Microbial diversity and functions in saline soils: A review from a biogeochemical perspective

Graphical abstract

Highlights

• •Recent advances in microbial diversity and key taxa in saline soils are summarized.
• •The threshold effect of salinity on soil C and N turnover exists in salinized soils.
• •Soil microorganisms have higher resistance to salt stress in already salinized soils.
• •Salt-tolerant microorganisms promote plant growth in a variety of ways.
• •Microbial resources developed by multi-omics are beneficial to saline ecosystems.

Abstract

Background

Soil salinization threatens food security and ecosystem health, and is one of the important drivers to the degradation of many ecosystems around the world. Soil microorganisms have extremely high diversity and participate in a variety of key ecological processes. They are important guarantees for soil health and sustainable ecosystem development. However, our understanding of the diversity and function of soil microorganisms under the change of increased soil salinization is fragmented.

Aim of Review

Here, we summarize the changes in soil microbial diversity and function under the influence of soil salinization in diverse natural ecosystems. We particularly focus on the diversity of soil bacteria and fungi under salt stress and the changes in their emerging functions (such as their mediated biogeochemical processes). This study also discusses how to use the soil microbiome in saline soils to deal with soil salinization for supporting sustainable ecosystems, and puts forward the knowledge gaps and the research directions that need to be strengthened in the future.

Key Scientific Concepts of Review

Due to the rapid development of molecular-based biotechnology (especially high-throughput sequencing technology), the diversity and community composition and functional genes of soil microorganisms have been extensively characterized in different habitats. Clarifying the responding pattern of microbial-mediated nutrient cycling under salt stress and developing and utilizing microorganisms to weaken the adverse effects of salt stress on plants and soil, which are of guiding significance for agricultural production and ecosystem management in saline lands.

Introduction

Soil salinization has been one of the major issues that substantially affect the structure, processes, and functions of global ecosystems [1], including soil nutrient cycling [2], [3], organic matter decomposition [4], plant productivity [5], [6], and biodiversity [7]. Under future climate change scenarios, it is predicted that global soil salinization will be exacerbated [8]. Soil degradation due to increased salinization has detrimental impacts on crop production and human well-being [9]. Given the projected sea-level rise (SLR) by climate change, soil salinization in the coastal area will directly act on population migration by reducing crop yield and negatively influencing regional socioeconomic development [10].

The causes of soil salinization are diverse and can occur in all climatic conditions [11], [12]. Generally, there are two types of soil salinization based on the dominant role of natural and human-induced actions: primary salinization and secondary salinization (Fig. 1). Soil primary salinization is mainly linked with the local climate, parent material, soil properties, and groundwater. Insufficient rainfall to replenish higher evapotranspiration or rising groundwater level can also lead to increased soil salinity [13]. Secondary or human-induced salinization is introduced by the inappropriate use of soil by humans. Saline irrigation combined with poor drainage conditions can easily result in salt accumulation on the soil surface. For coastal areas, seawater intrusion due to rising temperatures and rapid urbanization is projected to increase in future climate change scenarios [14]. Drought-induced salinity intrusion can also lead to the salinization of freshwater marsh wetlands, which in turn affects wetland ecological processes and functions (e.g., carbon dynamics) [15]. In short, a better understanding of the causes of salinization can guide targeted measures to avoid soil degradation in the future.

Fig. 1.

Causes of soil salinization including primary salinization and secondary salinization. A, shallow groundwater table and higher evaporation make soil accumulate salt (photo credit: Qingqing Zhao); B, saline water irrigation exacerbates the salinization of farmland soil (photo credit: Xiuyan Yang); C, drought-induced soil salinization in the coastal supratidal zone in the Yellow River Delta (photo credit: Guangliang Zhang); D, shallow groundwater and inappropriate management degrade the soil (photo credit: Guangmei Wang). (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)

As a critical driver of plant productivity and ecosystem micro-scale processes, soil microorganisms, how they respond to and adapt to the changing soil salinization condition and then perform vital functions, has been a hot topic in the field of environmental microbiology in recent years [16], [17], [18]. Soil microorganisms are also considered to be defenders used in the future to combat climate change and other adverse effects on ecosystems [19]. Therefore, we need to clarify the potential effects of salinization on soil microbial composition in diverse ecosystems and decipher the changing pattern in microbial-mediated ecosystem functions caused by increasing salinity.

Increased soil salinity is considered to be unfavorable to crop yield in most agricultural ecosystems, it has also been reported to cause ecosystem degradation in grassland and forest ecosystems [20], [21]. However, some studies have found that, for coastal wetlands, increasing salinity associated with SLR within a certain range is conducive to plant primary production, thereby promoting carbon storage [22], [23], [24]. Therefore, in the context of predictable future soil salinity changes, specific management practices should be adopted for different ecosystems to maintain soil health, which is conducive to the performance of ecological services. The important roles of microorganisms in saline soils are inevitably needed to be fully understood and revealed for the ecosystems.

