Plant–Soil Microbial Interaction: Differential Adaptations of Beneficial vs. Pathogenic Bacterial and Fungal Communities to Climate-Induced Drought

Abstract

Climate change and the increasing frequency and severity of drought events pose significant challenges for sustainable agriculture worldwide. Soil microorganisms, both beneficial and pathogenic, play a crucial role in mediating plant–environment interactions and shaping the overall functioning of agroecosystems. This review summarizes current knowledge on the adaptive mechanisms used by different groups of plant-beneficial soil microorganisms—rhizobacteria and arbuscular mycorrhizal fungi (AMF)—as well as phytopathogenic bacteria and fungi, in response to drought. The review focuses on identifying the commonalities and differences in the survival strategies of these groups of beneficial and pathogenic soil microorganisms under drought conditions. Additionally, it reviews and compares the plant defence mechanisms under drought conditions facilitated by rhizobacteria and AMF. Special attention is given to the genetic exchange between beneficial and pathogenic soil microorganisms through horizontal gene transfer (HGT), which allows them to exchange traits. It is observed that drought may favor enhanced genetic exchange and the spread of pathogenic traits in the soil microbiome. This review will be useful for a wide range of readers to better understand the dynamics of the soil microbiome under climate change and to apply this knowledge to sustainable agricultural practices.

1. Introduction

Drought is a common natural phenomenon that occurs periodically in almost all climatic zones [1]. According to various estimates, drought regions cover from 26.3 to 36.3% of the land area and occur on all seven continents [2,3]. It is believed that the absence of precipitation for several weeks results in a so-called meteorological drought, while a longer period results in an agricultural drought associated with crop losses [1]. The projected climate change in the direction of increasing the average daily temperature on the planet by several degrees will inevitably lead to an increase in the area of drylands and will have an even more negative impact on agriculture [4].

The increasing prevalence of dry spells poses serious problems for all kinds of soil microorganisms: viruses, bacteria, archaea, protists, oomycetes and fungi, both beneficial and pathogenic. On the one hand, drought reduces the ability of beneficial microorganisms to maintain complex natural ecosystems and promote efficient plant growth and development [5]. On the other hand, it affects pathogenic microorganisms by altering their activity and ability to infect plants [6]. Under drought conditions, the outcome of sustainable agronomy will depend on the competitiveness of adaptive survival strategies of all members of the soil community and their complex ecological interactions, both among themselves and with plants [7].

Microorganisms detect the smallest changes in environmental parameters and respond quickly by regulating the expression of their genes [8]. At the same time, each group of microorganisms has developed its adaptive strategies that help them to survive, including in drought conditions [8,9,10,11]. Despite the large amount of information accumulated in this field recently, many mechanisms of defence responses of soil microorganisms, especially pathogens, to drought remain poorly understood [7]. Also, little is known about the complex ecological interactions between all members of soil microbiomes and plants during drought periods. Meanwhile, drought has profound effects on soil microbiome dynamics, causing changes in virulence and pathogenicity of microorganisms through processes such as horizontal gene transfer and genetic exchange [12,13]. A comparative study of the adaptation mechanisms of all groups of soil microorganisms is essential for effective soil health management, counteracting the emergence of new pathogenic strains and successful agronomic practices [12,13].

Our review aims to summarize recent data on the defence strategies under drought conditions of soil bacteria and fungi, both beneficial and pathogenic, and to understand their similarities and differences. The review covers the following topics: (1) the effect of drought on soil microbiome structure; (2) adaptation mechanisms to drought stress of beneficial rhizobacteria and arbuscular mycorrhizal fungi (AMF) and their comparative characterization; (3) plant defence mechanisms carried out by rhizobacteria and AMF under drought conditions and their comparison; (4) adaptation mechanisms to drought stress of phytopathogenic bacteria and fungi and their comparison with adaptation strategies of beneficial soil microorganisms; and (5) an illustration of the role of horizontal gene transfer (HGT) in enabling pathogenic and non-pathogenic microbes to adapt to drought stress. This study also explores how interactions among soil, plants, and microbes influence HGT under drought conditions driven by climate change.

2. Impact of Drought on Microbial Community Structure

As climate changes induced by water scarcity intensify, the complex dynamics of soil microbiomes are undergoing significant shifts. Scientists have long studied the effects of drought on natural ecosystems, and most often on soil microbiota, as it is directly related to crop drought tolerance in particular, and to successful agronomy in general [14]. And currently, with global warming threatening to transform ecosystems, interest in this issue is increasing [15].

Notable progress has been made in the understanding of the influence of dry periods on the number and composition of soil microbial communities and their interactions with plants [15,16]. Increasing aridity has been shown to reduce soil microbial diversity and abundance [17], as well as microbial community structure and function [18]. It has also been noted in many studies that in most cases, it is not the drought period itself, but the constant change in drought-wetting regimes that has a greater impact on the microbial soil community [15,18].

Microbial cells must adapt when soils dry out, by reducing energy consumption, synthesizing osmoprotectants (trehalose, glycine-betaine, amino compounds, etc.), structurally changing the composition of phospholipids and fatty acids of the cell membrane, etc. [19]. In doing so, those species, and even strains that can do it better, will dominate the communities subjected to desiccation [20]. Most studies point to the advantages of Gram-positive bacteria (apparently due to a thick layer of cell wall peptidoglycan) and their increase during drought periods in both the soil and plant rhizosphere [21]. For example, Polish scientists showed that drought and rewetting stress changed the structure of the soil bacterial community in favor of Gram-positive bacteria of taxonomic categories Actinobacteria and Firmicutes, while the relative abundance of Gram-negative bacteria in most cases decreased, especially affecting representatives of Gammaproteobacteria and Bacteroidetes [22]. A study of Australian soil communities showed that during prolonged drought, an increase in the relative abundance of microorganisms belonging to oligotrophic taxa such as Actinobacteria (the oligotrophic species of this taxon), Alphaproteobacteria, Planctomycetes, Ascomycota and Basidiomycota occurred [23], whereas in wet periods, very different taxa such as Acidobacteria, TM7, Gemmatimonadates and Chytridiomycota dominated [23]. During dry periods, soils of Austrian mountain meadows were also dominated by specialized members of Actinobacteriota, especially of the genus Streptomyces [24]. At the same time, >90% of bacterial and archaeal taxa stopped dividing altogether or divided at significantly reduced growth rates [24]. Water limitation during drought and the associated increase in soil C/N ratio in Swiss forest soils promoted the spread of desiccation-tolerant oligotrophic taxa and caused a shift in the potential lifestyle of microorganisms from symbiotic to saprotrophic [25]. Sometimes, scientists observed unusual facts; for example, in the soils of the hyper-arid Atacama Desert on the west coast of South America (territory of Chile), one of the most life-hostile habitats on the planet, evidence of a metabolically active community of archaea was found during periods of wetting [26]. In a study by Chilakala et al., a drought-induced increase in phototroph populations in both the soil and root microbiome was observed [27]. This indicates the complex ways in which drought affects microbial composition and dynamics in the plant–soil system [28].

