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Aerobes and phototrophs as microbial organic fertilizers: Exploring mineralization, fertilization and plant protection features

['Eva Wambacq', 'Department Of Plants', 'Crops', 'Faculty Of Bioscience Engineering', 'Ghent University', 'Ghent', 'Research Centre Agrofoodnature', 'School Of Bioscience', 'Industrial Technology', 'University Of Applied Sciences']

Date: 2022-02 

Organic fertilizers and especially microbial biomass, also known as microbial fertilizer, can enable a paradigm shift to the conventional fertilizer-to-food chain, particularly when produced on secondary resources. Microbial fertilizers are already common practice (e.g. Bloom ® and Synagro); yet microbial fertilizer blends to align the nutrient release profile to the plant’s needs are, thus far, unexplored. Moreover, most research only focuses on direct fertilization effects without considering added value properties, such as disease prevention. This study has explored three promising types of microbial fertilizers, namely dried biomass from a consortium of aerobic heterotrophic bacteria, a microalga (Arthrospira platensis) and a purple non-sulfur bacterium (Rhodobacter sphaeroides). Mineralization and nitrification experiments showed that the nitrogen mineralization profile can be tuned to the plant’s needs by blending microbial fertilizers, without having toxic ammonium peaks. In a pot trial with perennial ryegrass (Lolium perenne L.), the performance of microbial fertilizers was similar to the reference organic fertilizer, with cumulative dry matter yields of 5.6–6.7 g per pot. This was confirmed in a pot trial with tomato (Solanum lycopersicum L.), showing an average total plant length of 90–99 cm after a growing period of 62 days for the reference organic fertilizer and the microbial fertilizers. Moreover, tomato plants artificially infected with powdery mildew (Oidium neolycopersici), a devastating disease for the horticultural industry, showed reduced disease symptoms when A. platensis was present in the growing medium. These findings strengthen the application potential of this novel class of organic fertilizers in the bioeconomy, with a promising match between nutrient mineralization and plant requirements as well as added value in crop protection.

Funding: The authors kindly acknowledge (i) the MIPi-Cleantech Flanders (Milieu-innovatieplatform; Environment innovation platform) project Microbial Nutrients on Demand (MicroNOD) for financial support, (ii) the project ’Saraswati 2.0’ (821427) funded by the European Union’s Horizon 2020 Research and Innovation programme, for financial support of A.A., (iii) the project ‘PurpleRace’ (40207) funded by IOF (Industrieel onderzoeksfonds) from the University of Antwerp for financial support of A.A, (iv) the Research Foundation Flanders (Fonds Wetenschappelijk Onderzoek - Vlaanderen) for supporting A.A. with a postdoctoral fellowship (12W0522N) and (v) the DOCPRO4project ‘PurpleTech’, funded by the BOF (Bijzonder onderzoeksfonds; Special research fund) from the University of Antwerp for financially supporting J.S. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Introduction

Our industrialized global society is heavily dependent on synthetic inorganic fertilizers for primary crop production in both agriculture and horticulture. It is estimated that over 110 million tons of N fertilizer (e.g. ammonium nitrate, ammonium sulfate and urea), 10.3 million tons of P and 15.6 million tons of K are annually consumed [1, 2]. Intensive fertilizer use has, however, serious environmental and economic repercussions [3]. When fertilizers are applied to the soil or in growing media (GM) for agricultural and horticultural applications, they are not completely consumed by plants, yet suffer from inefficiencies such as leaching, runoff and volatilization. For every 100 units of fertilizer applied to the land, only 4–14 units of nitrogen and 17 units of phosphorus are eventually consumed by humans [4–6]. A considerable portion of these fertilizers ultimately end up in the environment, resulting in detrimental effects on water quality (e.g. eutrophication), air quality (e.g. emissions of ammonia and nitrous oxide), the greenhouse gas balance (e.g. nitrous oxide), biodiversity and soil quality (e.g. acidification of soils) [7, 8].

Recycling nutrients from secondary resources may offer an improvement to the overall efficiency of the fertilizer-to-food chain [9]. Solid and liquid by-products and residues from plant and animal origin, such as animal manures, animal slurries, blood meal, cocoa shells, soybean meal and organic waste from restaurants and supermarkets play a central role [10]. These so-called organic fertilizers slowly release nutrients through decomposition or decay imposed by the microbiome present in the growing medium or the soil [11]. Organic fertilizers may provide benefits for the soil, such as better water retention, improved nutrient retention and an increase in the organic matter content of the soil, which on its account buffers the soil against salinity, pH changes and pesticides [12–15]. These organic fertilizers contribute to 5% of the total fertilizer market, yet their share will become more significant, as their annual growth rate was around 14% in 2019 compared to only 4% for the total fertilizer market [16].

