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Citation: Timofeeva, A.M.;
Galyamova, M.R.; Sedykh, S.E. Plant
Growth-Promoting Soil Bacteria:
Nitrogen Fixation, Phosphate
Solubilization, Siderophore
Production, and Other Biological
Activities. Plants 2023,12, 4074.
https://doi.org/10.3390/
plants12244074
Academic Editors: Loretta Pace,
Christian Dimkpa and Rihab Djebaili
Received: 25 September 2023
Revised: 4 December 2023
Accepted: 4 December 2023
Published: 5 December 2023
Copyright: © 2023 by the authors.
Licensee MDPI, Basel, Switzerland.
This article is an open access article
distributed under the terms and
conditions of the Creative Commons
Attribution (CC BY) license (https://
creativecommons.org/licenses/by/
4.0/).
plants
Review
Plant Growth-Promoting Soil Bacteria: Nitrogen Fixation,
Phosphate Solubilization, Siderophore Production, and Other
Biological Activities
Anna M. Timofeeva 1,2 , Maria R. Galyamova 2and Sergey E. Sedykh 1,2 ,*
1Institute of Chemical Biology and Fundamental Medicine, Siberian Branch of the Russian Academy of
Sciences, 630090 Novosibirsk, Russia; anna.m.timofeeva@gmail.com
2Faculty of Natural Sciences, Novosibirsk State University, 630090 Novosibirsk, Russia;
mgalyamova@gmail.com
*Correspondence: sedyh@niboch.nsc.ru
Abstract:
This review covers the literature data on plant growth-promoting bacteria in soil, which
can fix atmospheric nitrogen, solubilize phosphates, produce and secrete siderophores, and may
exhibit several different behaviors simultaneously. We discuss perspectives for creating bacterial
consortia and introducing them into the soil to increase crop productivity in agrosystems. The
application of rhizosphere bacteria—which are capable of fixing nitrogen, solubilizing organic and
inorganic phosphates, and secreting siderophores, as well as their consortia—has been demonstrated
to meet the objectives of sustainable agriculture, such as increasing soil fertility and crop yields. The
combining of plant growth-promoting bacteria with mineral fertilizers is a crucial trend that allows
for a reduction in fertilizer use and is beneficial for crop production.
Keywords:
plant growth-promoting bacteria; PGPB; soil bacteria; rhizosphere bacteria; phosphate
solubilization; biofertilizers; nitrogen fixation; phosphate fertilizers; siderophores; sustainable
agriculture
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
]. 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
]. Of particular significance is the fact that such bacteria interact with plant
roots and increase resistance to abiotic stresses [11].
This review provides a comprehensive account of the various ways in which soil
bacteria can be used to promote plant growth. We describe the nitrogen-fixing, phosphate-
solubilizing, and siderophore-producing activities of soil microorganisms. Addition-
ally, we discuss the creation of microbial consortia—including combining these with
fertilizers—that
can be introduced into soil to address the current challenges of
sustainable agriculture.
2. Nitrogen-Fixing Bacteria
Bacteria that fix atmospheric nitrogen (N
2
) live in plant tissues (e.g., tubers and roots)
and at the soil–rhizosphere interface, and can supply the significant amounts of mineral
Plants 2023,12, 4074. https://doi.org/10.3390/plants12244074 https://www.mdpi.com/journal/plants
Plants 2023,12, 4074 2 of 16
nitrogen required for plant growth [
12
,
13
]. 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 ni-
trogen [
14
]. 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
–
17
]. Non-symbiotic nitrogen-fixing bacteria that increase the productiv-
ity of cereal crops have been described for the following genera: Azospirillum,Azotobacter,
Beijerinckia,Burkholderia,Clostridium,Gluconacetobacter,Herbaspirillum,Methanosarcina, and
Paenibacillus [15,18,19].
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
]. 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. O
2
can inhibit nitrogenase and suppress N
2
fixation.
Nitrogen-fixing bacteria can avoid the potentially negative effects of O
2
by isolating the
nitrogen fixation in space, e.g., by using structures such as heterocysts, where the oxygen
concentration is kept low [22].
According to several reports, nitrogen-fixing soil bacteria supply a significant amount
of the mineral nitrogen used in agriculture [
23
], 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, N
2
O, and N
2
, which is considered undesirable
for agroecosystems, especially since N
2
O 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].
All known forms of nitrogenase require Fe atoms, with most of them also containing
metals such as Mo or V [
24
]. The nifH gene, encoding nitrogenase reductase [
25
] 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 signif-
icantly 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 syner-
getic 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
] and mycorrhizal fungi [
27
] are known to in-
crease the bioavailability of phosphorus from soil to plants [
28
]. They solubilize inorganic
phosphates and mineralize insoluble organic forms of phosphorus [
29
]. 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:
Plants 2023,12, 4074 3 of 16
Aeromonas,Agrobacterium,Azotobacter,Bacillus,Bradyrhizobium,Burkholderia,Cyanobacteria,
Enterobacter,Erwinia,Kushneria,Micrococcus,Paenibacillus,Pseudomonas,Rhizobium,Rhodococ-
cus,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].