Metagenomic studies by Chilakala et al. showed that in the chickpea rhizosphere zone, drought enhances the fungal microbiota by suppressing virus and algal populations [27]. In addition, prokaryotic communities were found to be less resistant to water limitation than fungal communities in most other studies [25]. Compared to bacteria, fungi have unique survival skills and physiological structures that enhance their drought tolerance [29]. However, in some cases, the opposite situation was also observed, apparently related to the predominance of drought-tolerant bacterial species such as Pseudomonas spp. and Bacillus spp. in the soil microbiome. These bacteria appeared to adapt to dehydration through their ability to form biofilms, produce stress-sensitive proteins, and utilize diverse nutrient sources, even under challenging conditions [30].

The adaptive response of the soil microbiome to drought is affected not only by the lack of moisture but also by other parameters: soil composition (nitrogen and carbon content and ratio), pH, presence of heavy metals, etc. [30,31]. Dehydration stress has been shown to affect microorganisms more strongly in soils with low organic matter content [32]. Ambient air temperature and atmospheric CO₂ content are also relevant [33]. For example, Metze et al. experimentally modelled what would happen to the soil microbial community under drought conditions during a six-year climate warming period involving a 3 °C increase in temperature and a 300 ppm increase in atmospheric CO₂ concentration [24]. It was demonstrated that in this scenario, there would be a 2.3-fold increase in the number of taxa undergoing active division (from 4% to 9%, compared to 35% under normal conditions), indicating the adaptation of numerous species to adverse conditions.

In some studies, it has been shown that plants and multicellular fungi can regulate the composition of the bacterial community of the rhizosphere by root exudation of various substances into the soil during drought [34,35]. For example, it was shown that the cactus Echinocactus platyacanthus in Mexico during drought periods changes the profile of amino acids secreted by its roots, which in turn restructures the microbial community in its rhizosphere in favor of bacteria belonging to the type Armatimonadota, classes Actinobacteria and Dehalococcoidia, families Gemmataceae and Nitrosococcaceae [36]. The fungi Rhizophagus and Serendipita have a protective effect on the bacterial communities of their hyphosphere, which are subject to water limitation [37].

Thus, drought stands out as one of the most perilous abiotic stresses affecting soil microorganisms, diminishing their activity and population while disrupting community composition. The species most adapted to prolonged absence of water survive. The composition of the community changes towards an increase in the proportion of fungal microbiota, Gram-positive bacteria and oligotrophic taxa. With the anticipation of more frequent droughts due to climate warming, research on innovative strategies to enhance the drought tolerance of microorganisms is of paramount importance. Mechanisms enabling microbes to endure and proliferate amidst diminishing moisture levels could introduce new functional groups into the ecosystem, offering substantial advantages to agriculture [35].

3. Adaptive Strategies Used by Beneficial Bacteria and Fungi under Drought

3.1. Effect of Drought on Rhizobacteria

The most beneficial soil bacteria are concentrated in the rhizosphere zone around plant roots. There are more than 30,000 species of rhizobacteria [38], which in the late 1970s came to be called “plant growth-promoting rhizobacteria” (PGPR) [39]. This group of bacteria includes several genera such as Pseudomonas, Enterobacter, Bacillus, Variovax, Klebsiella, Paraburkholderia, Azospirillum, Herbaspirillum, Gluconacetobacter, Serratia, Azotobacter, and others. They are widely distributed in soils worldwide, phylogenetically diverse, and often not species specific to the host plant [40,41]. This group of bacteria is very important from the point of view of efficient agronomy (restricted agriculture without the use of chemicals) because it participates in most biophysical and biochemical soil processes and promotes plant growth [40,42,43,44,45].

Rhizobacteria tolerate full or partial drought stress in different ways [46]. In experiments where aliquots of PGPR bacterial suspensions were subjected to drying under different conditions to a certain humidity or complete drying and then re-watered, the titer of surviving cells varied greatly [47]. For example, after complete drying and then re-watering, 3.2% cells of Acinetobacter calcoaceticus strain PADD68, 1.5% Arthrobacter phenanthrenivorans DSM 18606T and 31.5% Arthrobacter siccitolerans 4J27T [48] remained viable. Two strains of Bradyrhizobium japonicum, TXVA and TXEA, isolated from soybean root nodules in Texas, showed 87.1% and 93.9% survival rates, respectively, under 27% relative humidity conditions, while their counterpart, the wild-type strain B. japonicum USDA110, was also very resistant to desiccation, with 80.00% of cells surviving the experiments [49]. Some PGPRs are particularly sensitive to desiccation. For example, the titer of viable Pseudomonas putida KT2440T cells was not detected at all, after undergoing desiccation stress [46,47], although there is a suggestion that this may be due not to the death of all cells, but to their transition to a non-culturable state, which is one of the defence mechanisms against this type of stress [50]. For example, an experiment with PGPR Bradyrhizobium japonicum 5038 used fluorescent staining of stressed cells with live/dead cry-site and showed that several viable but unculturable cells were present in the culture medium after drying and rehydration [51]. The authors [52] analyzed 28 strains of rhizosphere bacteria able to withstand 18 days of air-drying stress (at 30 °C and 50% relative humidity) and proposed to divide all rhizobacteria into five categories: highly tolerant, tolerant, medium tolerant, low tolerant and very low tolerant. In doing so, they showed that under drought conditions, only the highly tolerant strains could adhere to maize seeds, colonize its rhizosphere and stimulate plant growth. However, bacterial strains with low tolerance levels, unlike highly tolerant strains, were unable to do so [52]. A lot of work has to be carried out to isolate drought-resistant strains with beneficial properties. For example, Indian researchers analyzed 164 isolates of rhizobacteria, out of which only five of them belonging to Enterobacter cloacae, Bacillus cereus and Bacillus megaterium showed resistance to desiccation and yet were able to stimulate the growth performance of wheat during drought [53].