In this review, we summarize the existing information on soil microbial diversity, community composition, and microbial-mediated biogeochemical processes under soil salt stress. Meanwhile, we emphasize the development and utilization of soil microbial resources in saline-alkaline soils to serve crop production, plant growth, and degraded soil restoration. Future research directions and priorities were also put forward. We hope this can contribute to generating progress in the understanding of microbial biodiversity and functions under the influence of soil salinization.

Mechanism of microbial response to soil salt stress

Within a given range of salinity fluctuations, soil microorganisms can adjust their own physiological metabolism to respond to salt stress. Some halophilic microbes can actively absorb salt ions (predominantly potassium ions) to increase cell osmotic pressure when the external salinity increases, sometimes accompanied by exporting sodium ions from the cell [25]. Alternatively, by synthesizing low-molecular-weight organic compounds, such as some amino acids and carbohydrates, in microbial cells, microorganisms can balance the osmotic pressure inside and outside the cell [4], [26]. Both osmo-adaptation strategies are undoubtedly energy-consuming.

In addition, microorganisms will also hibernate for a period of time to cope with unfavorable environmental conditions in salt marshes with frequent salinity fluctuation [27]. Owing to strong environmental perturbations such as nutrient and oxygen concentrations, the proportion of dormant microbial taxa can reach more than half or even higher in salt marsh sediments [28]. There is also a report that bacterial dormancy is more prevalent in freshwater habitats than hypersaline lakes, which may be due to the fact that these extremophiles need dormancy less often to thrive and survive in the hypersaline condition [29]. Indeed, excessive salinity stress means cell lysis and death for some intolerant microorganisms.

Soil microbial diversity and community in saline soils

Response patterns of soil microbial diversity along gradients of increasing salinity are habitat-specific or context-specific. Recent advances in the field of molecular ecology, especially the development of multiple ‘omics’ technologies, can provide insights into the changes or succession of diverse microbial taxa with increasing soil salt stress. Early comprehensive analysis showed that salinity was the major environmental determinant of microbial community composition than temperature, pH, and other physicochemical factors across global diverse environments [30], and saline soils were allowed to find new microbial diversity. However, at the local scale, the influencing strength of salinity is less important for microbial assemblage, particularly in ecosystems that are already salt-rich [31]. For instance, along a marine-terrestrial transition, soil physical structure and soil organic matter were the best predictors of fungal communities in coastal ecosystems [32]. Soil bacterial community assemblage was also collectively explained by the soil’s physical structure, pH, and salinity in this salt marsh chronosequence [33].

There are fundamental differences in the response of different soil microbial taxa to salt stress. It has been reported that soil salinity was not the constraint of bacterial communities in hypersaline soils, while the populations of archaea were significantly correlated with soil sodium concentration and electrical conductivity in these soils [31]. In a desert ecosystem, soil salinity imposed a strong pressure on prokaryotic communities, and a significant negative correlation between microbial diversity, richness and phylogenetic diversity (PD), and soil salinity level (with a range of 0–2.5 mS cm⁻¹) was detected [34]. Unexpectedly, within a range of soil electrical conductivity of 0–18 mS cm⁻¹ across oligohaline to hypersaline estuarine wetlands, bacterial alpha diversity reached the highest in moderate saline soils [35]. Similarly, along an estuarine salinity gradient, soil fungal richness was highest in the brackish marsh with intermediate salinity, but the presence of plants had an impact on fungal diversity that cannot be ignored [36]. Differences in the response of microbial diversity to salt stress in different studies should be related to the community composition of the microorganisms studied.

It is generally believed that fungi have a stronger ability to cope with osmotic stress than bacteria. However, the increasing importance of fungi under higher salinity levels has not been well presented [4]. Usually, land degradation due to soil salinization can lead to a shift in plant diversity, which directly affects microbial diversity and composition. For instance, grassland degradation that may be caused by soil salinization reduced the Shannon diversity of soil bacteria and fungi, and it was also found that fungi exerted a greater changing magnitude than bacteria [37]. In acidic soils dominated by fungal biomass in the floodplain of the Werra River in Germany, as soil salinity increased, the microbial community shifted toward increased prokaryotic abundance [38]. In arid and semi-arid areas grown with halophytes Leymus chinensis, the soil rhizosphere bacterial community was more tightly associated with soil salinization than soil fungi [39]. Collectively, when evaluating patterns of response of different microbial taxa to salt stress, soil background properties and vegetation types need to be taken into account.

