biology

Review
Utilization of Microbial Consortia as Biofertilizers and
Biopesticides for the Production of Feasible Agricultural
Product
Renganathan Seenivasagan and Olubukola Oluranti Babalola *

Food Security and Safety Niche Area, Faculty of Natural and Agricultural Sciences, North-West University,
Mmabatho 2735, South Africa
* Correspondence: olubukola.babalola@nwu.ac.za; Tel.: +27-1-8389-2568; Fax: +27-1-8389-2134

Simple Summary: Recently in agriculture, the usage of chemical pesticides and fertilizers has
increased tremendously. Additionally, it shows severe effects on human health, ecosystem, and
groundwater. Environment-friendly methods are used to improve soil fertility, pests, and disease
control. Biopesticide and biofertilizers have the future to upgrade sustainable agriculture for many
years. This review highlights the efficacy of biofertilizers and biopesticides in improving crop
yielding. It provides an eco-friendly and cost-effective method to get more yield for farmers. It
describes the prominence of microbial inoculants in plant cultivation.

Abstract: Farmers are now facing a reduction in agricultural crop yield, due to the infertility of
soils and poor farming. The application of chemical fertilizers distresses soil fertility and also





 human health. Inappropriate use of chemical fertilizer leads to the rapid decline in production
levels in most parts of the world, and hence requires the necessary standards of good cultivation
Citation: Seenivasagan, R.;
practice. Biofertilizers and biopesticides have been used in recent years by farmers worldwide to
Babalola, O.O. Utilization of
preserve natural soil conditions. Biofertilizer, a replacement for chemical fertilizer, is cost-effective
Microbial Consortia as Biofertilizers
and Biopesticides for the Production
and prevents environmental contamination to the atmosphere, and is a source of renewable energy.
of Feasible Agricultural Product. In contrast to chemical fertilizers, biofertilizers are cost-effective and a source of renewable energy
Biology 2021, 10, 1111. https:// that preserves long-term soil fertility. The use of biofertilizers is, therefore, inevitable to increase
doi.org/10.3390/biology10111111 the earth’s productivity. A low-input scheme is feasible to achieve farm sustainability through the
use of biological and organic fertilizers. This study investigates the use of microbial inoculants as
Academic Editors: Ana Alexandre biofertilizers to increase crop production.
and Kathrin Wippel

Keywords: bioinoculant; biopesticides; PGPR; microbial inoculants; organic farming; yield component
Received: 8 September 2021
Accepted: 12 October 2021
Published: 28 October 2021

1. Introduction
Publisher’s Note: MDPI stays neutral
Chemical fertilizers and pesticide dependence in conventional agriculture have in-
with regard to jurisdictional claims in
published maps and institutional affil-
creased, due to the significant growth of the human population and food demands [1].
iations.
Plant nutrition plays a major role in the increased demand for food supply. An increase
in crop production has made it possible through the use of commercial artificial fertiliz-
ers. Phosphorus, nitrogen, and potassium fertilizer have frequently increased for crop
production and agricultural systems with low cost [2]. Soil quality deterioration reversed
biodiversity, and increased water and air pollution, and human health has also created
Copyright: © 2021 by the authors.
excess use of chemical fertilizer [3]. The agriculture ecosystem, soil fertility, and cultivated
Licensee MDPI, Basel, Switzerland.
crop growth get affected, due to excessive usage of chemical pesticides [4]. To overcome
This article is an open access article
distributed under the terms and
such drawbacks, a biofertilizer, a biological agent, is used for convalescing this problem.
conditions of the Creative Commons
The loss of topsoil, soil infertility, plant growth reduction, reduced yield index, and gradual
Attribution (CC BY) license (https:// decrease of indigenous microbial diversity could be managed by microbial inoculants using
creativecommons.org/licenses/by/ agricultural practice. Pesticides and chemical fertilizers create environmental issues that
4.0/).