Thus, rhizobacteria have different tolerances to drought conditions, from very high to extremely low. There are species of rhizobacteria, e.g., Bradyrhizobium japonicum, which are more drought-tolerant. At the same time, isolates with different sensitivity to desiccation can be identified within the same species. Scientists aim to identify rhizobacterial isolates that are not only drought-tolerant but can also stimulate plant growth under such unfavourable conditions.

3.2. Adaptive Mechanisms of Rhizobacteria under Drought

The response of rhizobacteria to desiccation stress started to be studied about 100 years ago, which was due to their use as seed inoculants in agriculture [54]. It has now been shown that the adaptive strategies of rhizobacteria in response to climatic stressors include cellular, genetic, and enzymatic changes (Figure 1). Under drought conditions, changes in the cellular structure and metabolic activity of rhizobacteria are observed, affecting their survival and function under water-limited conditions [55,56]. Moreover, the main mechanism that allows rhizobacteria to survive under stress conditions is the alteration of gene expression toward the synthesis of protective substances such as trehalose, proline, glycine–betaine, glutamate, mannitol, hydroxylation, exopolysaccharides (EPSs), heat shock proteins, and proteins involved in cell membrane protection, DNA damage repair, and response to oxidative stress [57]. A metagenomic study by Bulgarelli et al. identified specific genes involved in mechanisms of responses to various abiotic stresses [58].

Cytryn et al. showed that desiccation of cells of Bradyrhizobium japonicum, a Gram-negative soil bacterium that converts atmospheric nitrogen to ammonia by forming a symbiotic association through soybean root nodules, results in differential expression of 15 to 20% of 8453 genes within 3 days [59]. The induction of trehalose-6-phosphate synthase (otsA), trehalose-6-phosphate phosphatase (otsB), and trehalose synthase (treS) genes, which encode two of the three trehalose synthesis pathways, is more than 2-fold increased, correlating with an increase in its intracellular concentration. The authors also showed that the expression of genes encoding isocitrate lyase, responses to oxidative stress, EPS synthesis and transport, heat shock proteins, enzymes for nucleic acid modification and repair, and the synthesis of pili and flagella increased under desiccation conditions. These metamorphoses occurring in cells contribute to their survival under conditions of severe dehydration [59]. Zhu et al. also demonstrated that different types of genes are differentially expressed in Bradyrhizobium japonicum cells during drought at 10% relative humidity and subsequent rehydration [51]. Significant activation of genes of trehalose biosynthesis (otsAB, treS and treYZ), ligD, oprB and sigma factor rpoH, as well as genes involved in signal transduction and transport of inorganic ions, was observed [51].

The accumulation of trehalose in cells in response to desiccation stress appears to be a universal mechanism of both rhizobacteria and other soil bacteria [51,60,61]. Trehalose accumulation in the cytoplasm, rather than in the periplasmic space, was found to be more important for cell survival during dehydration. Also, the chances of bacterial survival increase when trehalose is added to the medium [61]. Double mutants of otsA treY, which cannot accumulate trehalose, are more sensitive to the effects of desiccation and are also less competitive for nodule occupancy [62].

Trehalose is a non-reducing disaccharide (α-D-glucopyranosyl-1 and 1-α-D-glucopyranoside) containing two α-glucose molecules. The involvement of trehalose in cellular defence against stress is attributed to its stable structure. i.e., the low energy (1 kcal/mol) of the glycosidic bond connecting the two hexose rings [63], and several unique physical properties: high hydrophilicity and chemical stability, non-hygroscopic glass formation, and lack of internal hydrogen bond formation [64]. There are three mechanisms of biomolecule protection during desiccation involving trehalose that act in parallel: (1) the substitution of water molecules by trehalose molecules in the hydrate layer of biopolymers to stabilize their structure and prevent denaturation; (2) the formation by trehalose of amorphous, non-hygroscopic crystals causing a vitreous effect in the cell, which helps to keep all biopolymers intact for a long time; and (3) the interaction of a very flexible glycosidic bond between two D-glucose residues of trehalose with the polar groups of various biomacromolecules, ensuring their chemical stability [63,64].

Thus, the described adaptive mechanisms associated with changes in cellular structure and metabolic activity and synthesis of defence substances help rhizobacteria survive under reduced soil moisture both in free-living conditions and in symbiosis with plants [65].

3.3. Effect of Drought on Arbuscular Mycorrhizal Fungi

An important part of the beneficial soil microbiota is made up of arbuscular mycorrhizal fungi (AMF), which are obligate symbionts of 70–90% of plant species [66,67]. There are about 250 species of them [68]. They inhabit both root tissues as endophytes and the surface (rhizoplane) [69], increasing plant resistance to biotic (pathogens) and abiotic (drought) stresses [42,43]. Many AMF species are believed to be widespread, as they are quite resistant to any abiotic influences and can tolerate drought stress well [70]. However, water deficit affects the growth and development of AMF, which is manifested by a decrease in the growth of extra-radical hyphae, and a decrease in the ability to colonize plant roots and to carry out the process of sporulation [71]. All this leads to a decrease in the ability of AMF to form symbiotic associations with plant roots, which disturbs the balance of the soil microbiome [72]. Some studies have reported that mycorrhizal fungi respond to abiotic stress by reducing abundance and species biodiversity [73]. For example, a community of four AMF species (Diversispora aurantia, Diversispora omaniana, Septoglomus africanum and an undescribed Paraglomus species) isolated in the Arabian Desert from Bicolour Sorghum microsomes showed that under water deficit there was a decrease in total cell number and a decrease in the amount of extra-radical mycelium, leading to a partial reduction in the biomass of the host plant [74]. In a study of a semi-arid soil ecosystem in the Bou-Hedma National Park in Tunisia, it was shown that the AMF content in arid soil plots is lower than in soils in plots with normal moisture content, and in the former case, representatives of the Glomeraceae family are most common [75].