Soil harbors extremely diverse microbial species with different physiological characteristics. A large number of salt-tolerant microbial taxa are also recognized in different ecosystems. In a polar desert, Firmicutes can largely replace Acidobacteria and Actinobacteria in soils with increasing salinity [40], as microbial taxa affiliated with Firmicutes have Gram-positive cell walls and can form spore, which makes them resistant to harsh environments [41]. The Bacillus genera assigned to Firmicutes were also proven to produce halophilic enzymes in saline soils [42]. In natural saline soil, an increased abundance of Bacteroidetes in soils with higher salinity levels was verified [43]. Some well-known halotolerant bacteria classified into Gammaproteobacteria, Alphaproteobacteria, Bacteroidetes, and Verrucomicrobia were also identified in soils with the halophyte Suaeda salsa to help this non-host plant to withstand salinity [44]. These taxa were also found to be enriched in hypersaline soils in coastal wetlands [35] and degraded grasslands [37]. A study also revealed that microbial taxa belonging to Proteobacteria, Bacteroidetes, Actinobacteria, and Halobacteria have a high-salinity niche preference in desert soils [34]. Archaea living in hypersaline systems often harbor a phylogenetically diverse group with complex metabolic pathways to persist here [45], and some ectomycorrhizal fungi such as Tomentella, Lactarius, and Phialocephala were abundant in more saline soils grown with Black alder (Alnus glutinosa Gaertn.), but their dominance changed with plant development [46].

Soil microbial functions under salt stress

Microbial biomass and growth with increasing soil salinity

Soil microbial biomass and growth are important biological indicators for soil health assessment [47], [48]. Salinization-driven changes in microbial biomass and growth are pertinent to soil carbon dynamics and greenhouse gas emissions [49], [50]. There is no general pattern for the relationship between salinity and soil microbial biomass (or microbial biomass per unit of organic carbon) in environments including natural and manipulated soils, as reviewed by Rath and Rousk [4]. This is because the microbial biomass in the soil is constrained by a variety of historical and current environmental conditions [51], [52]. The quantification method may also affect the estimation of microbial biomass under salt stress. The quantificational polymerase chain reaction (qPCR) exhibited greater sensitivity in estimating microbial biomass in soils along salinity gradients than the lipid-based method [53]. Because of the different salt tolerance of bacteria and fungi to salt stress, the contribution of microbial residues to soil organic carbon (SOC) storage is salinity dependent. With the salinization of coastal wetlands, microbial necromass contribution to SOC shifts from fungal- to bacterial-dominated residue [54]. In addition to soil bacteria and fungi, by compiling data from published literature, recent research in coastal ecosystems also found that, as a top-tier heterotrophic microbial group, the productivity of testate amoebae reduced with increasing salinity [7].

For the influence of soil salinity on microbial growth, a consensus has gradually been reached on the depressive effect of excessive salinity on microbial growth in natural and agricultural land. By adding different salt solutions to a nonsaline soil, bacterial and fungal growth rates (leucine incorporation and acetate incorporation into ergosterol, respectively) were quantified and found that soil microbial growth was obviously inhibited by the salt exposure [55]. They also pointed out that fungi were more resistant to salt exposure than bacteria as revealed by the growth-based measurements. On the contrary, a study concluded that bacterial salt tolerance was less related to soil salinity across an arid agricultural salinity gradient [56]. The inhibitory effect of salinity on microbial growth is also indirectly caused by the availability of soil moisture and soil organic matter [53]. An updated research demonstrated that saline soils had higher bacterial salt resistance than low-salt soil, and an increased salinity within the appropriate range enhanced the growth of bacteria [17]. A study by Yan and Marschner [57] showed that microbes in saline soils did not have a stronger salt resistance than in non-salinized soils, microbial activity and biomass in saline soils were substantially regulated by substrate availability. Trait-based microbiological research is more conducive for us to reveal the microbial growth response under salt stress [58].

Soil organic carbon decomposition

SOC decomposition is one of the most basic and concerned ecological processes in belowground ecology and soil science. There is an urgent need to integrate microbial community ecology into belowground biogeochemistry to advance our understanding of soil biogeochemical cycles [59]. Previous studies have reviewed the SOC decomposition and dynamics in saline-alkaline soils and/or under salt stress [4], [60]. Here, we pay more attention to how microorganisms respond to salt stress and then regulate organic carbon decomposition.

The direction and magnitude of response in SOC decomposition to salinization are related to the background of the soil studied. By investigating soil microbial growth and soil respiration along natural salinity gradients, a strong negative correlation was observed between cumulative carbon emission and salinity, which was mainly ascribed to the fact that increased salinity directly inhibited the microbial growth rate, and ultimately led to the decrease in the decomposition of organic carbon [53]. A number of previous studies have also observed that the increase in salinity significantly inhibits the rate of organic carbon mineralization in different types of soils [4], [61], [62]. The types of ions in the process of soil salinization can also differ in the decomposition intensity of organic carbon. The inhibitory magnitude of sodium chloride on SOC decomposition (also including microbial growth) was higher than that of sulfate [55]. Salinity ionic stress may have a larger inhibitory effect on both aerobic and anaerobic carbon mineralization than the sulfate in a short-term microcosm experiment [63].