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
].
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
]. 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].
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
], 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], and intracellular phosphorylation [35].
3.2. Mineralization of Organic Phosphorus Compounds
Soil’s organic phosphorus compounds can account for up to 30–50% of soil phospho-
rus. 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
]. 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].
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
]. The phytase enzyme has been demonstrated to
cleave phytates [
39
]. Acid phosphatase activity has been observed in Pseudomonas fluo-
rescens [
40
,
41
], Burkholderia cepacia [
42
], Enterobacter aerogenes,Enterobacter cloacae,Citrobacter
freundi,Proteus mirabalis and Serratia marcenscens [
43
], and Klebsiella aerogenes [
44
]. Addition-
ally, phytase activity has been demonstrated for Bacillus subtilis,Pseudomonas putida, and
Pseudomonas mendocina [
45
]. 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
], indicating a close relationship between nitro-
Plants 2023,12, 4074 4 of 16
gen fixation and phosphate solubilization processes, and possible synergism of bacterial
consortia combining these activities.
4. Siderophore-Secreting Microorganisms
Fe
2+
ions are involved in various biochemical intracellular processes in plants, such
as atmospheric nitrogen fixation (see Section 1) and photosynthesis [
48
]. Although iron is
one of the most common elements in the Earth’s crust, its availability for plant root uptake
is extremely low due to the rapid oxidation of Fe
2+
ions to Fe
3+
ions in the environment,
making them insoluble [49].
Bacteria and other microorganisms are known to secrete siderophores—organic com-
pounds with a molecular mass of up to 1.5 kDa and a high affinity for Fe
3+
[
50
–
52
].
Siderophores secreted by rhizosphere microorganisms promote the conversion of Fe
2+
ions into a form available to plant roots [53,54], favoring plant growth and development.
Siderophore-producing bacteria have been described in twenty genera [
7
], includ-
ing Azospirillum,Azotobacter,Bacillus,Dickeya,Klebsiella,Nocardia,Paenibacillus,Pantoea,
Pseudomonas,Serratia,Streptomyces, and others. A number of genera from this list are
also known to contain atmospheric nitrogen-fixing and phosphate-solubilizing bacteria.
Some bacteria have been reported to exhibit multiple activities that promote plant growth
and development.
It should be noted that siderophores are not secreted only by soil bacteria. They can
also be produced by human pathogenic bacteria [55], fungi [56,57], and oomycetes [58].
4.1. Siderophores Produced by Soil Bacteria
The siderophore structure comprises an iron atom surrounded and coordinated by
oxygen atoms. The octahedral configuration that is most common in bacterial siderophores
contributes to the stabilization of Fe
3+
ions [
59
]. Fe
3+
ions can be coordinated by various
functional structural groups, with the most common being catecholates, hydroxamates,
α
-hydroxycarboxylates, and combinations of nitrogen-containing heterocycles, pheno-
lates, and carboxylates [
60
]. Siderophores are classified by structure and chemical na-
ture as catecholate, hydroxamate, carboxylate, and phenolate siderophores [
61
,
62
]. Some
siderophores are classified as mixed, due to their structure corresponding to two or three
classes simultaneously.
The structure of hydroxamate siderophores includes a functional group C(=O)N-
(OH)R, with R being an amino acid or its derivative. This group contains two oxygen
atoms forming a ligand with Fe
2+
ions [
61
]. Hydroxamate schizokinen siderophores have
been described in Bacillus megaterium [
63
]. The Rhizobium leguminosarum strain has also
been found to produce a schizokinen siderophore [
64
]. Other hydroxamate siderophores
have been described in Pantoea vagans [
65
], Rhizobium meliloti [
66
], R. leguminosarum, and
R. phaseoli [67,68].
Catecholate siderophores contain Fe3+ ions bound to catecholate or hydroxyl groups.
The structure of the resulting complex is also octahedral [
69
]. Catecholate siderophores
are most commonly derived from either 2,3-dihydroxybenzoic acid or salicylic acid [
70
].
Catecholate siderophores have been described in bacteria of the genus Azospirillum, in-
cluding A. brasilense [
71
], A. lipoferum [
72
], and A. vinelandii, which are known to produce
four different catecholate siderophores [
61
,
73
,
74
]. Other siderophores have been described
in Rhizobium leguminosarum [
64
], R. radiobacter (agrobactin) [
75
,
76
], Bacillus subtilis (itoic
acid) [77], and B. thuringiensis (bacillibactin) [78].