Within this family, different genera and species respond to water stresses in unique ways, affecting plant health and ecosystem function. For example, Augé et al. (2015) identified significant changes in taxonomic diversity and community structure of the genus Glomus spp. in response to drought, emphasizing the sensitivity of symbiotic associations of these AMFs to environmental stress [76]. Similar studies of AMF communities in Mediterranean ecosystems by Veresoglou et al. showed changes in the taxonomic composition of Funneliformis spp. and other AMF genera in response to water stress [77]. Somewhat adaptive responses to drought stress have been shown for the genera Diversispora [78], Rhizophagus, Archaeospora and Paraglomus [79]. In Lozano et al., the effect of drought stress on fungi belonging to the Basidiomycota and Ascomycota was noted. The relative abundance of Basidiomycota representatives decreased and Ascomycota representatives increased, presumably due to the formation of ascospores adapted to the drought environment [80].

Thus, AMF populations respond to drought conditions by experiencing decreased growth of extra-radical hyphae, reduced ability to colonize plant roots and sporulation, and reduced abundance and species biodiversity. As with rhizobacteria, more resistant species (e.g., those belonging to Basidiomycota) and less resistant species (e.g., those belonging to Ascomycota) can be distinguished among AMF. However, even within the same genus, both drought-tolerant and drought-sensitive AMF species can occur. Studies on the direct effects of abiotic drought stress on AMF are constantly ongoing [67,81]. So far, only the most general tenets of the effects of drought stress on AMF can be formulated, but extreme water regimes can significantly alter the local AMF community structure, which in turn affects all symbiotic relationships between plants and the soil microbiome [74,82].

3.4. Adaptive Mechanisms of AMF under Drought

Adaptive responses of AMF to dehydration and drought stress occur at cellular, genetic, and enzymatic levels (Figure 1). AMF can develop adaptive mechanisms and adapt to drought conditions primarily by producing more spores [73,81]. In this way, they solve the problem of immobility on the host plant roots and ensure almost 100% survival [83]. Cellular adaptations in response to drought also include changes in hyphal morphology and in the expression of aquaporins to regulate water uptake [84,85]. At the genetic level (based on transcriptome analyses), drought exposure causes significant shifts in stress gene expression [86]. During dry periods, there are strategic changes in the activity of key enzymes: phosphatases (involved in enhanced mobilization of phosphate) and nitrogenases (contributing to improved nitrogen assimilation) [87]. Also, AMF cells show increased activity of antioxidant enzymes such as superoxide dismutase and peroxidase, which play a vital role in mitigating oxidative stress [88]. This generalized response of AMF at cellular, genetic and enzymatic levels highlights their adaptability to adverse environmental conditions.

3.5. Comparison of Drought Adaptation Strategies of Rhizobacteria and AMF

Rhizobia bacteria and AMF exhibit active resistance to drought through evolutionary adaptive mechanisms involving cellular, genetic, and enzymatic alterations (Figure 1). These strategies in rhizobacteria and AMF share several similarities. For instance, when moisture levels in the environment decrease, both bacterial and fungal cells transform cellular structure and metabolic activity primarily through changes in gene expression, while effectively regulating the osmotic state of cells. Rhizobacterial cells actively produce desiccation-resistant compounds, primarily osmolytes, while fungal cells exhibit strategic changes in the activity of key enzymes such as phosphatases, nitrogenases, superoxide dismutase, and peroxidases, along with active secretion of enzymes into the external environment. The formation of stable cellular structures is another common mechanism observed in both bacteria and fungi. Under severe drought conditions, bacteria can slow down cell metabolism and enter a dormant state, forming dormant cellular forms, whereas fungi, along with spores, produce drought-resistant cells with thicker cell walls, such as sclerotia.

A third important mechanism observed during drought, shared by rhizobacteria and AMF, involves increased interactions with plant roots to establish symbiotic relationships. Bacteria utilize biofilm-forming mechanisms, aiding their survival outside of symbiotic relationships, while fungi incorporate processes of considerable hyphae outgrowth to better colonize roots. Thus, both rhizobacteria and AMF, through active adaptation to drought, not only protect themselves but also assist plants in survival, especially when acting in concert.

Figure 1. The adaptive strategies of soil- and root-associated bacteria vs. fungi during environmental stress (e.g., drought). The parts of the images used in this figure are modified from [89,90]. Website accessed on 5 March 2024 in www.wikipedia.org, www.shutterstock.com, www.en.wikipedia.org/wiki/Biofilm, www.shutterstock.com/search/soybean-root and www.voanews.com/a/drought-tightens-its-grip-on-morocco/6700790.

Figure 1. The adaptive strategies of soil- and root-associated bacteria vs. fungi during environmental stress (e.g., drought). The parts of the images used in this figure are modified from [89,90]. Website accessed on 5 March 2024 in www.wikipedia.org, www.shutterstock.com, www.en.wikipedia.org/wiki/Biofilm, www.shutterstock.com/search/soybean-root and www.voanews.com/a/drought-tightens-its-grip-on-morocco/6700790.

4. Defence Mechanisms of Rhizobacteria and AMF in Plants during Drought Conditions

4.1. Rhizobacteria-Mediated Plant Defence Mechanisms under Drought Conditions

In soil, the relationship between rhizobia and plants is crucial for the maintenance of plant productivity. Therefore, the main objective of effective agronomy—to increase plant resistance to various types of stresses, including drought—has been successfully addressed by the application of rhizobacteria [91]. Recently, researchers have focused their attention on the unique abilities of rhizobacteria [92] or their compositions with AMF [93,94] to help plants overcome various abiotic and biotic stresses.