Biology 2021, 10, 1111. https://doi.org/10.3390/biology10111111 https://www.mdpi.com/journal/biology

Biology 2021, 10, 1111 2 of 22

microbial inoculants can comfortably overcome, which serves as a potential alternative

and psychostimulants [5,6].
For a healthy environment, the management of integrated nutrient systems and sus-
tained agricultural productivity is greatly influenced by microbial inoculants [7]. Microbial
inoculants or biofertilizers contain living microorganisms that colonize the rhizosphere
and helps in the promotion of plant growth. The converts the insoluble elements in the
soil to a soluble form by a biological process similar to rock phosphate solubilization
and nitrogen fixation [8]. Beneficial microorganisms utilized in biofertilizers improve
microflora, soil health, plant growth, plant disease control, and protect the plant from
pests [9]. There are beneficial microbial inoculants, such as nitrogen fixer, phosphate,
sulfur, zinc solubilizer (VAM), and plant growth-promoting rhizobacteria, in biofertilizers.
Plant growth-promoting rhizobacteria are bacteria that live freely on rhizosphere soil and
promote plant growth. They also acts as biopesticides, based upon the ability or behavior
of the crops and biocontrol agents (Nitrogen fixer, PSB, and SSB) [10].
‘Biopesticide’ implies the use of beneficial microorganisms to control the insects.
However, the major constraint is the availability of biopesticides relative to the total
cropped area. Specific pesticides, derived from natural materials, act as biopesticides, such
as plants, animals, bacteria, and certain minerals [11]. Biopesticides are classified into 3
major categories: biochemical, plant, and microbial pesticides. All over the world, there
are 90% of all biopesticides utilized. The most commercially successful biopesticide in
the market is Bacillus thuringiensis (Bt) [12]. Modern agriculture requires biopesticide and
biofertilizers, due to the demand for safe and residue-free crop production [3]. Therefore,
to cater to the need, it is necessary that government, and nongovernment organizations
should promote entrepreneurs for biofertilizers and biopesticides production.
The objective of this review is the improvement of plant growth and yield through
various microbes, such as bacterial, fungal, virus, and algae inoculants as biofertilizer
(nitrogen fixers, phosphate solubilizer (PSB), sulfur solubilizer, PGPR, VAM, and Azolla),
PGPR (phosphate solubilizer, N2 fixers, phytohormones, siderophores, and antibiotics) and
biopesticides (microbial, plant incorporated protection, and biochemical).

2. Biofertilizer
Microbial inoculants or biofertilizers are preparation containing viable algae, fungi,
and bacteria alone or consortium together to support the plant growth and increase crop
yield [13]. Biofertilizers contain beneficial microbes that improve soil chemical and bio-
logical characteristics by fixing nitrogen, cellulolytic activity, or phosphate. When they
are applied to seed, plant surfaces, root, or soil, they inhabit the rhizosphere, and through
their biological activity, they enhance nutrient bioavailability, promote plant’s growth,
and increase the soil microflora. Thereby, they are preparations that readily improve
the fertility of the soil [14,15]. Rhizobium has symbiotic associations with legume roots,
such as rhizobacteria, that reside on the surface of the root or in the soil of the rhizo-
sphere. Broad-spectrum biofertilizers include Blue-Green Algae (BGA), Rhizobium, and
Azolla are crop-specific bio inoculants, such as Azospirillum, Azotobacter, phosphorus
solubilizing bacteria (PSB), vesicular-arbuscular mycorrhiza (VAM), and Anabaena, as
nitrogen-fixing cyanobacteria [15,16]. These bacteria are known as biofertilizers and plant
growth-promoting rhizobacteria (PGPR). Competition mechanisms and antagonism ac-
tivity are carried out by the enzymatic activity of PGPR for crop production, such as the
inhibition of phytohormones and phytoparasites; it also helps plants in withstanding stress
by heavy metal contaminations and pollutants [17,18].
Biofertilizers are eco-friendly, cost-effective, and can be produced in bulk on the farm
itself if necessary. The crop yield is increased by 10–40% and up to 50 percent of nitrogen
is fixed. The continuous application of biofertilizer of the land for 3–4 years can retain
fertility, due to the efficiency of parental inoculums, which could maintain the growth and
multiplication of plants effectively. They improve soil texture, pH, and other properties [19].
Biology 2021, 10, x 3 of 23

