Nitrogen-Fixing and Phosphate-Solubilizing Soil Bacteria: Comparison
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Please note this is a comparison between Version 2 by Jessie Wu and Version 1 by Sergey Sedykh.

Bacteria that fix atmospheric nitrogen (N2) live in plant tissues (e.g., tubers and roots) and at the soil–rhizosphere interface, and can supply the significant amounts of mineral nitrogen required for plant growth. Phosphate-solubilizing bacteria are known to increase the bioavailability of phosphorus from soil to plants, they solubilize inorganic phosphates and mineralize insoluble organic forms of phosphorus.

  • plant growth-promoting bacteria
  • PGPB
  • soil bacteria
  • rhizosphere bacteria
  • phosphate solubilization
  • biofertilizers

1. Introduction

In the second half of the twentieth century, the use of mineral fertilizers was one of the main factors contributing to crop production development. However, unbalanced fertilizer application has been reported to have a negative impact on crop production sustainability and environmental safety [1]. Another consequence is the loss of soil microbiome diversity, leading to reduced fertility [2,3][2][3]. A promising research avenue currently being explored is the use of bacteria to enhance soil fertility and stimulate crop yields [4]. Plant growth-promoting bacteria (PGPB) and their consortia [5] can naturally enhance plant growth, both directly and indirectly, by fixing atmospheric nitrogen [6], synthesizing plant hormones and siderophores [7], stimulating plant nutrient uptake [8], and suppressing pests and pathogens [9,10][9][10]. Of particular significance is the fact that such bacteria interact with plant roots and increase resistance to abiotic stresses [11].

2. Nitrogen-Fixing Bacteria

Nitrogen fixation has been described for both symbiotic legume bacteria and non-symbiotic soil bacteria (heterotrophic or autotrophic) found in soil or water, or on stones or fallen leaves. Symbiotic bacteria of legume nodules are believed to be the most critical component of the biological fixation of atmospheric nitrogen [14][12]. Non-symbiotic nitrogen-fixing soil bacteria are significantly underrepresented in the literature; existing publications are mainly concerned with cereal crops such as maize, rice, and wheat [15,16,17][13][14][15]. Non-symbiotic nitrogen-fixing bacteria that increase the productivity of cereal crops have been described for the following genera: Azospirillum, Azotobacter, Beijerinckia, Burkholderia, Clostridium, Gluconacetobacter, Herbaspirillum, Methanosarcina, and Paenibacillus [15,18,19][13][16][17].

Non-Symbiotic Nitrogen-Fixing Bacteria

Free-living nitrogen-fixing bacteria have been reported to use, rather than fix, nitrogen when mineral nitrogen is available in soil [20,21][18][19]. The basic enzyme of nitrogen fixation is nitrogenase. Its activity is sensitive to oxygen; requires metals that are part of the enzyme subunits (such as Fe, V, and Mo); depends on ATP and reduced coenzymes; and is low in the presence of mineral nitrogen. Free-living nitrogen-fixing bacteria can be obligate anaerobes, facultative anaerobes, or obligate aerobes found in different environments at different molecular oxygen concentrations. O2 can inhibit nitrogenase and suppress N2 fixation. Nitrogen-fixing bacteria can avoid the potentially negative effects of O2 by isolating the nitrogen fixation in space, e.g., by using structures such as heterocysts, where the oxygen concentration is kept low [22][20]. According to several reports, nitrogen-fixing soil bacteria supply a significant amount of the mineral nitrogen used in agriculture [23][21], making nitrogen fixation the second most important biogeochemical process after photosynthesis. This energy-dependent process requires sixteen ATP molecules to fix one atmospheric nitrogen molecule [6]. Soil bacteria can fix atmospheric nitrogen while exhibiting diazotrophic activity. However, they can also convert mineral nitrogen into NO, N2O, and N2, which is considered undesirable for agroecosystems, especially since N2O is a greenhouse gas. One strain of soil bacteria tends to contain different genes for nitrogen metabolism, with their expression largely dependent on mineral nitrogen availability in the environment. Variants of the soil bacterial consortia have been proposed, which can perform nitrogen fixation and contribute to nitrogen accumulation in the soils of agroecosystems [22][20]. All known forms of nitrogenase require Fe atoms, with most of them also containing metals such as Mo or V [24][22]. The nifH gene, encoding nitrogenase reductase [25][23] as well as several other genetic markers, is widely used to analyze the ability of bacteria to fix nitrogen, as well as the distribution of nitrogen-fixing agents in communities. The availability of cellular ATP and soluble phosphates in the environment significantly influences the process of nitrogen fixation. Additionally, this process depends on the availability of iron ions in the environment and cellular Fe-containing cofactors and enzymes. Nitrogen fixation, in turn, provides the nitrogen compounds necessary for metabolic processes. Given the above, it is beyond doubt that the processes of nitrogen fixation, phosphate solubilization, and siderophore synthesis are interrelated. The synergetic effect of the simultaneous introduction of a consortium of bacteria exhibiting these activities individually, or several activities simultaneously, into the soil can stimulate plant growth and development, meeting the goals and objectives of sustainable agriculture and contributing to the economical and rational use of fertilizers.