PGPR induces immunity to abiotic stresses in plants, which is called induced systemic tolerance (IST) [95]. In addition, through physicochemical modifications, rhizobacteria induce increased plant resistance to drought, which is termed rhizobacterial-induced drought tolerance and resistance (RIDER) [93,96]. Numerous studies have demonstrated how PGPRs help crops combat drought and other types of abiotic stress by positively affecting growth, yield, and nutrient uptake [92,97,98]. Rubin et al. (2017) conducted a meta-analysis of 52 publications on the effects of rhizobacteria (mainly Pseudomonas, Azospirillum, Azotobacter and Bacillus) on plant growth (mainly maize, wheat, sunflower and lettuce) [99]. The authors systematized the data and summarized the fact that under standard moisture conditions, rhizobacteria contributed 35%, 28% and 19% to the increase in root weight, shoot weight and seed yield, respectively, whereas under drought conditions, rhizobacteria contributed 43%, 45% and 40%, respectively [99]. Recently, research in this area has continued with even greater intensity. To effectively help crops cope with drought, researchers propose the use of increasingly effective PGPR strains [100] or combinations of bacterial cultures [98,101], as well as mixed combinations of rhizobacteria with mycorrhizal fungi [101,102]. Attention is also paid to selecting the stage of plant development at which the application of rhizobacteria will be most effective [103]. The most interesting works are those in which researchers propose to apply a combination of rhizobacteria and various additives: fertilizers, metabolites, hormones, nanoparticles, etc., to help plants during drought. For example, Khan showed that the combined application of rhizobial cultures Planomicrobium chinense and Bacillus cereus and the plant growth hormone, salicylic acid, effectively mitigates the adverse effects of water stress on wheat by increasing protein, sugar and chlorophyll content in leaves [104]. The same positive synergism increasing yield and physiological parameters of wheat under drought conditions was observed with rhizobacteria and cytokinins applied at different stages of plant development (tillering, flowering, and grain filling) [105]. Muhammad et al. showed that the combined application of rhizobacteria Azospirillum brasilense and ZnO nanoparticles (NPs) has a synergistic effect on wheat, providing growth stimulation, reducing drought stress and increasing yield [106].

There is no single mechanism by which rhizobacteria protect plants from desiccation stress. Typically, PGPBs use a wide range of adaptive measures that may vary depending on the species and strain of rhizobacteria [107]. According to the type of effects on plants, they can be divided into direct and indirect, and, according to the organizational level at which changes occur, into physical, molecular and biochemical [108]. Thus, direct mechanisms (and at the same time biochemical) include how PGPR directly affects plants during drought: enhancing nitrogen fixation; inducing the production of abscisic acid, which leads to the partial closure of the stomata and reduces water evaporation through transpiration; influencing the levels of phytohormones (auxins, gibberellins and cytokinins); influencing the production of antioxidants to reduce reactive oxygen species (ROS) [109]; effecting the increase in the production of osmolytes, carbohydrates, amino acids, polyamines and volatile organic compounds [110]; the production of ACC deaminase, which reduces the concentration of ethylene (a plant hormone responsible for slowing down root and shoot growth under drought conditions) in plants by cleaving its precursor, which supports normal plant growth [111]; and others. The study of these mechanisms has been systematized in detail in numerous reviews published in recent years [93,112].

Indirect mechanisms may include PGPR-mediated actions that also contribute to plant survival during drought; for example, increasing the availability of soil nutrients and minerals by solubilizing phosphate or producing siderophores that help iron uptake [113]. Also, indirect methods include preventing the harmful effects of phytopathogens by producing PGPR antibiotics, antagonistic substances (phenazine, diacetylphloroglucinol, hydrogen cyanide, 2-3-butanediol, acetoin), siderophores, and lytic enzymes (chitinase and glucanase, which destroy the cell wall of fungal pathogens) [114,115]. Molecular mechanisms are related to the effect of rhizobacteria on plant gene expression [116]. For example, it was shown that PGPR inoculation caused up-regulation of drought stress-related genes (early dehydration response genes, heat shock proteins, various enzymes, etc.) in wheat, pepper, mungbean and Arabidopsis [117]. Physical mechanisms include the ability of PGPR to produce EPS in the soil, which fulfills several functions [112]. On the one hand, oligo- and polysaccharides are absorbed by the surface of soil particles, and through cationic, hydrogen and Van der Waals interactions with soil chemical compounds, increase its stability and moisture retention capacity [118]. The water-holding capacity of such exometabolism can reach seventy grams of water per gram of polysaccharide [119]. On the other hand, EPS promotes the formation of hydrophilic biofilms (in the form of capsules) on the surface of plant roots, further protecting them from drying [120,121].

Thus, rhizobacteria can significantly reduce drought stress for plants, and even contribute to the increase of biomass and yield to a greater extent than under normal humid conditions. For this purpose, beneficial rhizobacteria use various mechanisms, including (1) enhancing nitrogen fixation by plants; (2) influencing plant gene expression; (3) inducing the production of protective and signaling compounds in plants (such as abscisic acid, osmoprotectants, antioxidants, amino acids, enzymes, etc.); (4) modulating the levels of phytohormones; (5) increasing the availability of nutrients and minerals from the soil; (6) protecting against phytopathogens; and (7) producing exopolysaccharides (EPSs) in the soil, which increases its water-holding capacity.

4.2. AMF-Mediated Plant Defence Mechanisms under Drought

Arbuscular mycorrhizal fungi (AMF) significantly increase host plant resistance to both abiotic and biotic stresses [122,123,124], primarily because they form symbiotic relationships with most terrestrial plants. This symbiosis enhances the plant’s ability to absorb nutrients and water, thereby improving overall plant health and stress tolerance [125]. They manage to increase the drought tolerance of plants due to the developed network of their mycelium, and the production of glomalin [126], as well as several other mechanisms acting at three levels: physiological, morphological and molecular [127]. Studies investigating the phenomenon and mechanisms of AMF-mediated enhancement of plant resistance during drought are plentiful, and interest continues to grow [128,129]. Yu Wang [127] analyzed the publication activity over several years on this issue. The authors write that in 2011 there were 27 articles related to this topic, in 2021 there were already 124 articles, and in 2022 there were 131 articles, with the focus increasingly shifting to studying the molecular mechanisms that explain how AMF enhance plant tolerance to drought [127].

