Plant Growth Promoting Microorganisms in Soilless Systems: History
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Contributor:
Snezhana Mourouzidou
,
Georgios K. Ntinas
,
Aphrodite Tsaballa
,
Nikolaos Monokrousos

Soilless systems, such as hydroponics and aquaponics, are gaining popularity as a sustainable alternative to traditional soil-based agriculture, aiming at maximizing plant productivity while minimizing resource use. Plant growth-promoting microorganisms (PGPM) have emerged as a promising solution to overcome these issues. Bacillus, Pseudomonas, and Azospirillum are the most extensively studied genera for their effectiveness as growth promoters, inducing changes in root architecture morphology. Furthermore, PGPM inoculation, either alone or in synergy, can reverse the effects of nutrient deficiency and salt stress. The genera Pseudomonas and Trichoderma were recognized for their solid antagonistic traits, which make them highly effective biocontrol agents in hydroponic systems. The findings indicate their ability to significantly reduce disease severity index (DSI) through mycoparasitism, antibiosis, and induced systemic resistance. In aquaponic systems, the inoculation with Bacillus subtilis and Azospirillum brasilense demonstrated increased dissolved oxygen, improving water quality parameters and benefiting plant and fish growth and metabolism. 

  • hydroponics
  • aquaponics
  • beneficial microorganisms
  • biological control agents
  • Soilless
  • PGPR
  • AMF

1. Introduction

In the context of sustainability goals, it is essential to assess suitable instruments to facilitate the transition towards a resilient agricultural model that balances trade-offs between sustainability and intensification. The growing global population and food and water security concerns necessitate solutions prioritizing environmental sustainability and efficient production [1]. Farmers worldwide face significant challenges in meeting food production demands while mitigating the worsening state of the land caused by intensification. To ensure a sustainable food supply, there is a need to shift the focus from solely maximizing crop production to innovative and precise agriculture practices. Moreover, the predicted climate scenarios pose a considerable risk, particularly in regions heavily dependent on weather and seasonal changes. Nutrient-depleted soils, soil degradation, and water pollution are already a reality and are expected to worsen in the future [2]. Considering the trajectory of agriculture through the lenses of environmental sustainability and food security, soilless systems present an attractive option. These systems can reduce the negative impact of resource depletion and climate dependency, enabling the achievement of desired sustainability goals.
Soilless cultures can address numerous agricultural issues by improving water and nutrient use efficiency, promoting production sustainability, and adapting to the circular economy [3]. Consequently, soilless farming offers excellent potential for agriculture to achieve an environmentally friendly future and overcome challenges related to food security and quality control [4]. Growing crops in a medium other than soil is referred to as a soilless system, which includes hydroponics, a controlled environment agriculture based on substrate culture instead of soil for crop production [5][6]. Hydroponics allows for precise supply and regulation of the nutrient solution (NS) in the plants’ rhizosphere, reducing problems related to soil pollution, enabling shorter crop cycles, and faster plant growth. Furthermore, this system is more efficient and accurate in regard to the use of water and fertilizers [6]. Hydroponics can be categorized into open and closed systems and varies in media used for crop growth, including liquid medium, organic (peat, rice husk, coco coir), and inorganic (rockwool, perlite, vermiculite, pumice) [7]. Soilless systems are known for their advantageous control over the microclimate, making them suitable for areas where agricultural production is typically challenging, such as degraded land, eroded soil, contaminated or acidified and salinized soil, and areas with a cold or deserted climate. This eliminates dependency on the season and geographical location [7]. In recent years, aquaponics, a type of hydroponics that combines fish and crop cultivation, has become an attractive form of precision farming [8]. This system utilizes fish effluent as the nutrient medium for plant growth, resulting in no or partial fertilization [9]. The coupled aquaponic system includes a unidirectional water flow from the fish to a hydroponic unit, which completes the cycle by returning to the fish tanks. In contrast, the decoupled system separates the aquaponic and hydroponic units, and the water flow does not return to the fish [10]. This type of farming is considered highly resource-efficient, providing control over essential elements required for crop and fish growth, and is not limited to growing seasons [11].
Meeting environmental and economic sustainability regulations has become increasingly important in modern agriculture. As a result, farmers are exploring alternative methods to increase production while minimizing negative environmental impacts. One promising solution is using Plant Growth Promoting Microorganisms (PGPM) in hydroponic systems. PGPM have been shown to improve plant performance and yield while addressing issues such as inadequate water quality that can cause soluble salt damage and nutrient imbalances. Moreover, salinity stress is a major challenge in hydroponic systems, negatively affecting plant growth and microbial populations. Halotolerant PGPM effectively enhance plant response to salinity stress [12]. Furthermore, using PGPM can help address plant protection challenges in soil-free systems. In contrast to soil-based agriculture, hydroponic systems create an environment that fosters pathogen proliferation. Therefore, integrated pest and disease management (IPDM) can be particularly challenging in hydroponic systems, and traditional chemical control methods may be detrimental to the overall system. Due to this, biological control methods such as PGPM are gaining attention as promising chemical control alternatives. While chemical control methods such as fungicides and nematicides are still commonly used in soil and soilless systems, their effectiveness, as well as availability of fungicides applicable to soilless cultures, is often limited [13]. Therefore, biological control methods such as PGPM offer a promising solution for sustainable pest and disease management in hydroponic systems.