In tidal wetlands where freshwater and saltwater interact, ranging from freshwater to oligohaline conditions, salinity increases could dramatically promote the activity of carbon-degrading extracellular enzymes and thereby increased soil microbial decomposition rates in these low salinity tidal wetlands [64]. Furthermore, a global meta-analysis presented that hydrolytic carbon-acquiring enzyme activities were reduced by salinization, but oxidative carbon-acquiring enzymes were enhanced in tidal wetlands, yet salinization still exerted adverse effects on soil organic carbon storage from a comprehensive perspective [65]. Field investigation and analysis based on metagenomic sequencing in saline soils also provided clear evidence that microbial carbon metabolic potentials (carbohydrate metabolism and genes encoding glycosyl transferases and glycoside hydrolases) were negatively correlated with soil salinity, therefore higher saline soils corresponded to low carbon emissions [66]. Based on these collected research results, the increase in soil salinity is not beneficial to the long-term storage of soil organic carbon.

Meanwhile, an incubation experiment revealed that, compared with liable carbon resources such as glucose, salinity reduced the ability of microorganisms to decompose cellulose more although the microbial characteristics of the tested saline and non-saline soil should be different [67]. In an investigation study of the microbial functional gene abundance along a coastal salinity gradient, the abundance of most genes encoding carbon degradation was negatively correlated with salinity, however, the abundance of gene encoding ligninase increased with enhancing soil salinity [35]. This may be due to the higher proportion of recalcitrant carbon in high-salt environments [68]. Overall, it’s needed to link the microbial functional genes with microbial carbon degrading enzymes when understanding the roles of the microbial community in regulating SOC turnover in the context of soil salinization.

Microbial carbon use efficiency (CUE), which reflects the partitioning of carbon allocation between microbial growth and respiration, was also explored under soil salinization in some studies. Soil microbial CUE inferred by eco-enzymatic stoichiometry follows a unimodal pattern along a salinity gradient in coastal soils [69]. Within a controllable range of increased salinity, higher salinity promoted microbial CUE with less effect on microbial growth. Increasing salinity also affects SOC decomposition and its sequestration by suppressing plant productivity, as quantified at a broad scale [70]. An attempt has been made to relate CUE to microbial genome size and suggested that larger genomes can access a wider variety of carbon substrates and thus behave with higher CUE [71]. Increasing salinity by saltwater intrusion significantly altered soil microbial diversity and communities, but microbial CUE was less influenced [72]. The emerged microbial functions (e.g., CUE) can be indirectly affected, such as by mediating soil structure, plant biodiversity, and nutrient state under soil salinization [73], [74], [75]. For instance, increasing soil salinity decreased microbial enzyme activities, but increased the metabolic quotient (higher metabolic quotient means lower CUE), the presence of plants in saline soils can relieve the adverse effects of salinity on microbial catabolism [76].

With the more refined description of the composition of soil microbial communities at the taxonomic level, it has become a critical topic to predict soil CUE by analyzing the dynamics of soil microbial communities under soil salinization, but so far there is no such research. Incorporating microbial CUE into the next-generation model of soil biogeochemistry is needed, we know less about this, especially in saline soils.

Soil nitrogen cycling

Nitrogen cycling in soils includes nitrogen mineralization, nitrogen fixation, nitrification, denitrification, dissimilatory nitrate reduction to ammonium (DNRA), anaerobic ammonium oxidation (Anammox), and so on (as shown in Fig. 2 and ref. [77]). The nitrogen turnover in soils is jointly affected by physical (nitrate leaching, [78]), chemical (ammonia volatilization and dissolution, [79]), and biological processes (plant uptake and microbial utilization, [80]). Here, we focus on nitrogen cycling processes mediated by soil microorganisms, including nitrogen biogeochemical rate, functional gene abundance, and microbial communities involved in nitrogen transformation under soil salinization.

Fig. 2.

Soil microbial nitrogen metabolism across oxic and anoxic conditions, which includes nitrogen forms, nitrogen processes, and main functional genes involved in nitrogen cycling.

Nitrogen mineralization refers to the process by which organic nitrogen in the soil is converted into inorganic nitrogen under the action of soil microorganisms. A review suggested that soil salinization had negative effects on nitrogen mineralization in coastal wetlands as microbial activity could be inhibited by the increasing salinity [81]. On the contrary, a meta-analysis indicated that soil salinization significantly increased net nitrogen mineralization, because greater nitrogen content in plant detritus and higher abundance of specific microbial groups responsible for nitrogen mineralization can be used to explain the result [3]. Most current estimates of nitrogen mineralization rates are based on the changes of ammonium over time in the field or incubation. The DNRA process can produce ammonium, and ammonium can also be assimilated or nitrified by microorganisms. Therefore, the ¹⁵N tracer technology can be a more scientific and effective method for nitrogen mineralization estimation [82].