AMF alter host plant physiology under drought conditions: they adjust water potential and gas exchange, increase water and nutrient uptake, and improve stomatal regulation [71,130,131]. AM extraradical hyphae can create shared mycorrhizal networks between neighbouring plants, helping to transmit signals and exchange nutrients [129]. At the biochemical level, AMF modulate levels of hormones (such as strigolactones, jasmonic acid, abscisic acid, etc.), activate antioxidant defence systems, and help plant cells maintain osmotic pressure [125,126,127,128,129,130,131,132]. For example, Zou [133] analyzed changes in root metabolites of walnut (Juglans regia) after inoculation with the arbuscular mycorrhizal fungus Diversispora spurca under drought conditions using ultra-high-performance liquid chromatography. It was found that inoculation of plants with AMF under drought stress increased the activity of 49 metabolites (including 2,3,5-trihydroxy-5-7-dimethoxyflavanone) and decreased the activity of 116 metabolites [133]. In a study by Sheteiwy [134], it was shown that inoculation of soybean (Giza 111) with AMF, together with rhizobacteria, under stress conditions increased the content of primary metabolites and mitigated the drought-induced decrease in soluble sugars, lipids, protein, and oil, and resulted in decreased levels of stress hormones (abscisic acid) and increased gibberellin, trans-zeatin-riboside and indoleacetic acid in seeds of inoculated plants [134]. In another work on soybean, it was shown that inoculation of plants with mycorrhizae–rhizobia consortium during drought increased the relative water content of leaves and the amount of osmoprotectant proline in beans, as well as pod number, pod fresh weight and seed dry weight [93].

All these changes are based on molecular mechanisms associated with changes in gene expression and regulation of transcription factors [127]. For example, in [134] it was shown that AMF inoculation of plants induced the expression of genes involved in lipid and protein biosynthesis and blocked the expression of genes involved in their degradation. Studies of mycorrhizal fungi and soybean interactions have demonstrated that under soil drought conditions, AMF can trigger the expression of catalase and peroxidase genes in plants [135]. AMF have also been shown to significantly up-regulate the expression of key genes of the ABA signaling pathway TFT2 and TFT3 in tomatoes under drought conditions [136]. Recently, mycorrhizal fungi were found to modulate plant drought tolerance through the regulation of transcription factors (GRAS, MYB, and AP2/ERF) [127].

Thus, AMF are indispensable helpers for plants under drought conditions. The mechanisms by which they reduce plant drought stress are even more diverse and extensive than those of rhizobacteria. Like rhizobacteria, AMF also influence plant gene expression, and do so through the regulation of transcription factors. AMF can alter the host plant physiology, regulate its water potential and gas exchange, increase water and nutrient uptake, improve stomatal regulation, modulate hormonal levels, and influence the activity of at least 165 metabolites. In addition, they can do what rhizobacteria cannot, namely, using extra-radical hyphae to create common mycorrhizal networks between plants for various kinds of exchange. Thus, the study of the molecular mechanisms of AMF assistance to plants during drought continues. The data obtained will contribute to the prospective development of efficient agronomy.

5. Adaptive Strategies during Drought of Pathogenic Bacteria and Fungi and Their Comparison with Adaptive Strategies of Beneficial Microorganisms

5.1. Adaptation of Phytopathogenic Fungi and Bacteria to Drought

Seventy to eighty percent of plant diseases resulting in enormous losses in agriculture are caused by pathogenic fungi belonging to the genera Alternaria, Aspergillus, Botrytis, Cladosporium, Verticillium, Pythium, Fusarium, and Rhizoctonia [137]. Several hundred species of bacteria belonging to the Proteobacteria, Mollicutes, and Actinomycetes are also plant pathogens. Entering the plant through natural openings such as stomata and lenticels, or wounds, the bacteria cause necrosis, maceration of tissues, wilting, and hyperplasia [138].

During drought, the spread of pathogens increases, and the likelihood of plant infection and disease severity increases. Modelling coupled with experimental data has shown that the prevalence of major soil fungal pathogens belonging to the genera Alternaria, Fusarium, Venturia, and Phoma is likely to increase under projected global warming [139]. However, phytopathogenic bacteria and fungi, as well as beneficial ones, tolerate drought in different ways. For some, drought is an additional factor that promotes their activity, while for others, reduced moisture becomes a hardship, and they reduce their pathogenic claims on plants [140]. For example, chickpea production worldwide is significantly constrained by a disease called dry root rot (DRR) caused by the phytopathogenic fungus Macrophomina phaseolina. Studies conducted by multiple groups of scientists have shown that drought and high temperatures exacerbate the impact of pathogens on various crop plants, including chickpeas [141,142]. These pathogens encompass pea root rot (Aphanomyces euteiches), white rot of onion (Sclerotium cepivorum), wheat spot (Gaeumannomyces graminis var. tritici), wheat crown rot (Fusarium spp.), black foot of Brassica (Leptosphaeria maculans), and black foot of grape (Ilyonectria/Dactylonectria spp.) [140]. Botryosphaeria doithidea becomes more active during dry periods, colonizing the above-ground parts of host plants through wounds and causing lesions on a wide variety of tree and shrub species [6]. Climate change is projected to contribute to more frequent and intense outbreaks of diseases caused by Botryosphaeria dothidea, as well as Neofusicoccum parvum, due to their expanding range [143].

On the other hand, soil pathogens belonging to the taxa Oomycota, Phytophthora, and Pythium species are more sensitive to drought, and their distribution will decrease during dry periods [144]. For example, Phytophthora, which destroys the fine root system of plants, has been shown to increase its pathogenic activity in wet conditions and decrease it in dry soils. Drought has also been found to alleviate the severity of sclerotinia rot in kiwifruit (S. sclerotiorum) and red-needle leaf blight in radiata pine (Phytophthora pluvialis) [140]. In dry periods, the activity of the bacterial pathogen Xylella fastidiosa, which affects grapevines, also decreases. During drought, necrotrophic (feeding on the contents of dead plant cells that they killed) pathogens will be more active, depleting plant resources through regeneration and compartmentalization processes. In contrast, diseases caused by biotrophic (feeding on the contents of living plant cells) pathogens will be less severe, due to the close correlation between pathogen effectiveness and plant nutritional status, but only until the plant is on the verge of destruction [145].