Siderophores containing several Fe
2+
chelating groups are categorized as the mixed
type. Pseudomonas strains secreting pyoverdines have been described [
79
,
80
], with their
structure comprising a quinoline chromophore, a peptide, and a dicarboxylic acid or its
amide attached to the chromophore [81].
For various strains of Pseudomonas fluorescens, several pyoverdins [
82
], enantio-
pyochelin [
83
], quinolobactin [
84
], ornichorrugatin, and prepseudomonin have been de-
scribed [
85
]. Pantoea eucalypti has been shown to secrete pyoverdine- and pyochelin-like
Plants 2023,12, 4074 5 of 16
siderophores in the alkaline medium [
86
]. The pyoverdine siderophore azotobactin has
been described in the A. vinelandii strain [87].
It is noteworthy that Fe ions possess a higher affinity for bacterial siderophores com-
pared to fungal siderophores, providing the former with antifungal properties. To date, the
antifungal properties of the pyoverdine of Pseudomonas sp. have been investigated most
thoroughly [
88
]. In summary, not only can pyoverdines favorably affect plant growth, but
they can also exhibit antifungal properties and control relevant phytopathogens [89].
4.2. Life Cycle of Siderophores
Siderophores are synthesized in the cytoplasm and peroxisomes [
49
,
90
]. Next,
siderophore molecules are secreted into the extracellular space. Following the binding of
siderophores to Fe
3+
ions, the complexes of iron ions and siderophores are transported
into the periplasm by specific receptors. This transport mechanism—as opposed to a
concentration gradient—is energy dependent, further confirming that the processes of ATP
synthesis, atmospheric nitrogen fixation, and phosphate solubilization in the bacterial cell
are interrelated.
The availability of iron ions for intracellular processes is due to two mechanisms: the
reduction of Fe
3+
ions to Fe
2+
ions and the dissociation of the iron–siderophore complex,
or the binding of ions to a higher-affinity acceptor [
59
]. Siderophore-interacting proteins,
siderophore reductase, and enzymes that hydrolyze iron–siderophore complexes have
been characterized [
49
]. It is apparent that the reduction of an iron ion in the siderophore
complex is much more advantageous for the cell, allowing the siderophore molecule to be
reused, which is unfeasible when siderophores are hydrolyzed by hydrolases.
Siderophores secreted by rhizosphere bacteria provide iron to plant roots and stimulate
plant growth whenever the bioavailability of iron ions is low. Two mechanisms by which
plants obtain iron ions from siderophores secreted by microorganisms have been described.
The first mechanism involves the transport of siderophore complexes with iron ions to the
apoplast, leading to siderophore reduction and Fe
2+
ion delivery to the root. The second
mechanism allows iron ions to be exchanged between bacterial siderophores and plant
siderophores [91].
5. Isolation and Biochemical Analysis of Soil PGPB
Since it is impractical to conduct
in vivo
experiments with numerous bacterial isolates,
the procedure of soil PGPB analysis is first directed toward the analysis of useful traits.
Thus, PGPB are inoculated into plants, and the strains showing the best results are chosen,
as described in [
92
]. Almost all methods for testing bacterial activity involve the primary
isolation of pure cultures of microorganisms followed by inoculation into different media,
with the corresponding activity assessed by growth or changes in color/transparency
around the colony. Figure 1illustrates the beneficial effects of soil PGPB on the soil’s
biological activities towards promoting plant growth and development.
5.1. Isolation of Nitrogen-Fixing Bacteria
A 10 g soil sample is usually used to isolate soil bacteria. The procedure involves
sample homogenization with 90 mL of sterile water, and using serial dilutions (1:10) up to
10
−6
. One milliliter of the resulting solution is applied to a Petri dish containing nutrient
agar and incubated for 2–5 days at 28
◦
C [
93
]. After incubation, colonies of soil bacteria are
dissolved in sterile saline.
To isolate diazotrophic (nitrogen-fixing) bacteria, diluted soil bacteria samples are
inoculated into nitrogen-free semisolid media (Ashby’s Mannitol Agar or various other
compositions) and incubated for up to seven days at 28
◦
C. After the incubation, samples
in Petri dishes—with the media covered with colorless or colored colonies, plaque, or
film—are considered positive for the presence of nitrogen-fixing bacteria. A single colony
or bacterial biomass is taken from the surface of each culture medium using a sterile
loop and used to inoculate fresh N-free semisolid media of the same type. This step
Plants 2023,12, 4074 6 of 16
is usually repeated two or three times to ensure that the isolates grow in a nitrogen-
free culture medium. At each stage, a microscopic or molecular biological (PCR, 16S
sequencing) control is used to confirm that a pure strain of bacteria is transferred to the next
Petri dish [94].