Biology 2021, 10, 1111 3 of 22

multiplication of plants effectively. They improve soil texture, pH, and other properties
[19].
Biofertilizers are
Biofertilizers are renewable
renewablesources
sourcesofofplant
plantnutrients
nutrientscomplementing
complementingchemical
chemicalfertil-
fer-
izers at a low cost. In comparison to chemical fertilizers, biofertilizers are environmentally
tilizers at a low cost. In comparison to chemical fertilizers, biofertilizers are environmen-
friendly; can be produced from natural sources, prevented from damage but also helps in
tally friendly; can be produced from natural sources, prevented from damage but also
building up healthy soil, and to some extent, plants are cleansed from chemical fertilizers
helps in building up healthy soil, and to some extent, plants are cleansed from chemical
that are precipitated [20]. Considering biofertilizer as a modern tool for agriculture, its use
fertilizers that are precipitated [20]. Considering biofertilizer as a modern tool for agricul-
is vital as components of integrated nutrient management, reduction in the usage of haz-
ture, its use is vital as components of integrated nutrient management, reduction in the
ardous chemicals, cost-effective, and source of renewable energy for plants in sustainable
usage of hazardous chemicals, cost-effective, and source of renewable energy for plants
agriculture [21] (Figure 1 and Table 1).
in sustainable agriculture [21] (Figure 1 and Table 1).

Figure
Figure 1.
1. PGPR
PGPR classification
classification and
and involving microorganisms.
involved microorganisms.

Table
Table 1. Microbial 1. Microbial
inoculants inoculants
used as usedPlant
biofertilizers, as biofertilizer, PGPR, and
Growth Promoting Biopesticides.
Rhizobacteria, and Biopesticides.