Microbial fertilizers constitute a novel and promising class of organic fertilizers based on using microbial biomass as a source of plant nutrients [17, 18]. The microbes can be produced on secondary resources such as industrial wastewater, sewage, manure, etc [19, 20]. Microbial biomass can serve as a multi-nutrient fertilizer mainly rich in nitrogen (7–9 g N 100 g-1 dry matter) with an elemental composition of C 4.2 O 1.8 H 0.8 NP 0.2 S 0.1 K 0.1 [18, 21]. In principle, dried microbial biomass produced on secondary resources is mixed with a growing medium or soil [17, 18]. The microbiome present in the growing medium or soil will then mineralize the microbial biomass, thereby making nutrients available for plant growth [11].

Three types of microbial fertilizers are generally considered for microbial fertilizer production on secondary resources: (i) a consortium of aerobic heterotrophic bacteria (AHB); [22], (ii) photoautotrophic microalgae (MA); [23, 24] and (iii) photoheterotrophic purple non-sulfur bacteria (PNSB); [17, 18, 25, 26]. AHB are probably the most widely applied and explored microbial fertilizers. A very common type of AHB is treated and stabilized sewage sludge a.k.a. biosolids (Bloom® and Synagro). In Europe, for example, around 10 million tons dry matter is annually produced [27]. Extensive research has been performed on the mineralization and fertilization properties of biosolids. A review of 32 studies by Rigby, Clarke showed that the mineralizable nitrogen decreased with increasing biological stabilization [28]. In terms of fertilization, increased crop yields have been reported for different plants such as rice, radish, wheat and barley [29]. Added value properties such as plant protection have, according to the authors’ knowledge, not yet been reported.

MA have also been explored as a microbial fertilizer, yet not as extensively as AHB. The mineralization of different types of MA has been studied, showing different final plant-available N fractions for Nannochloropsis biomass (31% after 95 days); [24], microalgal bacterial flocs (25% after 95 days); [8, 30], Arthrospira platensis biomass (72% N after 77 days); Spanoghe, Grunert (18) and algal biomass grown on manure effluents (41% after 63 days). In terms of fertilization, several plants have been explored such as cucumber and cord seedlings, parsley (Petroselinum crispum), petunia and tomato (Solanum lycopersicum L.), showing an equal or improved performance compared to commercial inorganic and/or organic fertilizers [8, 18, 24, 30]. Relatively to AHB, added value properties of MA and their extracts have extensively been reported in terms of (a)biotic plant protection (e.g. antifungal, bacterial and antinematodal activity, alleviation of drought and salt stress) and biostimulation (e.g. increase in germination rate, salt tolerance, nutritional value, etc.) [31].

PNSB are probably the most novel type of microbial fertilizer. Mineralization studies on PNSB biomass are, however, limited to our previous research on Rhodobacter sphaeroides. A final plant-available N fraction of 70% was observed after 77 days [18]. Also, as fertilizer, only a few plants were tested such as pasture ryegrass (Lolium rigidum Gaudin), mandarine tree (Citrus reticulata) and parsley (Petroselinum crispum) [18, 20, 32]. Nonetheless, all results showed a positive or comparable effect of PNSB biomass on plant growth or fruit quality and production relative to the control [18, 20, 32]. In terms of added value properties of PNSB for plants, multiple researchers have reported growth promotion and alleviation of environmental stress [17].

Although AHB, MA and PNSB have been studied as a source of microbial fertilizers, research is mainly limited to their individual contribution to plant growth. Our previous research is one of the first to study blends and indicated that it is economically sensible because it can provide cheap nutrients and added value for plants [18]. The goal of this study was to gain a broader understanding of the applicability across horticultural and agricultural for microbial fertilizers based on AHB, MA and PNSB, both individually as well as in blends. First, nitrogen mineralization and nitrification profiles were determined in a commercially relevant growing medium. Second, the fertilization effect of the microbial fertilizers was evaluated on the plant growth performance in pot trials with perennial ryegrass (Lolium perenne L.) and tomato. Third, disease susceptibility towards a biotrophic fungus (Oidium neolycopersici) and two necrotrophic fungi (i.e. Alternaria solani and A. alternata) was assessed for tomato, to explore added value properties of the three microbial fertilizers.

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