Plants 2023, 12, x FOR PEER REVIEW 6 of 17
Figure 1. Different soil PGPB influence plant growth and development in various beneficial ways.
These include fixation of atmospheric nitrogen, solubilization of phosphates and potassium, secre-
tion of siderophores and phytohormones, and activity against plant pathogens. Moreover, bacterial
consortia provide cumulative effects, favoring various aspects of plant viability.
5.1. Isolation of Nitrogen-Fixing Bacteria
A 10 g soil sample is usually used to isolate soil bacteria. The procedure involves
sample homogenization with 90 mL of sterile water, and using serial dilutions (1:10) up
to 10−6. One milliliter of the resulting solution is applied to a Petri dish containing nutrient
agar and incubated for 2–5 days at 28 °C [93]. After incubation, colonies of soil bacteria
are dissolved in sterile saline.
To isolate diazotrophic (nitrogen-fixing) bacteria, diluted soil bacteria samples are
inoculated into nitrogen-free semisolid media (Ashby’s Mannitol Agar or various other
compositions) and incubated for up to seven days at 28 °C. After the incubation, samples
in Petri dishes—with the media covered with colorless or colored colonies, plaque, or
film—are considered positive for the presence of nitrogen-fixing bacteria. A single colony
or bacterial biomass is taken from the surface of each culture medium using a sterile loop
and used to inoculate fresh N-free semisolid media of the same type. This step is usually
repeated two or three times to ensure that the isolates grow in a nitrogen-free culture me-
dium. At each stage, a microscopic or molecular biological (PCR, 16S sequencing) control
is used to confirm that a pure strain of bacteria is transferred to the next Petri dish [94].
5.2. Phenotypic Characteristics and Genotyping of Bacteria
Bacterial colonies are characterized by their morphological characteristics, such as
cell and colony shape, color, elevation and opacity, and Gram staining [95]. To identify
the genus (and species) of the strains, sequencing of the 16S rRNA gene is commonly used.
This gene is used due to specific characteristics such as size, ubiquity among bacteria, and
low rate of evolution. Bacterial genomic DNA is isolated [96]. Partial amplification of the
16S rRNA gene for Sanger sequencing is carried out using 27F (5′-AGAGTTT-
GATCCTGGCTCAG-3′) and 1492R (5′-GGTTACCTTGTTACGACTT-3′) primers. Maxi-
mum likelihood phylogenetic reconstruction of 16S rRNA genes allows strain classifica-
tion to the genus or species level.
5.3. Metabolic Characterization of Plant Growth Promotion
Metabolic characterization of a strain, in the sense of biochemical activities associated
with plant growth promotion, involves growing bacteria on Petri dishes or 96-well plates
Figure 1.
Different soil PGPB influence plant growth and development in various beneficial ways.
These include fixation of atmospheric nitrogen, solubilization of phosphates and potassium, secretion
of siderophores and phytohormones, and activity against plant pathogens. Moreover, bacterial
consortia provide cumulative effects, favoring various aspects of plant viability.
5.2. Phenotypic Characteristics and Genotyping of Bacteria
Bacterial colonies are characterized by their morphological characteristics, such as cell
and colony shape, color, elevation and opacity, and Gram staining [
95
]. To identify the genus
(and species) of the strains, sequencing of the 16S rRNA gene is commonly used. This gene
is used due to specific characteristics such as size, ubiquity among bacteria, and low rate of
evolution. Bacterial genomic DNA is isolated [
96
]. Partial amplification of the 16S rRNA
gene for Sanger sequencing is carried out using 27F (5
0
-AGAGTTTGATCCTGGCTCAG-3
0
)
and 1492R (5
0
-GGTTACCTTGTTACGACTT-3
0
) primers. Maximum likelihood phylogenetic
reconstruction of 16S rRNA genes allows strain classification to the genus or species level.
5.3. Metabolic Characterization of Plant Growth Promotion
Metabolic characterization of a strain, in the sense of biochemical activities associated
with plant growth promotion, involves growing bacteria on Petri dishes or 96-well plates
with different media, or assessing the production of bioactive compounds secreted by PGPB
through analytical methods.
5.3.1. Solubilization of Phosphates and Potassium
Phosphate solubilizing activity can be determined by growing bacterial isolates in a
modified agar medium. This medium contains a 2% (w/v) inorganic source of phosphate,
i.e., tricalcium phosphate (Ca
3
(PO
4
)
2
), referred to as Pi. Alternatively, lecithin is used as
the organic phosphate source, and this medium is called Po. The cultivation is conducted
at a temperature of 30
◦
C for seven days. Clear zones forming around bacterial colonies
indicate that specific bacterial isolates are solubilizing phosphate [93,94].
