. aquatic and terrestrial ecosystems is the main driver for eutrophication [5]. This article is an open access article Transitioning to a closed-loop nutrient cycling approach can sustainably provide distributed under the terms and long-term food security [6]. Human excreta are the primary source of essential nutrients conditions of the Creative Commons in domestic wastewater. Urine contains an estimated 50% of P and 80% of N present in Attribution (CC BY) license (https:// creativecommons.org/licenses/by/ domestic wastewater while accounting for less than 1% of wastewater volume [7]. Source- 4.0/). separation of urine for fertilizer production can reduce the environmental impact compared Microorganisms 2021, 9, 1326. https://doi.org/10.3390/microorganisms9061326 https://www.mdpi.com/journal/microorganisms Microorganisms 2021, 9, 1326 2 of 25 to synthetic fertilizers [7,8]. Hilton et al. [7] assessed that fertilizer production from source- separated urine could reduce greenhouse gas emissions by 47%, energy consumption by 41%, eutrophication potential by 64%, and freshwater use by 50% compared to synthetic fertilizer use. Different techniques exist to recover nutrients from urine [9]. For example, K-struvite precipitation allows for the recovery of K and P [10]. The use of electrodialysis (ED) combined with precipitation and nitrification can recover NPK [11]. Through sponta- neous biological hydrolysis of urea, N can be recovered as ammonia or ammonium [12]. The use of urine-derived fertilizers can be as effective as synthetic fertilizers in supporting plant growth [13–17]. However, the application of urine-derived fertilizers in soilless culture systems has received little attention. El-Nakhel et al. [18] explored the use of urine- derived fertilizers in a soilless culture of Lactuca sativa L. The application of K-struvite and ED-concentrate nutrient solutions resulted in similar growth performance compared to commercial mineral fertilizer. In addition, K, Ca, Mg, and organic acids accumulated + in the lettuce leaves, which can have dietary benefits [18,19]. In contrast, high NH4 lev- els in the hydrolyzed urine nutrient solution resulted in poor growth performance and dark green leaves [18,20,21]. In addition, the high salt content of urine-derived fertiliz- ers can be disadvantageous in soilless systems, especially for a salt-sensitive crop like lettuce [18,22,23]. The root-associated microbial community may be a key factor impacting the effective- ness of urine-derived fertilizers. In the plant holobiont, the complex array of interactions be- tween the plant host and microbes allows them to develop mutually beneficial traits [24,25]. Dynamics between rhizosphere microbes mediate nutrient cycling, potentially influencing plant growth [25,26]. For example, N-fixing microbes, like nodule forming rhizobia, can convert atmospheric N2 to readily available nitrogen for plant uptake [27]. Organic N is converted by microbes into plant-available ammonium and nitrate, though plants can also take up simple organic N compounds like amino acids [28,29]. In addition, certain micro- bial taxa can solubilize phosphorus and iron, improving their plant availability [30,31]. Plants can shape their rhizosphere microbiome to adapt to the environment’s nutrient status to gain benefit over competitors [26]. Other examples of beneficial interactions between the plant host and rhizosphere microbes are the alleviation of salt stress and the protection against pathogens through induced systemic resistance or direct competition between microbes [32–34]. Research on the influence of organic fertilizer on rhizosphere microbial community dynamics in soilless culture is limited [35,36]. In soil, conventional and organic agricultural management practices were shown to differ in rhizosphere microbial community structures, which shifted the rhizosphere N-cycling pathways [37]. The application of microalgal biomass as organic fertilizer in a barley soil pot experiment changed the bacterial and protozoan community structures [38]. In soilless culture, the application of organic fertilizer impacted the functionality and microbial associations in the root zone [35,36]. The soil and soilless culture experiments also identified the plant host as an important driver shaping the root-associated microbial community [35–37]. In addition, the type of growing medium used in soilless culture can affect the microbial community structure [39,40]. The impact of urine-derived fertilizers on the root-associated microbial communities in soilless culture has yet to be elucidated. In this study, we assessed the role of three urine-derived fertilizers (ED concentrate, K-struvite, and hydrolyzed urine) in shaping the root-associated microbial communities of lettuce in soilless culture (Figure1). We asked the following questions: (1) Does the type of urine-derived fertilizer differently affect lettuce phenotype and physiology? (2) Does the application of urine-derived fertilizers result in distinct root-associated bacterial community structures? (3) Are the key members of the community networks correlated to plant phenotype and physiology as affected by the urine-derived fertilizers’ nutrient status? Microorganisms 2021, 9, 1326 3 of 25 Figure 1. Schematic view of the experiment. Source-separated urine was converted into three urine-derived fertilizers: electrodialysis concentrate, K-struvite, and hydrolyzed urine. These urine-derived fertilizers were applied in a soilless culture of Lactuca sativa L. The plant phenotypes, physiological states, and root-associated bacterial communities were evaluated and compared to commercial mineral fertilizer. 2.
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