2. PGPM as Plant-Promoting Growth Treatment and Facilitation of Nutrient Uptake

The potential of PGPM to enhance crop growth is widely recognized, as they can improve plant performance by promoting the mineral nutrient acquisition and converting unavailable nutrients into available forms [14]. Bacillus, Pseudomonas, and Azospirillum are the most extensively studied genera for their effectiveness as growth promoters in soilless cultivation systems, with species such as Bacillus subtilis, Bacillus licheniformis, Pseudomonas fluorescens, and Azospirillum brasilense among the most commonly tested. These PGPM have demonstrated their ability to solubilize nutrients, which is particularly promising for increasing nutrient reuse efficiency in soilless systems, such as hydroponics and aquaponics [15]. In hydroponics, soil-related issues such as phosphate precipitation can also occur. In a study by Cerozi and Fitzsimmons [16], the introduction of various Bacillus spp. into aquaponics resulted in a significant increase in orthophosphate concentration and subsequent P accumulation. PGPM-mediated P solubilization is achieved by releasing mineral-dissolving compounds, such as organic acids, that can chelate cations bound to phosphate, converting it into a readily available form for crop uptake [17][18].
PGPM can be applied in various ways. The most straightforward technique is to add a bio-inoculant directly to the NS or the growing medium. In aquaponic systems, the bio-inoculant can also be introduced into the biofilter or sump component [19]. An overview of PGPM addition to the aquaponic system, which combined the growth of seabass (Lates calcarifer) and basil, showed the alteration of root morphology of inoculated plants through auxin-IAA production by Azospirillum brasilense. This alteration extended the absorption area of water and minerals from the surrounding environment, resulting in improved physiological parameters of basil yield [20]. Similarly, in sweet basil, the impact was seen on the accumulation of sulfur (S) at the leaf level and increased iron (Fe) and phosphorus (P) concentration, doubling the plants’ biomass [21]. Mia et al. [22] correlated banana plantlets’ enhanced performance and the growth promoter’s trait to improve nutrient accumulation, demonstrating the potential to decrease the amount of nitrogen (N) fertilizer and compensate for the N concentration in non-inoculated plants. Recent studies have shown that applying A. brasilense in consortium with Trichoderma harzianum enhanced leaf nutrient concentration, resulting in overall yield growth (by 10.91%) and better mass accumulation as dry root matter and chlorophyll index [23]. 
There is ample evidence of the ability of PGPM to promote plant growth under stress conditions while remaining metabolically active. For instance, Lee et al. [24] established a relationship between increased weight and length of lettuce and the upregulation of genes related to plant growth when Pseudomonas chlororaphis was introduced. Similarly, the beneficial traits of Pseudomonas agglomerans, when applied with Bacillus pyrocinnia, were attributed to P solubilization, 1-aminocyclopropane-1-carboxylic acid (ACC) deaminase activity, and siderophore production [25].
The genus Bacillus showed a range of responses in hydroponic experiments with the existing factor of salinity stress or N-free conditions. Mia et al. [22] determined that Bacillus sphaericus can be used as a viable alternative to commercial nitrogen fertilizers, as it has been shown to increase nitrogen concentration in both roots and leaves, resulting in improved production of primary, secondary, and tertiary roots, greater leaf area, and higher total chlorophyll content. Bacillus subtilis was determined to directly enhance nutrient acquisition in tomato plants, resulting in increased overall tomato yield (by 13.7%), consistent with the results of Kidoglu et al. [26], who reported augmented tomato yield by 36% when inoculated with Bacillus spp. [27].
Although the combination of AMF with other beneficial microorganisms has demonstrated significant results, single-type inoculation can also serve as a growth promoter. For example, Rhizophagus irregularis, when used in a hydroponic float system, altered the biometrical characteristics of tomato tissues, leading to immense total dry weight and root length, mainly by facilitating nutrient uptake with high N and P accumulation [28].

3. PGPM for Alleviation of Salinity Stress

The use of PGPM also has interesting implications in reversing the adverse effects of salt stress commonly observed in hydroponic systems. This stress negatively affects crop growth by creating an osmotic effect due to the accumulation of excess salt in the growing medium, leading to limitations in water uptake by roots [29]. Five studies investigated the efficacy of the genus Bacillus in promoting plant growth and mitigating the impact of salinity on crops. Seifi et al. [30] determined that B. subtilis exhibited a halotolerant characteristic that reduces the synthesis of ethylene hormone, resulting in positive lettuce responses (both physiological and photosynthetic) to high electrical conductivity (EC) in irrigation water in a hydroponic system. Moncada et al. [31] demonstrated that Bacillus amyloliquefaciens reversed the reduction in lettuce biomass caused by salinity through changes in phytohormone content, antioxidant defense mechanisms, osmolyte production, and ACC deaminase activity. Bacillus amyloliquefaciens also showed potential as a stress alleviator by enhancing nutrient uptake and proline accumulation in crops subjected to saline conditions and inducing antioxidant levels [12].