Nitrification is an aerobic process mediated by ammonia oxidizers (also called nitrifiers) that oxidizes ammonia to nitrite or nitrate. The effect of salt stress on soil nitrification is tightly related to the degree of soil salinization. As reported by ref. [82], in the initial stage of soil salinization, seawater intrusion in coastal wetlands simulated by adding salt solution significantly inhibited potential nitrification rates but increased markedly the nitrification rates in the later stage of salinization. Within a wider range of soil salinity fluctuations (0–20 mS cm⁻¹), the abundance of functional genes (such as amoA and hao) decreased along with increasing salinity gradients [35], [84]. There may be an optimal salinity threshold for the activity of nitrifiers [3]: within an optimum of increasing salinity, the nitrification rate could be enhanced; extensive salinity can make a suppressive influence on nitrification rates by constraining the microbial physiology [85]. Different nitrifier groups can exhibit distinct sensitivity to increasing salt exposure. Culture experiments showed that ammonia-oxidizing bacteria (AOB) can dominate nitrification and pose higher abundance at intermediate salinity, while ammonia-oxidizing archaea (AOA) exhibited higher salinity tolerance with less affected after salinity elevation [86]. By combining ¹³C-DNA stable-isotope probing (SIP) with genomic sequencing, a considerable number of salt tolerance ammonia oxidizers belonging to Nitrosococcus and Nitrosospira in saline and non-saline agricultural soils were identified [18]. These ammonia oxidizers hold a variety of genes participating in Na⁺ extrusion /H⁺ import, and compatible solutes biosynthesis.

Traditionally, two steps are involved in nitrification: ammonia oxidizers firstly oxidize ammonia to nitrite, then nitrite-oxidizing bacteria (NOB) convert nitrite to nitrate [82]. Complete nitrifiers such as Nitrospira bacteria were found that they can directly use catalyze ammonia to nitrate (also called comammox or complete ammonia oxidation) [87], [88]. However, we know less about them in saline soils which also represent a specific environment.

The influence of soil salinization on denitrification varies with soil background salinity level, salinization stage, and ecosystems. Depressed denitrification was observed in tidal freshwater wetland soils after exposure to saline water in the Hudson River, USA [89]. A laboratory-incubated experiment in tidal forest soils showed that increasing salinity stimulated denitrification in soils with lower background salinity, but had less effect in soils with relatively higher background salinity levels [90]. Inferred from the results by ref. [83], in the initial stage of soil salinization, low salinity promoted soil denitrification but inhibited nitrification, resulting in higher N₂O emission; in the later stage of salinized soil development, salinity significantly promoted nitrification, which provided more nitrate substrates for the denitrification although it was depressed, as a consequence, higher N₂O generation was also observed. A meta-analysis also suggested that soil salinization effect on denitrification was not statistically significant although there was a decreasing trend between them across coastal wetlands [3]. Considering the fact that soil denitrification preferentially occurs in anoxic conditions, changes in soil redox environment, moisture, and substrate availability caused by soil salinization can have a non-negligible impact on denitrification [91].

Increasing soil salinity also has contrasting effects on microbial DNRA. Microbial DNRA and denitrification all reduce nitrate, denitrification can cause nitrogen loss in the form of nitrogen gas whereas DNRA can result in the conservation of nitrogen (NH₄⁺) in soils [92]. By comparing the soil denitrification and DNRA potentials in freshwater and oligohaline wetlands, it was observed that increasing salinity shifted the nitrate reduction regime from denitrification toward DNRA [93]. A similar study also suggested the positive relationship between the DNRA and salinity level in the freshwater wetlands of Massachusetts, USA [94]. An integrated data analysis showed that soil salinization generally suppressed the DNRA [3]. Factors controlling soil DNRA are complex, soil DNRA potential was more regulated by substrates rather than nrfA gene abundance along an estuarine and intertidal wetland [95]. Soil organic matter quality and sulfide content also play important roles in the partitioning of the DNRA and denitrification in estuarine saline soils [93], [96]. Soil DNRA can be more favored in anoxic environments when organic carbon or sulfide are effective, whereas denitrification would be more supported in soils with limited electron donors but sufficient nitrate [82].

Anammox is also a key pathway that is responsible for nitrogen loss in soils (NH₄⁺ + NO₂^– → 2H₂O + N₂), which is mediated by specialized microbes and ubiquitous in natural and artificial settings [97]. Anammox bacteria are also more prevalent in saline/alkaline than acidic soils [98], which are affiliated with the Planctomycetes phylum with slow growth rates [99]. Although the contribution of Anammox to N₂ production was low compared to denitrification in tidal marshes, the highest relative importance of Anammox was observed in low salinity marshes, increasing salinity lowered the importance of Anammox to nitrogen removal [100]. It has been also demonstrated that soil N₂ production in coastal tidal flats and inland paddy was dominantly contributed by denitrification over Anammox, and soil salinity driven the Anammox bacterial community in coastal flats (dominated by Candidatus Scalindua and Candidatus Kuenenia) and paddy soils (dominated by Candidatus Brocadia) [101]. Incubation experiments proposed that the low-salinity treatment stimulated the soil Anammox but it was inhibited by high-salinity addition [102]. A meta-analysis by ref. [3] manifested that soil salinization on average stimulated Anammox more than twofold. A higher abundance of hzo gene (mediating the Anammox process) was also observed in soils located in tidally influenced wetlands than that in riverine wetlands [35]. Anammox bacteria generally exhibited higher salt tolerance, which makes them to adapt high-salt environments, this may explain the increasing trend of Anammox potential after salinity exposure [103]. Collectively, we summarize a conceptual diagram based on existing reports on soil carbon and nitrogen cycles under the influence of salinization across different ecosystems (Fig. 3).