The ability of bacteria to solubilize potassium is assessed with agar containing mica
powder (0.2%) as the single source of potassium. Bacterial cultures that form a clear zone
are considered K solubilizers [97,98].
These methods make it possible to quantify the biochemical characteristics of mi-
croorganisms. The ability of isolates to dissolve phosphorus is assessed by measuring
Plants 2023,12, 4074 7 of 16
the translucent halo around the colony. The phosphate solubilization index (PSI) and
potassium solubilization index (KSI) are determined by calculation, using the equation
in which the diameter of the clear zone is added to the colony diameter and the sum is
divided by the colony diameter [98,99].
5.3.2. Siderophore Production
PGPB isolates are inoculated onto chromazurol S (CAS) agar plates to screen for
siderophore-producing activity. The formation of an orange halo around the bacterial
colony indicates the production of siderophores [
100
]. Solid agar medium CAS can also
be used to qualitatively determine siderophore production. Chromazurol S is a complex
compound containing iron ions. The siderophores are strong Fe-chelators, and the removal
of iron from the complex changes its color from blue to orange.
Based on this method, a quantitative assessment of the concentration of siderophores
in the supernatant can be performed. This can be done by mixing the supernatant with the
CAS reagent (1:1), and, after 20 min, by measuring the optical density at 630 nm [
101
]. The
chromazurol assay does not reveal the type of bacterial siderophores. However, there are
at least three other identification methods. The Arnow test [
102
] allows the presence of
catechol groups in siderophores to be identified. The Csáky assay [103] is used to identify
the presence of hydroxamate-type siderophores. The Shenker test can detect carboxylate
siderophores [104].
5.3.3. Analysis of Phytohormone Production
Auxin, ethylene, abscisic acid, cytokinin, and gibberellin are prominent classes of
phytohormones, with each playing a distinct role in plant growth and development. PGPB
can supply plants with significant amounts of auxin, resulting in modifications to the
development of root systems [
103
,
104
]. These changes occur through the synergistic action
of exogenous and endogenous auxin [
105
]. In addition, enzymes produced by plant
growth-promoting bacteria, such as 1-aminocyclopropane-1-carboxylate (ACC) deaminase,
indirectly contribute to architectural and functional modifications of the root [106].
Among the phytohormones produced by PGPB, auxins and indolyl-3-acetic acid (IAA)
are the most studied [
107
,
108
]. The main pathway of their biosynthesis is carried out
through tryptophan as a precursor [
109
], and a number of papers show the importance
of bacterial IAA in promoting plant growth [
110
]. Several methods are used to determine
IAA. One method is the determination of IAA using gas–liquid chromatography with a
mass-selective detector (emission 360 nm, excitation 282 nm). This method requires the use
of expensive equipment and complex sample preparation. The second method for deter-
mining IAA is the interaction of IAA with Salkovsky’s reagent (2 mL of 0.5 M solution of
FeCl
3
in 100 mL of 37% HClO
4
), which leads to a colored compound. Inoculants are grown
in R2A broth containing 2 mM L-tryptophan, an IAA precursor. The supernatant is mixed
with Salkovsky’s reagent, and the concentration of IAA is assessed spectrophotometrically
via the optical density of the colored product at 530 nm [111–113].
The enzyme 1-aminocyclopropane-1-carboxylate deaminase is responsible for ethylene
synthesis and indirectly contributes to architectural and functional modifications of the
root [
114
]. Quantitative analysis of deaminase activity is based on the ability of microor-
ganisms to assimilate 1-aminocyclopropane-1-carboxylate as the sole nitrogen source [
115
].
Bacteria are spot-inoculated into nitrogen-free saline DF (Dworkin and Foster) media on
plates supplemented with ACC, and incubated at 30
◦
C for 5 days. Growth of isolates on
ACC-supplemented plates demonstrates deaminase activity.
5.4. Analysis of Antagonistic Activity against Phytopathogens and Competition between Strains
A test for antifungal activity is used to analyze the antagonistic activity of bacterial
strains [
116
]. Bacterial strains are evenly distributed over a Petri dish containing a potato
dextrose agar medium. The plates are incubated at 4
◦
C for 2 h to promote the diffusion of
bacteria into the medium, and then a 6 mm diameter fungal disk sample is placed in the
Plants 2023,12, 4074 8 of 16
center of each Petri dish. The plates are incubated under dark conditions at a temperature
of 25
◦
C for a period of seven days. Calculation of the percentage inhibition of radial
growth involves subtracting the Rs value (radius of fungus in the presence of bacteria) from
the Rc value (radius of fungus control) and dividing the remainder by Rc, according to the
formula [
116
]. Inhibition of the growth of the phytopathogen indicates the biocontrol of
the bacterial strain studied.