Biofertilizer PGPR Biopesticide Refer-

References
Biofertilizer PGPR Biopesticide
Rhizobium, Azotobacter, Acetobacter, Aeromonas hydrophila, Azotobacter, Bacillus thuringiensis, B.
ence
Rhizobium, Azotobacter,
Azospirillum brasilense, Azospirillum Acetobacter, Aeromonas
Achromobacter, Alcaligenes, Anabaena, hydrophila, Bacillus thuringiensis, B. thuringiensis
thuringiensis var. kurstaki (Bt), B.
Azospirillum
brasilense, lipoferum, lipoferum,
Azospirillum Arthrobacter, Azoarcus,
Azotobacter, Azospirillum brasilense,
Achromobacter, Alcali- var. thuringiensis var. israelensis
kurstaki (Bt), (Bt), B. var.
B. thuringiensis
Azotobacter chroococcum,
Azotobacter chroococcum, Acetobacter A. irakense,
genes,A. lipoferum, Arthrobacter,
Anabaena, Azotobacter, Azoar- israelensis
thuringiensis var.
(Bt), B.tenebrionis,
thuringiensisB. var.
Acetobacter diazotrophicus, Acinetobacter calcoaceticus, A. baumannii, thuringiensis var. aizawai, B.
diazotrophicus, Bacillus licheniformis,
Bacillus licheniformis, B.
cus, Azospirillum brasilense, A. ira-
Bacillus polymyxa, Beijerinckia, Burkholderia
tenebrionis, B. thuringiensis var. aiza-
thuringiensis japonensis, B. popilliae,
B.megaterium,
megaterium, B. mucilagenosus,gladioli,
B. mucilagenosus, B. kense, A. lipoferum,
Burkholderia cepacia, Clostridium,Aci- wai,
Azotobacter, B. thuringiensis
B. lentimorbus, japonensis,
B. sphaericus, B. B.
edaphicus, B. B.
B. edaphicus, subtilis,
subtilis,Actinomyces, netobacter
Derxia, calcoaceticus,
Enterobacter, Erwinia spp.,A. Ewingella
baumannii, popilliae,
pumilus, B.
B. lentimorbus, B. sphaericus, [22–25]
subtilis, B. firmus,
Actinomyces, Streptomyces,
Streptomyces, americana,
Herbaspirillum serope- Escherichia
Bacillus polymyxa,vulneris, Flavobacterium, B.Burkholderia
Beijerinckia, pumilus, B.cepacia, B. B. firmus,
subtilis,
Herbaspirillum seropedicae, Frankia, Gluconacetobacter, Klebsiella, amyloliquefaciens, B. licheniformis, [22–25]
dicae, Rhizobium phaseoli, Thiobacil- Burkholderia gladioli, Burkholderia ce- Burkholderia cepacia, B. amyloliquefa-
Rhizobium phaseoli, Thiobacillus Mycobacterium phlei, Proteus penneri, Erwinia amylovora, Pasteuria
lus thioxidans,
thioxidans, Glomus
Glomus fasciculatum,
fasciculatum, pacia, Clostridium,
Pseudomonas fluorescens, P.Derxia,
luteola, Enterobac-
P. ciens, B. licheniformis,
penetrans, Erwinia amylo-
Pasteuria usage,
Blue
BlueGreen Algae(BGA),
Green Algae (BGA), and Azolla. ter, Erwinia
alcaligenes, P. putida,spp., Ewingella
Rhizobium ameri-
leguminosarum, vora, Pasteuriaspp.,
Pseudomonas penetrans, Pasteuria
Streptomyces
and Azolla. Rahnella aquatilis,
cana, Serratiavulneris,
Escherichia plymuthica, S. ficaria, usage,
Flavobacte- griseoviridis, and Xanthomonas
Pseudomonas spp., Streptomy-
Sinorhizobium, Shigella
rium, Frankia, spp., Vibrio fluvialis,
Gluconacetobacter, campestris
ces pv. poannua,
griseoviridis, and Xanthomonas
and Zoogloea
Klebsiella, Mycobacterium phlei, Pro- campestris pv. poannua,
teus penneri, Pseudomonas fluorescens,
Biology 2021, 10, 1111 4 of 22

2.1. Nitrogen Fixers

Nitrogen fixation is a dynamic and high-energy demanding process [26]. Elemen-
tal nitrogen conversion by biological nitrogen fixation is one way of converting into a
plant’s usable form. Organic compounds are transformed into inert atmospheric N2 by
nitrogen-fixing bacteria [27]. In biofertilizers, nitrogen fixers or N2 fixing species are used as
fertilizers containing living microbial inoculants or microorganism classes. Microbial inocu-
lants, such as Azotobacter, Rhizobium, Blue-Green Algae (BGA), Azospirillum, and Azolla,
are used as biofertilizers, which help in nitrogen fixation by converting atmospheric nitro-
gen to plant useable form. Legume plants have root nodules inhabiting bacteria belonging
to the genera Sinorhizobium, Azorhizobium, Rhizobium, Bradyrhizobium, and Mesorhizobium,
collectively called rhizobia [22]. When rhizobial culture is inoculated in the field, rhizobial
symbiosis occurs, increasing the yield of pulse crops up to 15–20 kg N/ha by rhizobium,
and crop yield is increased by up to 20% [28].
By nature, Azotobacter has a major role in the nitrogen cycle as it has a range of
metabolic capabilities [29]. Along with nitrogen-fixing, Azotobacter also produces vita-
mins, such as riboflavin and thiamine [30], indole acetic acid (IAA), cytokinins (CK), and
Gibberellins (GA), via plant hormones [31]. Atmospheric nitrogen is fixed and supplied
as ammonium by Azotobacter chroococcum. Therefore changing over of ammonium ions
improves plant development by root architecture advancing and seed germination enhance-
ment [32]. Azotobacter is also used to kill pathogenic microorganisms surrounding crop
plant root systems [33]. Azospirillum is another aerobic, free-living, motile, gram-negative
bacterium that can thrive under flooding conditions [34], supporting various aspects
of plant growth and development [35]. Infield trials and greenhouse experiments with
Azospirillum species, such as Azospirillum, including A. irakense, A. lipoferum, A. halopraef-
erens, A. amazonense, and A. brasilense, shows improved crop yield and plant growth [34]
(Table 2). Plants inoculated with Azospirillum showed higher water and mineral uptake
leads to better yield [22]. Hungria et al. [36] reported that Azospirillum brasilense is compe-
tent enough to promote the growth of plants by fixation of nitrogen, which helps to save
money.
For the global nitrogen cycle, cyanobacteria are very necessary for significant N2
fixers on earth [46]. Cyanobacteria, mostly used as nitrogen-fixing biofertilizers, includes
Scytonema, Tolypothrix, Plectonema, Aulosira, Anabaena, and Nostoc [47,48]. Along with
releasing growth-promoting substances, Cylindrospermum musicola also releases vitamins
and nitrogen. In rice plants, it also improves root growth and yield [49]. Crop plants
inoculated with Rhizobium sp. showed a substantial increase in growth and yield, through
a high number of root nodules, compared to uninoculated plants [50].