Fig. 3.

Conceptual diagram indicating the response of microbial diversity, microbial growth rate, SOC decomposition, microbial carbon use efficiency (CUE), and soil nitrogen metabolism to increasing salinity in non-saline and saline soils based on previous studies.

Soil phosphorus and sulfur cycling

Phosphorus and sulfur are widely involved in the synthesis of microbial cell membranes, DNA, and proteins in the soil [104]. However, there is much less research on the changes in soil phosphorus and sulfur and the role of microorganisms under the influence of salinization than carbon and nitrogen turnover.

Existing studies have shown that salinity affects the availability of phosphorus in the soil. For instance, when freshwater forested wetlands were converted into oligohaline marshes, phosphorus mineralization was stimulated by soil salinification [105]. Compared with freshwater wetlands, soils in brackish wetlands contained higher available phosphorus which can well be ascribed to the higher abundance of genes that participated in phosphorus solubilization (e.g., gcd and ppa) and phosphorus mineralization (e.g., phoD, phy, and ugpQ) [106]. This study also implied that slight salinization of coastal freshwater wetlands may enhance the soil phosphorus availability by regulating the microbial community mediating phosphorus cycling. Some salt-tolerant phosphate solubilizing bacteria (PSB) also exist in saline soils, which play critical roles in solubilizing unavailable phosphorus into bioavailable phosphorus [107].

Sulfur oxidation and reduction are the main metabolic processes in soil sulfur cycling, which are microbially carried out by sulfur-oxidizing (SOB) and sulfur-reducing bacteria (SRB) in all ecosystems [108]. Wetland salinization could increase the generation of sulfides which are toxic for plant growth [109]. Increased soil salt stress can reduce soil oxygen availability, as a consequence, induce the accumulation of sulfide in soils [89]. Some SOB and SRB groups living in salt-saturating conditions have been found, such as the SOB genera Thioalkalivibrio, Thioalkalimicrobium, Thioalkalispira, and Thioalkalibacter within the Gammaproteobacteria, the SRB genera Desulfonatronovibrio, Desulfonatronum, and Desulfonatronospira belonging to Desulfovibrionales [110]. The SOB and SRB communities and their mediated sulfur-cycling processes in saline soils are needed to be characterized in detail.

Applying soil microbiome to cope with soil salinization

Soil microorganisms are viewed as an important tool against the threat of irreversible global salinization, as they can mitigate some negative impacts of salt stress on plants [111]. Saline soils are important sources because they provide specific habitats for many novel salt-tolerant microorganisms, where researchers have isolated a large number of plant growth-promoting (PGP) microorganisms and applied them to agricultural production or degraded soil restoration. For instance, some 1-aminocyclopropane-1-carboxycarboxylate (ACC) deaminase-producing bacteria from rice rhizosphere in coastal soils were isolated and their considerable positive impacts on seed germination and root growth were observed [112]. Bacteria belonging to Bacillales, Actinomycetales, Rhizobiales, and Oceanospirillales have also been isolated from paddy soil, and the growth-promoting effect of rice could be associated with the production of ACC deaminase, induction of proline accumulation, and reduction of the salt-induced malondialdehyde in the plant [113]. A study demonstrated that the core microbiome in the rhizosphere of Halophyte Suaeda salsa holds genes encoding the processes of salt stress acclimatization and nutrient solubilization in coastal saline soils [44].

And many salt-tolerant PGP microorganisms have been effectively identified and characterized as potential PGP groups for application to plant growth in saline soils, such as Azotobacter, Bacillus, Brevibacterium, Halococcus, Lysinibacillus, Paenibacillus, Pseudomonas and so on [114]. Plants can also recruit the specific salt-tolerant bacterial consortium instead of individual bacterial members for enduring resistance against salt stress and promoting plant growth [115].