A cross-test is used to assess antagonistic activity between bacterial strains [
113
]. The
first strain is applied to the agar medium in perpendicular streaks and grown at 30
◦
C for
3 days. The second strain is then applied with strokes at an angle of approximately 90
◦
,
extending outward from the emerging colonies of the first strain. Both strains of bacteria
are incubated at 30
◦
C for another 3 days. Colony lines and zones of inhibition that arise
at the intersection of strains are visualized. Strain compatibility is characterized by the
absence of inhibition zones at the intersection of two colonies. The incompatibility is caused
by competition between bacteria.
5.5. Analysis of Plant Growth Promotion
Sterile plant seeds are germinated and grown under sterile conditions at 22
◦
C with
a photoperiod of 16 h of light and 8 h of darkness [
117
]. Five- to ten-day-old seedlings
are inoculated with a bacterial culture, with uninoculated plants used as controls. After
inoculation, photographs of the plants are taken every two days to determine the length
of the primary root and the number and density of lateral roots (density is the number of
lateral roots or the length of the primary root). The seedlings are weighed and dried at 80
◦
C
in paper bags until a constant weight is reached. Wet and dry biomass are determined.
5.6. Bacterial Genes Promoting Plant Growth
Several bacterial genes are already known to be involved in the beneficial effects
observed in plants, such as (i) genes involved in atmospheric nitrogen fixation (Nif genes,
which encode the nitrogenase complex and other regulatory proteins); (ii) genes responsible
for the formation of legume nodules (nod); (iii) genes controlling pathogens (chi genes,
which produce chitinases, and sfp genes, which produce surfactins); (iv) genes involved in
the production of phytohormones (acdS, which encodes the production of ACC-deaminase,
improving stress resistance by reducing ethylene levels in the plant, and ipdC/ppdC, which
are involved in the production of indoleacetic acid); (v) genes involved in vitamin produc-
tion (pqq, which encodes pyrroloquinoline quinone); and (vi) genes involved in nutrient
mobilization (bgl/ybg genes, which are involved in phosphate solubilization, and rhb genes,
which encode siderophore production).
The nifHDK,nifDK,nifK, and nifD genes predict nitrogen fixation ability in bacterial
genomes [
118
]. Phytase is one of the main enzymes produced by phosphate-solubilizing
bacteria during the mineralization of organic phosphorus. This enzyme releases phos-
phorus from organic materials in the soil, which is stored as phytate [
39
]. Gluconic acid
secretion is the best-characterized phosphate solubilization mechanism, which is medi-
ated by pyrroloquinoline quinone (PQQ)-dependent glucose dehydrogenase (GDH) [
119
].
Analysis of the genes (pqqA,pqqE,pqqAD, and pqqD) encoding the cofactor PQQ is used
as a proxy for phosphate solubilization. Auxin, ethylene, abscisic acid, cytokinin, and gib-
berellin are well-known classes of phytohormones. PGPB can increase plant productivity
by causing changes in plant roots via auxin production, which acts synergistically with
endogenous auxin and alters the development of the plant root system [
120
]. Indole-3-
pyruvate decarboxylase (IPDC) is a key enzyme in synthesizing heteroauxin, the most
important auxin encoded by the ipdC gene.
Specific or universal primer pairs and Sanger sequencing, or NGS in the case of soil
consortia, are used to analyze the genes mentioned above.
Plants 2023,12, 4074 9 of 16
5.7. Environmental Factors That Can Affect PGPB and Increase or Decrease the Synthesis of Plant
Growth-Promoting Substances
Various environmental factors are known to affect the production of plant growth-
promoting substances by PGPB. These factors include interaction with other microorgan-
isms in the soil, climate zone soil types, soil physicochemical properties, and environmental
conditions [
32
]. For example, PGPB in soils exposed to extreme environmental conditions,
such as saline–alkaline soils, soils with high nutrient deficiencies, or soils from extreme
temperature environments, tend to solubilize more phosphate and potassium than bacteria
in soils from more moderate conditions [28].
The PGPB activity is also affected by soil composition. The growth rate of microorgan-
isms was found to be related to the concentration of soluble phosphate [
121
]. Additionally,
the growth rate of the Pseudomonas aeruginosa strain was estimated to be 25 times greater
under phosphate excess than under phosphate deficiency [
122
]. The PGPB-mediated min-
eral phosphate solubilization activity was found to be inhibited by soluble phosphate via
a negative feedback mechanism [
123
]. In this way, the phosphate-solubilizing activity of
bacteria is induced by low levels of exogenous soluble phosphate and inhibited by high
levels of exogenous soluble phosphate [33].
Various abiotic stresses can result in higher production of various growth-promoting
factors. For example, drought and/or salt stress can increase the sensitivity of many plants
to various phytopathogens, frequently by reducing the ability of the plant to effectively
attack the pathogen. Under unfavorable conditions, PGPB were found to increase the secre-
tion of the phytohormones abscisic acid, salicylic acid, and ethylene, which are responsible
for activating the signaling cascade of various genes involved in salt tolerance [124].