During drought, phytopathogenic microorganisms may be affected by processes that completely reduce their virulence properties. It has been shown that in response to an increase in ambient temperature, some phytopathogens undergo genetic changes leading to a decrease in heat tolerance, virulence, and ability to survive in soil [146]. For example, in a study by Cubeta et al. [147], it was shown that while coping with desiccation stress, the pathogen Rhizoctonia spp. alters cellular and enzymatic functions at the genetic level, reducing cellular virulence and pathogenicity. That is, under drought conditions, Rhizoctonia spp. ceases to be a pathogen [147].

Thus, drought has different effects on phytopathogens. Most of them increase their activity during droughts and intensify their infectivity against plants. Such phytopathogens include pathogens of pea root rot, white rot of onion, wheat blotch, fungi of the genus Penicillium, and many others. There are also those whose activity will decrease, such as the Phytophthora pathogen. In general, there is an opinion that during drought, necrotrophic pathogens will become more active and biotrophic pathogens will become less active. Drought can also completely change the virulent properties of some phytopathogenic fungi and deprive them of pathogenicity.

5.2. Similarities and Differences in Adaptive Strategies of Pathogenic and Beneficial Microbes to Drought Conditions

Pathogens, as well as beneficial microorganisms, defend themselves against drought stress, with most of their adaptive mechanisms overlapping (Figure 2). One of the main defence mechanisms of pathogenic fungi and bacteria during drought and other unfavorable conditions, as well as AMF and some spore-forming species of rhizobacteria, is the formation of large amounts of stable structures, in the form of which they can persist in the soil for a very long time. For example, the main crop pathogens of fungi (belonging to the genera Fusarium or Verticillium) and oomycetes form stable structures: microsclerotia, sclerotia, chlamydospores, oospores, etc., to survive in arid conditions [6].

Some genomic adaptation mechanisms to drought in pathogenic and non-pathogenic microorganisms, although having a common basis, differ in the direction of action (Figure 2). Such mechanisms include changes in gene expression and the production of antioxidant enzymes. Both pathogenic and non-pathogenic microorganisms in response to drought regulate their gene expression toward the production of essential metabolites involved in defence mechanisms. However, non-pathogenic soil microbes, especially plant-growth promoting species, express genes associated with stimulating plant growth under stress conditions; for example, Azospirillum brasilense produces large amounts of phytohormones [148], whereas pathogens during drought stimulate the expression of pathogenicity, virulence and host-colonization factors (including adhesins, polysaccharides and degradative enzymes), as in Fusarium oxysporum [149] or Botrytis cinerea [150]. One of the key pathogenicity factors is the type III secretion system, which introduces effector proteins into the host cell cytosol to manipulate plant cellular processes, such as basal defence, to the benefit of the pathogen [151]. In addition, both microbial groups can produce antioxidant enzymes, but their main focus is different: non-pathogens use them to increase their stress tolerance, such as Trichoderma harzianum [152], while pathogens use them to manipulate host invasion, such as the pathogen Botrytis cinerea [150].

Like beneficial microorganisms, pathogens produce osmoprotectants such as proline, glycine-betaine, and other amino acids in their cells when water is scarce during drought, as the oomycete Phytophthora infestans does, for example [153]. In a study by El-Abyad et al., it was shown that the sugar beet-root rot pathogens Fusarium solani and Sclerotium rolfsii under stress conditions produce alanine, proline and histidine, which play an important role in the osmoregulation of their cells [154]. In response to the changing osmotic conditions that accompany drought, pathogens not only produce osmoprotectants but also trigger other osmosensing mechanisms that help them survive. A study by Rossier and Vorhölter [155] showed how this occurs in the pathogenic bacterium Xanthomonas campestris, which causes a multitude of diseases in monocotyledonous and dicotyledonous crops worldwide [155]. The same signal-transduction cascades under osmotic stress conditions are also triggered in beneficial soil microbes such as Bacillus subtilis [156].

Drought favours biofilm formation in both beneficial and pathogenic microbes. However, rhizobacteria and AMF form biofilms around plant roots to reorganize the soil structure and protect themselves and the host plant. Pathogens, on the other hand, use this strategy to invade and infect the plant.

Thus, the main mechanisms of survival under drought conditions for phytopathogens and beneficial microorganisms coincide with the formation of a large number of stable structures (sclerotia, chlamydospores, etc.), changes in gene expression, production of protective and signalling substances, and increased biofilm formation. However, the direction of most mechanisms has a negative tendency, which is directed against plants. In addition, drought stimulates pathogens to produce phytotoxins and secretory effectors, which also contribute to plant infection and damage.

6. Genetic Exchange through Horizontal Gene Transfer (HGT) within Soil–Plant Microbial Ecosystem during Drought

6.1. HGT between Non-Pathogenic and Pathogenic Microorganisms during Drought

Horizontal gene transfer (HGT) is a mechanism by which DNA is transferred between unrelated organisms in a non-Mendelian manner [157,158,159]. Interspecies gene transfer was first studied by transferring virulence genes from pathogenic to non-pathogenic bacteria, which contributed to the rapid spread of bacterial antibiotic resistance in hospitals [160]. HGT allows microorganisms to acquire beneficial traits such as stress resistance and antibiotic resistance on the one hand, and negative traits such as virulence factors on the other hand [161]. Horizontally transferred virulence genes often include genes involved in bacterial adhesion, secretion systems, toxin production and iron assimilation [162]. When such genes are acquired as a result of HGT, pathogens gain additional advantages, as in the case of Bacillus anthracis and Fusarium oxysporum, which cause serious diseases of the plant root system [162]. Pathogens that acquire additional properties as a result of HGT may expand their habitat, which is an undesirable event for agriculture [13].