4. PGPM as Biocontrol Agents

The potential of PGPR, PGPF, and endophytes as biocontrol agents against pathogens and diseases in soilless systems has been investigated in several studies conducted over the past twenty years. Among these studies, eight have focused on PGPR, eight on PGPF, and three on endophytes. The shift from soil-based farming to hydroponic systems presents a significant risk of disease outbreaks caused by aquatic-adapted pathogens such as Fusarium, Pythium, and Phytophthora species. These pathogens can produce zoospores that rapidly infect new hosts in recirculating systems [32].
Applying biocontrol agents in soilless systems offers an advantage over soil-based cultivation, as hydroponic systems have limited space and volume, making the introduction of BCA into the rhizosphere easier. Conversely, in soil-based systems, it is challenging to apply beneficial microorganisms in sufficient concentrations to the lower parts of the root system [33]. Among the genera of microorganisms tested in hydroponic settings as biocontrol agents, Pseudomonas, Fusarium, and Trichoderma have been extensively studied and have demonstrated high efficacy in reducing the severity of the disease index (SDI) and inducing defense mechanisms in plants. Beneficial microorganisms such as Pseudomonas and Trichoderma, in combination with Fusarium solani, have shown effective colonization of the rhizosphere and demonstrated mycoparasitism, antibiosis production, nutrient competition, and Induced Systemic Resistance (ISR) in plants. When tested in hydroponically grown zucchini, these species increased resistance to the phytopathogen Phytophthora capsici, resulting in better yields and reducing losses caused by crown rot. Hence, they exhibit great potential as biocontrol agents in hydroponic systems [13].
Trichoderma polysporum and T. harzianum exhibited strong antagonistic traits when applied in combination with the bacterium Streptomyces griseoviridis against Phytophthora cryptogea [34]. Inoculated in consortium with Gliocladium catenulatum and Pseudomonas chlororaphis, they outcompeted Fusarium oxysporum for niche and nutrients and successfully reduced its spore germination [35]. Mycoparasitism has also been determined to be an effective mechanism for inhibiting the pathogenic mycelial growth of Cercospora hypha, which causes foliar disease. All strains of T. asperellum tested in lettuce showed mycoparasitic ability by colonizing C. hypha, drilling holes in its mycelia, and reproducing conidia [36]. Additionally, in cucumbers attacked by Fusarium, the avirulent strain of the same genus (F. oxysporum CS-20) was determined to generate strong antagonistic activity, produce enzymes such as chitinase, and induce ISR, resulting in reduced DSI (from 61.67 to 41.67%) [37]. Direct antagonism was also observed between the beneficial F. oxysporum and Curvularia lunata, and Rhizoctonia solani present in lettuce crops, which was achieved by secreting spreading non-volatile inhibitory substances, promoting plant growth and accomplishing biocontrol goals [38]. In soilless systems, the inactivation of pathogens such as F. oxysporum is often treated with slow sand filtration, which does not eliminate them. Other physical methods, such as heat treatment or UV radiation, can also be used, but they affect the whole system, including the beneficial microbial community [39]. In hydroponic systems, treatments for Fusarium have shown low success rates, making biocontrol an attractive solution. Diverse species of Trichoderma, Penicillium, and Phoma have effectively reduced disease severity (from 59.3 to 3.7) and inhibited spore germination through direct [40].
Pythium spp. is a common phytopathogen found in soilless systems and has been detected on roots in both the NFT system and NS, along with a significant number of aerobic bacteria [41]. Managing diseases caused by Pythium can be complex and costly, requiring chemical control. However, studies have shown that Pseudomonas fluorescens can alleviate tomato crop stress caused by Pythium, reducing the disease severity index from 3.9 to 1.2 [38]. Lee et al. [24] investigated the antagonistic interaction between Pythium as a pathogen and Pseudomonas chlororaphis as a biocontrol agent, demonstrating that Pseudomonas upregulates proteins involved in the jasmonic acid biosynthesis pathway and induces ISR. Pseudomonas protegens and P. brassicacearum were determined to be effective against hairy root disease caused by Agrobacterium rhizogenes in tomato crops by producing antibiotics such as phenazines, pyrrolnitrin, and pyoluteorin [42]. Despite being less common in soilless systems than fungal infections, the efficacy of Pseudomonas against bacterial infections has been confirmed [43].

5. Substrate-PGPM Specificity

The ability of PGPM to colonize the rhizosphere is determined by factors such as the moisture-holding capacity, temperature, and electrical EC of the growing medium [44]. While most studies do not establish a clear correlation between the substrate and specific PGPM species, some assumptions can be made based on experiment results. Akkopru et al. [45] determined that the concentration of endophytes such as Ochrobactrum and Pantoea agglomerans decreased in plant organs and peat as a growing medium. In contrast, pumice was discovered to have better disease control potential and supported better colonization and antifungal activity of BCA such as Trichoderma polysporum, T. harzianum, and Streptomyces griseoviridis, particularly at the early stage of cultivation [35].

This entry is adapted from the peer-reviewed paper 10.3390/su15075959

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