2.2. Phosphate Solubilizing Microorganisms

Plant growth and metabolism processes are mainly affected by the nutrient nitrogen
followed by phosphate [51]. In virtually all major metabolic processes, such as respiration,
photosynthesis, energy accumulation, and transfer, signal transduction, cell enlargement,
cell division, and macromolecular biosynthesis, they play an important role. Phosphate
contributes to the resistance to disease and helps to survive winter rigors in plants [52,53].
As it is present in the form of insoluble phosphates, approximately 95–99 percent of
soil phosphorous is unusable for plants [54]. The P-solubilizing potential of microbial
inoculants (biofertilizers) is used as an environmentally safe alternative to further chemical-
based P fertilizer applications in agricultural soil [55]. Phosphorous can be solubilized by
many microorganisms, including bacteria, fungi, actinomycetes, and even algae, such as
Cyanobacteria and Mycorrhiza [1,56].
The most popular inoculants for phosphorus solubilizing bacteria (PSB) belong to the
genera Pseudomonas spp. and Bacillus [57,58]. Other bacteria identified include Serratia,
Rhodococcus, Chryseobacterium, Phyllobacterium, Arthrobacter, Delftia sp., Gordonia, [37],
Xanthomonas [38], Azotobacter [39], Enterobacter, Pantoea, Klebsiella [40,41], Vibrio proteolyticus[42],
Beijerinckia, Burkholderia, Erwinia, Flavobacterium, Microbacterium and Rhizobium [35],
Biology 2021, 10, 1111 5 of 22

Xanthobacter agilis [43]. By releasing complexing or mineral dissolving compounds, such as

(i) organic acid anions, protons, siderophores, CO2 , and hydroxyl ions; (ii) extracellular en-
zyme release; and (iii) substrate degradation and P release, the soil microorganism employs
P-solubilization mechanisms [59]. Organic acids are low molecular weight, such as citric
and gluconic acids, which are synthesized by PSB during inorganic P solubilization [60].
The phosphate with the chelating cations of carboxyl and hydroxyl groups binds with
organic acids, thereby releasing soluble phosphate and inducing soil acidification [61].
Heavy metal immobilization is performed by phosphate fertilizers. Microorganisms and
plants solubilize insoluble phosphate compounds using their phosphatase enzyme and
organic acids [62,63].

Table 2. Microbial inoculants in phosphate, sulphate, zinc solubilizer and nitrate, siderophore producers are used as biofertilizer.