Figure 2provides a schematic representation of the environmental factors that affect
PGPB and the secretion of substances that enhance plant growth.
Plants 2023, 12, x FOR PEER REVIEW 9 of 17
The nifHDK, nifDK, nifK, and nifD genes predict nitrogen fixation ability in bacterial
genomes [118]. Phytase is one of the main enzymes produced by phosphate-solubilizing
bacteria during the mineralization of organic phosphorus. This enzyme releases phospho-
rus from organic materials in the soil, which is stored as phytate [39]. Gluconic acid secre-
tion is the best-characterized phosphate solubilization mechanism, which is mediated by
pyrroloquinoline quinone (PQQ)-dependent glucose dehydrogenase (GDH) [119]. Anal-
ysis of the genes (pqqA, pqqE, pqqAD, and pqqD) encoding the cofactor PQQ is used as a
proxy for phosphate solubilization. Auxin, ethylene, abscisic acid, cytokinin, and gibber-
ellin are well-known classes of phytohormones. PGPB can increase plant productivity by
causing changes in plant roots via auxin production, which acts synergistically with en-
dogenous auxin and alters the development of the plant root system [120]. Indole-3-py-
ruvate decarboxylase (IPDC) is a key enzyme in synthesizing heteroauxin, the most im-
portant auxin encoded by the ipdC gene.
Specific or universal primer pairs and Sanger sequencing, or NGS in the case of soil
consortia, are used to analyze the genes mentioned above.
5.7. Environmental Factors That Can Affect PGPB and Increase or Decrease the Synthesis of
Plant Growth-Promoting Substances
Various environmental factors are known to affect the production of plant growth-
promoting substances by PGPB. These factors include interaction with other microorgan-
isms in the soil, climate zone soil types, soil physicochemical properties, and environmen-
tal conditions [32]. For example, PGPB in soils exposed to extreme environmental condi-
tions, such as saline–alkaline soils, soils with high nutrient deficiencies, or soils from ex-
treme temperature environments, tend to solubilize more phosphate and potassium than
bacteria in soils from more moderate conditions [28].
The PGPB activity is also affected by soil composition. The growth rate of microor-
ganisms was found to be related to the concentration of soluble phosphate [121]. Addi-
tionally, the growth rate of the Pseudomonas aeruginosa strain was estimated to be 25 times
greater under phosphate excess than under phosphate deficiency [122]. The PGPB-medi-
ated mineral phosphate solubilization activity was found to be inhibited by soluble phos-
phate via a negative feedback mechanism [123]. In this way, the phosphate-solubilizing
activity of bacteria is induced by low levels of exogenous soluble phosphate and inhibited
by high levels of exogenous soluble phosphate [33].
Various abiotic stresses can result in higher production of various growth-promoting
factors. For example, drought and/or salt stress can increase the sensitivity of many plants
to various phytopathogens, frequently by reducing the ability of the plant to effectively
attack the pathogen. Under unfavorable conditions, PGPB were found to increase the se-
cretion of the phytohormones abscisic acid, salicylic acid, and ethylene, which are respon-
sible for activating the signaling cascade of various genes involved in salt tolerance [124].
Figure 2 provides a schematic representation of the environmental factors that affect
PGPB and the secretion of substances that enhance plant growth.
Figure 2.
Environmental factors that affect the secretion of plant growth-favoring substances by
soil bacteria.
6. Consortia of Soil PGPB
The soil microbiome is a complex community of millions of species with billions of
possible interactions between them. Given that no soil bacterial species exist in isolation,
these interactions result in new properties that are not characteristic of individual genera,
species, and/or strains of bacteria [
5
]. Consortia formed through the interaction of several
bacteria are promising for agricultural applications [
125
,
126
] compared to single-species
inoculants [
127
]. However, it is essential for the species within a consortium not to be
antagonistic to each other, and to be able to occupy a wider range of ecological niches
than they would if they were isolated [
128
]. On the one hand, a more diverse microbial
consortium may provide a greater number of functions beneficial to plants [
129
]. On the
other hand, some strains of PGPB may simultaneously exhibit several activities favorable to
plant growth. For example, several publications report that nitrogen-fixing bacteria exhibit
phosphate-solubilizing and other activities. Alternatively, it is not known how actively a
single bacterial strain can simultaneously exhibit several traits favorable for plant growth
Plants 2023,12, 4074 10 of 16
and development. Whatever the case, the application of microbial consortia can provide
several plant-beneficial functions to the soil, to be performed simultaneously by different
consortium members due to their mutual complementarity.