Drought and water deficit exert selective pressure on soil microbial communities, favouring genetic exchange as a survival strategy [163,164]. Both non-pathogens and pathogens undergo HGT to adapt to changing environmental conditions [165]. For example, it has been shown that non-pathogenic bacteria such as Pseudomonas putida can acquire stress-tolerance genes in response to drought [166], while pathogens such as Xylella fastidiosa can exchange genes related to virulence and host specificity [167].

A change in resource allocation under drought conditions may increase the likelihood of HGT between soil pathogenic and non-pathogenic microbes (Figure 3). This is because microbes under stress, instead of focusing on their normal cellular processes, are more likely to engage mechanisms such as conjugation, transduction and transformation, which favour HGT.

The success of HGT during drought may depend on a variety of factors. For example, enhanced biofilm formation during drought by all members of the soil microbiome promotes HGT by forming favorable conditions for it. That is, biofilms often serve as foci of genetic exchange, creating an environment for interaction between different microbial species [168]. Other abiotic environmental factors of soil and plant rhizosphere, such as nutrient availability, can also influence HGT. Favourable factors will favour the persistence of transferred genes, whereas critical reductions in soil moisture and nutrient availability may limit HGT and restrain the spread of both beneficial and detrimental traits [169].

Thus, drought has a profound effect on the dynamics of the soil microbiome, causing changes in the virulence and pathogenicity of microorganisms through genetic exchange. HGT allows non-pathogenic microorganisms to acquire beneficial stress-resistant and antibiotic-resistant properties, enhancing their ability to survive and promote plant health under unfavourable conditions [170]. On the other hand, as a result of HGT, there is a threat of wider spread of pathogenic traits, emergence of new pathogenic strains, and increased virulence of already known pathogens [171]. The role of HGT in the processes of mutual transition from non-pathogenicity to pathogenicity requires further study [172]. Drought conditions can both restrain and promote HGT. The complex interplay between environmental stressors, microbial-community dynamics and genetic exchange emphasizes the need for a thorough understanding of these mechanisms to effectively manage soil health and counteract the emergence of new pathogenic strains [12,13].

6.2. Soil, Plant, and Microbial Interaction Factors Affect HGT under Drought

Horizontal gene transfer (HGT) is a pivotal mechanism in the evolution and adaptation of microbial communities within the soil microbiome, especially under environmental stress conditions such as drought. This process allows for the exchange of genetic material between organisms, enabling microbes to acquire traits that enhance their survival in challenging environments. Several key factors influence HGT events, particularly under drought conditions, including soil pH, moisture, texture, organic matter, mineral content, the abundance of pathogenic and non-pathogenic microbial communities, and host susceptibility (Figure 3).

Soil pH is a fundamental determinant of microbial community composition and function. It has a direct impact on microbial diversity and activity, influencing the stability and mobility of genetic elements involved in HGT. Variations in soil pH can alter the competitive dynamics between pathogenic and beneficial microbes, potentially enhancing or inhibiting HGT processes. For example, shifts in pH levels can lead to changes in microbial interactions, thereby affecting the transfer of genes related to virulence and stress tolerance [173]. Soil moisture is another critical factor that regulates microbial activity and gene transfer. Drought conditions often result in reduced soil moisture, which can stress microbial communities. In response to such stress, microorganisms may engage in HGT to acquire genes that confer drought tolerance, allowing them to survive in arid environments. The movement of genes associated with osmoprotectants and stress response is particularly important for microbial survival during water scarcity [174]. The abundance of pathogenic and non-pathogenic microbial communities is a key determinant of the potential for gene exchange between these groups. A high density of microbial populations increases the likelihood of HGT, particularly in environments where drought exerts selective pressure. This gene exchange can involve traits related to virulence, antibiotic resistance, and stress response, significantly influencing the survival and ecological success of both pathogens and non-pathogens [175]. Host susceptibility plays a crucial role in the dynamics of HGT under drought conditions. Plants under stress such as drought may become more vulnerable to pathogen invasion. This increased susceptibility can create opportunities for HGT between pathogenic and beneficial microbes. As a result, genes that enhance or diminish the virulence of pathogens or the protective capabilities of beneficial microbes may be transferred, affecting the overall health of the soil–plant system [38].

Therefore, HGT within the soil microbiome is a multifaceted process influenced by a combination of key biotic and abiotic factors. Understanding how soil–plant microbiome influences HGT, especially under drought conditions, is essential for predicting microbial interactions and their implications for soil health and plant productivity. As climate change continues to alter environmental conditions, further research into these dynamics will be crucial for developing sustainable agricultural practices.

7. Summary

The review has provided a detailed examination of the contrasting adaptive strategies employed by beneficial and pathogenic soil bacterial and fungal communities in response to climate-induced drought stress. Key results are the following: 1. Both pathogenic and non-pathogenic microorganisms undergo a range of cellular, genetic, and enzymatic changes to survive under drought conditions. Common adaptation mechanisms include the production of osmoprotectants, altered gene expression, and biofilm formation. 2. There are distinct differences in the focus of adaptive strategies between pathogens and mutualistic (beneficial) microbes. Pathogens tend to prioritize virulence factors and suppress plant growth, while beneficial microbes enhance plant growth and stress tolerance. 3. Horizontal gene transfer (HGT) is a crucial adaptive mechanism, allowing both pathogenic and non-pathogenic microbes to acquire beneficial traits like stress tolerance and virulence factors. Environmental stressors like drought can promote increased genetic exchange and the spread of pathogenic traits. Horizontal gene transfer (HGT) within the soil microbiome is a vital process influenced by a mix of biotic and abiotic factors within the soil–plant microbial ecosystem. 4. The complex interplay between drought-adapted microbes, both beneficial and pathogenic, and their interactions with plants, highlights the need for a deeper understanding of soil microbiome dynamics under climate change. In conclusion, this review highlights the various survival strategies of soil microorganisms during climate-induced drought, shedding light on the adaptive mechanisms and evolutionary trajectories of both beneficial and pathogenic soil-microbiome members. These insights are crucial for enhancing sustainable agriculture and aiding experts in agronomy, pathology, microbiology and ecology. With this knowledge, researchers can lead pioneering studies and develop effective strategies to combat challenges posed by global warming. Utilizing innovative methods to harness plant–soil microbial resources, these efforts aim to significantly benefit crop producers globally.