Types Bacteria Fungi/VAM Actinomycetes Cyanobacteria/Yeast References

Alcaligenes sp., Aerobacter aerogenes, Aspergillus awamori, A. niger, A. terreus, Actinomyces Anabaena sp.,
Achromobacter sp., Actinomadura A. flavus, A. nidulans, A. foetidus, A. sp. and Calothrix braunii,
oligospora, Agrobacterium sp., wentii, Fusarium oxysporum, Alternaria Streptomyces Nostoc sp., and
Azospirillum brasilense, Bacillus teneius, Achrothcium sp., Penicillium sp. Scytonema sp.,
circulans, B.cereus, B.fusiformis, B. digitatum, P. lilacinium, P. balaji, P.
pumilus, B. megaterium, B. mycoides, B. funicolosum, Cephalosporium sp.,
polymyxa, B. coagulans, B.chitinolyticus, Cladosprium sp., Curvularia lunata,
B. subtilis, Bradyrhizobium sp., Cunnighamella, Candida sp., Chaetomium
Brevibacterium sp., Citrobacter sp., globosum, Humicolainslens, H. lanuginosa,
PSM * Pseudomonas putida, P. striata, P. Helminthosporium sp.,
fluorescens, P. calcis, P. corrugate, Paecilomycesfusisporous, Pythium sp.,
Flavobacterium sp., Nitrosomonas sp., Phoma sp., Populosporamytilina,
Erwinia sp., Micrococcus sp., Myrotheciumroridum, Morteirella sp.,
Escherichia intermedia, Enterobacter Micromonospora sp., Oideodendron sp.,
asburiae, Serratia phosphoticum, Rhizoctonia solani, Rhizopus sp., Mucor
Nitrobacter sp., Thiobacillus ferroxidans, sp., Trichoderma viridae, Torula
T. thioxidans, Rhizobium meliloti, and thermophila, Schwanniomyces occidentalis,
Xanthomonas sp. and Sclerotium rolfsii.
Glomus fasciculatum (VAM)
Acidothiobacillus, Thiomicrospira, Aureobasidium, Epicoccum, Penicillium,
Thiosphaera, Paracoccus, Xanthobacter, Aspergillus, Alternariatenuis,
Alcaligenes, Pseudomonas, Thiobacillus Aureobasidiumpullulans,
SSM * thiooxidans, T. ferrooxidans, T. thioparus, Epicoccumnigrum,
T. denitrificans, and T. novellus Scolecobasidiumconstrictum, and [22,34,35,37–45]
Myrotheciumcinctum
Azospirillum lipoferum, A. brasilense, Acidothermus Cylindrospermum
Azoarcus, Azotobacter chroococcum, A. cellulolyticus musicola and
peroxydans, A. nitrogenifigens, Anabaena azollae
Rhizobium, Bradyrhizobium,
Sinorhizobium, Azorhizobium,
NO3 * Mesorhizobium, H. seropedicae, H.
rubrisubalbicans Burkholderia sp.,
Rhizobium leguminosarum bv. trifolii, B.
vietnamiensis,
Gluconacetobacterkombuchae, G.
johannae, G. azotocaptans, G.
diazotrophicus, and Swaminathania
salitolerans
Bacillus sp., Ochrobactrum, Kluyvera Aspergillus nidulans, A. versicolor, Nocardia Saccharomyces
ascorbata, Salmonella, Enterobacter, Penicillium chrysogenum, P. citrinum, asteroids, cerevisiae (Yeast)
Yersinia, Mycobacterium, B. megaterium, Mucor, Rhizopus, Trametes versicolor, Streptomyces
Ochrobactrum anthropi, Proteus vulgaris, Ustilago sphaerogina, Debaromyces sp., griseus, and
Siderophore Pseudomonas fluorescence, P. putida, and Rhodotorula minuta Actinomadura
Escherichia coli, Salmonella, Klebsiella madurae
pneumoniae, Vibrio cholerae, V.
anguillarum, Aeromonas, Aerobacter
aerogenes, Yersinia, and Mycobacterium
Bacillus subtilis, Gluconacetobacter Aspergillus niger and Penicillium luteum Saccharomyces sp.
ZSB * diazotrophicus, Thiobacillus thioxidans, (Yeast)
and T. ferroxidans
* PMS—Phosphate Solubilizing Microorganism, SSM—Sulphte Solubilizing Microorganism, ZSB—Zinc Solubilizing Microorganism.