The application of a mixture of Bacillus,Pseudomonas, and Streptomyces isolated from
soil and exhibiting phosphate-solubilizing activity has been shown to provide better re-
sults in accelerating the linear growth and root growth of plants compared to the use of
individual strains. Another example is the inoculation of wheat seeds with Pseudomonas
fluorescens Ms-01 and Azosprillum brasilense DSM1690 bacteria, which solubilize phosphates
and secrete auxins that strongly increase root and shoot biomass compared to the appli-
cation of the strains separately [
130
]. The consortium of Bacillus firmus,Cellulosimicrobium
cellulans, and Pseudomonas aeruginosa has been demonstrated to increase the root length
and linear growth of amaranth plants more effectively than when applying the strains one
by one or in pairs [
131
]. In recent years, an increasing number of scientific papers have
focused on the application of bacterial consortia with a positive effect on plant growth and
development, corroborating their unequivocal relevance and significance.
Combined Application of Bacteria and Phosphate Fertilizers
The coapplication of phosphate-solubilizing bacteria and some phosphate fertilizers
has been demonstrated to produce a synergistic effect and increase agronomic efficiency,
such as when using phosphorites (rock phosphates) [
132
–
134
]. Inoculation with phosphate-
solubilizing bacteria has been found to significantly improve corn growth when applied
with various inorganic and organic fertilizers: manure, poultry manure, superphosphate,
and phosphate [
135
]. Inoculating wheat plants with Pseudomonas sp. or Enterobacter
sp. and applying diammonium phosphate has been proven effective [
131
]. Enterobacter
sp. has been reported to increase phosphorite solubilization from 17.5% [
136
] to 27%
compared to the release from phosphorites (4%) alone [
137
]. A combination of a one-time
inoculation of wheat plants with five different strains of Pseudomonas (P. plecoglossicida,
P. reinekei,P. koreensis,P. japonica, and P. frederiksbergensis) and phosphate application was
found to increase phosphate availability, nutrient availability, and chlorophyll content,
and to improve the morphological characteristics associated with a higher phosphorus
uptake [
138
]. A consortium of three strains, P. corrugata,P. koreensis, and P. frederiksbergensis,
was found to enhance the plant growth of alfalfa (M. truncatula) when coapplied with
phosphate fertilizers [139].
Phosphate-solubilizing soil bacteria are known not only to increase the efficiency
of mineral phosphate fertilizers, but also to have beneficial effects when applied with
organic fertilizers. For example, the application of a mixture of compost (biogas production
residues) coupled with fossil phosphate-solubilizing bacteria Bacillus sp. was reported to
enhance the availability of free phosphate in soil, increase the soil’s organic matter content,
and boost the population of phosphate-solubilizing bacteria [140].
To summarize, the inoculation of crops with phosphate-solubilizing bacteria combined
with mineral or organic fertilizers is a promising integrated strategy for increasing soluble
phosphate availability, improving the agronomic efficiency of phosphate fertilizer usage,
increasing soil fertility, and achieving sustainable agriculture goals.
7. Conclusions
Recent studies have shown that the application of PGPB as a biofertilizer is of great
importance for the sustainable management of soil resources. The quality and nutritional
value of agricultural products are of great significance to consumers. Further research in
this area is necessary to provide farmers with timely information on the biological activ-
ity of PGPB. Atmospheric nitrogen fixation, phosphate solubilization, and increased iron
bioavailability in soil due to soil bacteria all contribute to sustainable agricultural develop-
ment, particularly by increasing soil fertility and crop yields. The usage of soil bacteria and
their consortia for inoculation into plant seeds, as well as for coapplication with mineral fer-
tilizers, may eventually contribute to developing a new generation of farming technologies
Plants 2023,12, 4074 11 of 16
with lower costs and reduced negative effects on the environment. Analyzing the molecular
mechanisms of nitrogen fixation, phosphate solubilization, and siderophore synthesis,
as well as identifying bacterial strains that can simultaneously exhibit several different
activities, are necessary steps to create commercial bacterial preparations for enhancing
plant growth in crops. One area that demands special consideration is the experimental
testing of both individual strains and their consortia across various climatic zones, diverse
soil types, and different crops. The authors of this review find such experimental research
highly relevant due to the potential ineffectiveness of commercial preparations.
Author Contributions:
Conceptualization, A.M.T., M.R.G. and S.E.S.; writing—original draft prepa-
ration, A.M.T.; writing—review and editing, S.E.S.; visualization, A.M.T.; funding acquisition, S.E.S.
All authors have read and agreed to the published version of the manuscript.
Funding:
This work was supported by the Ministry of Science and Higher Education of the Russian
Federation, agreement No. 075-15-2021-1085.
Data Availability Statement: Not applicable.
Conflicts of Interest: The authors declare no conflict of interest.
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