There are several mechanisms that can explain the improving plant tolerance by salt-tolerant microorganisms under salt stress (Fig. 4). Some salt-tolerant PGP bacteria are able to encode the ACC deaminase to degrade the ACC (the precursor of ethylene) and reduce the negative effects of ethylene on plant growth [116]. PGP bacteria can also be tightly associated with plant roots and produce some osmolytes (e.g., carbohydrates and proteins) to alleviate the osmotic stress [117]. Some halotolerant PGP bacteria can colonize in plant roots as endophytic bacteria, and various antimicrobial metabolites are produced against pathogens under stressful conditions [118]. It was also found that the PGP bacteria Kocuria erythromyxa EY43 and Staphylococcus kloosii EY37 can decline the absorption of toxic ions (sodium and chloride ions) from saline soils for the growth of the strawberry plant [119]. The applications of salt-tolerant PSB are viewed as an effective and economical way to manage the phosphorus deficit in saline soils as they can activate the bio-unavailable phosphorus in saline soils [107]. Several halotolerant bacterial isolates (belonging to Klebsiella, Pseudomonas, Agrobacterium, and Ochrobactrum) have the ability to fix nitrogen and produce ACC deaminase, thereby enhancing peanut seedlings and growth [120]. Arbuscular mycorrhizal fungi (AMF) are also highly hoped to alleviate salinity stress for host plants due to their importance in plant nutrition uptake, water absorption, and protection from pathogens [121].

Fig. 4.

Mechanisms of salt-tolerant plant growth-promoting microbes to assist plant growth enduring salt stress in saline soils.

Under stressed conditions, plants can promote the growth of specific microorganisms in the rhizosphere by regulating the composition of root exudates, thus improving the adaptation of plants in harsh ecosystems [122]. Changes in root exudates (e.g., phenolic acids and terpenoids) directly affect the composition and metabolic activity of the rhizosphere microbiome [123]. In turn, root exudates contribute to the formation of carbon pools such as microbial residues and mineral-associated organic carbon (MAOC) in the soil [124], then affecting soil carbon sequestration in saline soils. However, until now, we still lack an integrated understanding of the plant-microbial-soil systemic responses to salt stress.

The rapid development of metagenomics and other molecular techniques provide a powerful tool for the exploration of more salt-tolerant microorganisms, which can help us to have a better understanding of how these microorganisms survive in saline soils and how they affect soil health and mediate ecosystem functions [125]. Therefore, we propose that the development of microbial resources in saline soils through advanced omics techniques is beneficial to ecosystem health and sustainable agriculture. It is a convenient and effective way to capture changes in microbial diversity and community structure under salt stress through the application of metagenomic sequencing technology (Fig. 5). We can also use transcriptomics to analyze the metabolic processes and gene regulation of active microorganisms during salt stresses [126]. Considering that salt stress can cause changes in the expression of defense-related proteins, activation of antioxidant machinery, accumulation of osmolytes, and exopolysaccharides synthesis [127], it’s particularly important to reveal the molecular mechanisms of salt stress on microbial and plant cells through these multi-omics approaches, also including metaproteomics and metabolomics. Soil bioengineering tools like metagenomics and metabolomics can help decipher novel microbial metabolites from stressed ecosystems [128]. Microbial salt-specific metabolites and triggered genes can also be explored by these multi-omics in the near future [129].

Fig. 5.

Multi-omics approaches applied to saline soils for developing microbial resources.

The combination of several molecular ‘omics’ approaches makes it possible to reveal new mechanisms of microbially driven processes under environmental changes [130]. With the help of microbiome-assisted strategies, soil-borne plant pathogens can be effectively suppressed through the manipulation of soil microbiota, such as by soil pre-fumigation, organic amendment, crop rotation, and intercropping in agricultural ecosystems [131]. In natural settings, plants often selectively recruit beneficial microbiomes in the rhizosphere by changing the composition of root exudates to withstand harsh environments [132]. A recent review also pointed out that inoculation with key microbiota members has the potential to improve plant growth by influencing plant traits [133].

Additionally, the alteration of soil microbial communities and functions by emerging pollutants (EPs), in particular, such as micro/nanoplastics, metallic nanoparticles (MNPs), antibiotics, and organophosphate esters (OPEs), cannot be ignored [134], [135], [136] in saline soils. It has been becoming a hot topic to disentangle how these EPs, in conjunction with environmental changes (e.g., saline stress), affect microbially mediated processes of geochemical cycling and energy flow [134], [137].

Knowledge gaps and research priorities

Soil salinization is one of the major global issues due to its adverse influence on agricultural productivity and ecosystem sustainability. Numerous molecular-based surveys have been conducted to explore the changing pattern of microbial diversity and community in saline soils from diverse ecosystems including coastal wetlands [32], [35], desert ecosystems [34], inland Salt Lake [17], forest [47], [85], grassland [72], and agriculture [138]. These studies mainly focused on soil bacteria and fungi, seldom research explored the diversity and functions of archaea and protists although they also play critical roles in soil microbial food web and microbial-mediated biochemistry in saline soils [139], [140], [141]. In salinized soils caused by either natural or artificial factors, the general pattern and community assembly of them are needed to be extensively clarified and revealed in different habitats.