Phosphate solubilizing and stress-tolerant bacteria Burkholderia vietnamiensis pro-

duces gluconic acids, and 2-ketogluconic, which is involved in solubilizing phosphate [62].
Tomar et al. [64] reported that black gram (Vigna mungo) and lentil (Lens esculentus) inoc-
ulated with B. firmus, a phosphate solubilizing bacteria showed significant results in the
increase of seed yield. Chabot et al. [65] described that the inoculation of P-solubilizing
Rhizobium leguminosarum leads to the growth of maize and lettuce. Some fungi, such as
Biology 2021, 10, 1111 6 of 22

Penicillium and Aspergillus, act as phosphorus solubilizers [53]. Mittal et al. [66] isolated
six P-solubilizing fungi, four strains of Penicillium citrinum, and two strains of A. awamori,
from the rhizosphere of various crops. A. awamori showed shoot height increase of 7–12%,
seed number increase to three-fold, and increase in seed weight to two-fold, in comparison
to uninoculated plants. Hajra et al. [67] reported that mycorrhizal plants had increased
plant height and leaf area, in comparison to non-mycorrhizal plants, also showed a sharp
decrease of nematode infection in plants (Table 2).

2.3. Potassium Solubilizing Microorganisms

Potassium is the third important plant growth nutrient that plays a vital role in plant
metabolism, growth, and development. The plants would have poorly formed roots, grow
slowly, produce small seeds and have lower yields without a sufficient supply of potas-
sium [68] and increased vulnerability to diseases [69] and pests [70]. Potassium solubilizing
microbes produce organic acids that can solubilize potassium rock [71]. Rhizosphere soil
microbial inoculants, including Aspergillus, Bacillus sp., Clostridium, Burkholderia, Acidoth-
iobacillus ferrooxidans, Pseudomonas, Paenibacillus sp., Bacillus mucilaginosus, B. circulans, and
B. edaphicus has been reported to be released from potassium-bearing minerals in soils in
an accessible form [72].
Organic acids are produced and secreted by microbial inoculants, such as Bacillus
mucilagenosus and Bacillus edaphicus, in the solubilization of rock potassium [73]. Potassium
solubilizing bacteria (KSB) beneficial effects have been reported on the growth of grape
and cotton [74], sorghum [75], wheat [76], sudangrass [77], cucumber and pepper [66]. The
significant mobilization of high potassium from waste mica, which acted as a potassium
source for plant growth, resulted in wheat plants with Bacillus mucilaginosus, Azotobacter
chroococcum, and Rhizobium [78].