3. Phosphate-Solubilizing Microorganisms

Phosphate-solubilizing bacteria [26][24] and mycorrhizal fungi [27][25] are known to increase the bioavailability of phosphorus from soil to plants [28][26]. They solubilize inorganic phosphates and mineralize insoluble organic forms of phosphorus [29][27]. Microorganisms capable of solubilizing phosphorus have been considered in a previous review [8], which describes the phosphate-solubilizing activity of bacteria belonging to the following genera: Aeromonas, Agrobacterium, Azotobacter, Bacillus, Bradyrhizobium, Burkholderia, Cyanobacteria, Enterobacter, Erwinia, Kushneria, Micrococcus, Paenibacillus, Pseudomonas, Rhizobium, Rhodococcus, Salmonella, Serratia, Serratia, Sinomonas, and Thiobacillus. Additionally, consideration is given to fungi belonging to Achrothcium, Alternaria, Arthrobotrys, Aspergillus, Cephalosporium, Chaetomium, Cladosporium, Cunninghamella, Curvularia, Fusarium, Glomus, Helminthosporium, Micromonospora, Phenomiocenspora, Phenomiocenspora, Phenomycylum, Populospora, Pythium, Rhizoctonia, Rhizopus, Saccharomyces, Schizosaccharomyces, Schwanniomyces, Sclerotium, Torula, Trichoderma, and Yarrowia. Among all phosphate-solubilizing microorganisms, bacteria significantly predominate, accounting for up to 50%, while fungi cover up to 0.5%. Most phosphate-solubilizing microorganisms are found in the rhizosphere [30][28].

3.1. Solubilization of Inorganic Phosphorus Compounds

Phosphorus compounds in soil can be both inorganic and organic. The following inorganic phosphate compounds have been described: apatite, strengite, and variscite; in addition to secondary minerals, such as ferric, aluminum, and calcium phosphates [31][29]. It has been established through various studies that the primary mechanism responsible for the mineral phosphate solubilization exhibited by bacteria is the secretion of organic acids [28,31,32][26][29][30]. Soil bacteria have been reported to secrete organic acids, stimulating phosphate solubilization by acidifying the environment and by chelating metal ions from the corresponding inorganic compounds [32,33][30][31]. The solubilization efficiency also significantly depends on the strength and chemical structure of organic acids. For example, carboxylic acids containing a single carboxyl group are known to be less efficient than dicarboxylic or tricarboxylic acids. It has also been demonstrated that aromatic organic acids are less active than the corresponding aliphatic analogs. The methods of mass spectrometry analysis, gas chromatography, and high-performance liquid chromatography [8] have proven that the organic acids secreted by rhizosphere bacteria in soil are involved in phosphate solubilization. These include acetic, adipic, butyric, citric, fumaric, glutaric, glycolic, glyconic, glyoxalic, 2-ketogluconic, lactic, malic, malonic, oxalic, propionic, succinic, and tartaric acids [30][28], with gluconic and 2-ketogluconic acids apparently being the most important. The secretion of organic acids by bacterial cells is associated with several metabolic pathways, such as the direct oxidation of low molecular weight precursors in the periplasm [34][32], and intracellular phosphorylation [35][33].

3.2. Mineralization of Organic Phosphorus Compounds

Soil’s organic phosphorus compounds can account for up to 30–50% of soil phosphorus. Organic phosphorus compounds are mainly found in the form of phytate (inositol phosphate). The other organic soil phosphates described in the scientific literature include nucleic acids; mono-, di-, and tri-esters; and phospholipids [26][24]. Xenobiotic phosphonates are organic phosphorus compounds that can also be found in high concentrations in soil. These include antibiotics, detergents, pesticides, flame retardants, and other compounds. All the molecules mentioned above must be converted into soluble ionic phosphate forms before being assimilated by plant roots [36][34]. Organic compounds are metabolized by enzymes secreted into the environment by phosphate-solubilizing bacteria. Nonspecific acidic phosphatases that cleave phosphate from the ester or phosphoanhydride bond are represented by phosphomonoesterases: alkaline and acidic phosphatases [37,38][35][36]. The phytase enzyme has been demonstrated to cleave phytates [39][37]. Acid phosphatase activity has been observed in Pseudomonas fluorescens [40[38][39],41], Burkholderia cepacia [42][40], Enterobacter aerogenes, Enterobacter cloacae, Citrobacter freundi, Proteus mirabalis and Serratia marcenscens [43][41], and Klebsiella aerogenes [44][42]. Additionally, phytase activity has been demonstrated for Bacillus subtilis, Pseudomonas putida, and Pseudomonas mendocina [45][43]. Interestingly, the secretion of phosphatases by soil bacteria significantly depends on both the free phosphate already available in the soil and the availability of inorganic nitrogen [46,47][44][45], indicating a close relationship between nitrogen fixation and phosphate solubilization processes, and possible synergism of bacterial consortia combining these activities.

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