Recent studies emphasized that microbial roles in mediating soil biogeochemical cycles should be incorporated into the process-based models to improve the accuracy of earth biogeochemical models [142]. Whereas these models are less been focused on the effect of soil salinization on microbial-driven functions such as SOC decomposition, nutrient turnover, and greenhouse gas emission. Especially, less research can accurately capture the periodic fluctuations in microbial diversity and its induced effect on biogeochemical cycles with the occurrence of soil salinization.

Soil salinization not just affects changes in edaphic properties, but also leads to the succession of vegetation and alternation in environmental conditions. It is necessary to strengthen the research on the spatial–temporal stability of microbial communities under salt stress, tipping points, disturbance-recovery processes, and the importance of historical events and local context in driving community response to the changing salinity in soils.

Soil, microorganisms, and plants interact with each other and perform various ecological functions. The tripartite interaction between them was reviewed and discussed in different environments [143], [144]. However, in salinized soils, microbial diversity, plant growth, and soil conditions are often explored individually or in pairs. We lack the understanding of how the interaction between them changes under salinization. The microbial omics technology and advanced microscopy should provide new insights into these mechanisms of interaction between saline soil, microorganisms, and plant.

Meanwhile, future research needs to enhance the mechanistic understanding of how soil microorganisms regulate context-dependent biogeochemical processes across spatial and temporal scales. The development of salt-tolerant functional microorganisms in different habitats can help to deal with the adverse effects on ecosystem functions by soil salinization. For instance, by applying salt-tolerant plant growth-promoting rhizobacteria (PGPR) (Sphingobacterium BHU-AV3), the inoculated tomato plants promoted salt resistance by decreasing levels of oxidative stress, lipid peroxidation, reactive oxygen species (ROS), and cell death, and enhancing antioxidant activities and energy metabolism [145]. Halotolerant PGP bacteria Staphylococcus sciuri ET101 has also been verified to protect plant photosynthesis by the interplay between carboxylation and oxygenation under salt stress conditions [146]. However, the interaction between microorganisms and plants remains particularly unrevealed under salt stress. Based on remediation or restoration targets, such as plant productivity enhancement, stress resistance, nutrient enhancement, biodiversity maintenance, and greenhouse gas mitigation, we can enhance the development and utilization of targeted microbial resources in saline soils. Then, criteria applicable to different scenarios for microbial resourcefulness should be developed for different saline ecosystems.

Concluding remarks

Soil is a non-renewable resource, it’s difficult to restore it to its original healthy level once degraded by salinization. Soil salinization is occurring at an unprecedented rate across global ecosystems. Climate change and anthropogenic activity are expected to further exacerbate soil salinization. Therefore, it is necessary to develop effective measures to reduce the risk of salinization by anthropogenic activities. This review presents a comprehensive view of the impacts of salt stress on the microbiologically mediated biogeochemical cyclings and highlights that soil microbiome can be harnessed as a nature-based solution for the restoration of salinized soils and saline ecosystem sustainability. Future studies should strengthen the answer to some key questions that help to cope with salt stress and ecosystem degradation, such as:

(1) What is the tipping point for the response of different soil microbial constituents in saline and non-saline soils?

(2) How do alter environmental conditions to modulate microbial diversity and functions under human control?

(3) How to use microbiomes in saline soils to serve human society?

(4) How do microorganisms interact with each other and interplay with upper trophic levels (e.g., nematodes) under salt stress, and how can their interactions be used to guide ecosystem diversity maintenance and smart agricultural production?

Answering these questions will enable us to take active and effective measures to mitigate the adverse effects of soil salinization. We should apply salt-tolerant microorganisms as a biological tool for improving plant salt stress tolerance. Meanwhile, we also emphasize the development of salt-tolerant microorganisms serves agricultural production, environmental pollution control, and restoration of degraded ecosystems, and ultimately benefits human well-being.

Compliance with Ethics Requirements

This article does not contain any studies with human or animal subjects

CRediT authorship contribution statement

Guangliang Zhang: Conceptualization, Writing – original draft. Junhong Bai: Conceptualization, Supervision, Project administration, Writing – review & editing. Yujia Zhai: Writing – review & editing. Jia Jia: Investigation, Validation, Formal analysis. Qingqing Zhao: Investigation, Resources, Formal analysis. Wei Wang: Investigation, Formal analysis. Xingyun Hu: Conceptualization, Visualization.

Declaration of Competing Interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Biographies

guangliang Zhang obtained his Ph.D. degree in Environmental Science at School of Environment, Beijing Normal University in 2022. Now he is a post-doctor at the Advanced Institute of Natural Sciences, Beijing Normal University at Zhuhai. His research focuses on environmental microbiology, soil carbon sequestration, and biogeochemistry in coastal wetlands.

junhong Bai is a professor in Environmental Science at Beijing Normal University. He got his Ph.D. degree from Northeast Institute of Geography and Agroecology, Chinese Academy of Sciences. His research interests include coastal wetland restoration, wetland ecological processes and modeling, wetland biogeochemistry, wetland soil pollution and environmental microbiome.