2.4. Sulfur Dissolving Microorganisms

For the growth and development of plants, sulfur is one of the sixteen elements
and the fourth main nutrient in crop production, after N, P, and K. As a result of mi-
crobial activity, which includes mineralization, immobilization, oxidation, and reduction
processes, sulfur transformations in the soil. Sulfur oxidizing bacteria synthesis of or-
ganic compounds from carbon dioxide by sulfur oxidation process and produce sulfuric
acids. Enzyme sulfatase was used in the catalyzation of sulfur compound mineraliza-
tion and transformation into forms accessible to plants [79]. After the inoculation of
sulfur-oxidizing bacteria (Thiobacillus), seeds of high S-demanding crops have proved to
be very effective, making sulfur more accessible to the plants. Some autotrophic species
also exhibit chemolithotrophic growth on inorganic sulfur compounds, such as Acidoth-
iobacillus, Thiosphaera, and Thiomicrospira, but some heterotrophs, such as Xanthobacter,
Paracoccus, Pseudomonas, and Alcaligens [80]. Thiobacillus novellus is considered an optional
chemoautotroph, while chemoautotrophs are obligatory for Thiobacillus ferrooxidans, T.
thiooxidans, T. denitrificans and T. thioparus. Inorganic sulfur compounds are reduced or par-
tially oxidized by a heterogeneous group of sulfur bacteria. Thiobacilli plays a significant
function in the sulfur oxidation and oxidation process, producing acidity, which aids to
solubilize plant nutrients and enhances soil fertility [81]. T. ferrooxidans and T. thioxidans
inoculation increased sulfur oxidation to pyrite and subsequently, rock phosphate solubi-
lization [82]. Elemental sulfur and thiosulphate are oxidized by some fungi, which include a
range of Penicillium species, Epicoccum nigrum, Alternaria tenius, Scolecobasidium constrictum,
Aspergillus, Aureobasidium pullulans, and Myrothecium cinctum [83] (Table 2).

2.5. Zinc Solubilizers

Microorganisms provide micronutrients, such as copper, iron, and zinc by transform-
ing the nutrients present in the soil into accessible fertilizers. The solubilization of zinc by
microorganisms, viz., T. thioxidans, Saccharomyces sp., and Bacillus subtilis. Bacillus sp. can be
used as a biofertilizer for zinc, can replace zinc sulfate, which is costly, and can be used in
Biology 2021, 10, 1111 7 of 22

conjunction with compounds, such as zinc sulfide (ZnS), zinc oxide (ZnO), zinc carbonate
(ZnCO3 ), and with cheap zinc compounds. Zinc, an important micronutrient for growth
and metabolism, is needed by plants and microorganisms. Zinc is the main compound
in an enzyme system, acting as a metal activator and co-factor for many enzymes [84].
Gluconacetobacter diazotrophicus, Pseudomonas, Aspergillus niger, and Penicillium luteum pro-
ducing organic acid, such as gluconic acids; it derivatives as 2- and 2,5-keto-derivatives
are Zn compound solubilizers [85]. Thiobacillus ferroxidans, T. thioxidans, and facultative
oxidizers of thermophilic iron have enormous ability to solubilize sulfide ore zinc [86].
Bullen and Kemila [87] report that a few fungal sp. were affected by zinc. Aspergillus niger
has been found to withstand a high level of zinc capable of growing below 1000 mg Zn
and is used for zinc quantification in soils containing low zinc (Table 2).
Biology 2021, 10, x 8 of 23

3. Plant Growth Promoting Rhizobacteria (PGPR)

Soil
beeninoculants or microbial
found to withstand inoculants
a high level are farm
of zinc capable applications
of growing below 1000thatmgstimulate
Zn and is the growth
of plants
usedand arequantification
for zinc beneficial microbes. Similar
in soils containing lowbacteria
zinc (Tableengage
2). in a symbiotic association
with crop plants, promoting both partners [14]. By stimulating growth regulators, these
3. Plant Growth Promoting Rhizobacteria (PGPR)
inoculants enhance plant nutrition and promote growth. Effective inoculants that increase
Soil inoculants or microbial inoculants are farm applications that stimulate the
the availability to plants of macronutrients, such as nitrogen and phosphorus, are nitrogen
growth of plants and are beneficial microbes. Similar bacteria indicate a symbiotic associ-
fixers ation
and phosphate
with crop plants,solubilizers
promoting[88].both These
partnersbacteria are classified
[14]. By stimulating growthas biofertilizers
regulators, and rhi-
zobacteria
these that promote
inoculants plant
enhance growth.
plant nutritionPGPR can be growth.
and promote definedEffective
as free-living
inoculantsbacteria
that of the rhi-
zosphere thatthe
increase enhance plant
availability growth
to plants and functionsuch
of macronutrients, as asspecialists
nitrogen and inphosphorus,
biocontrol,are biopesticides,
nitrogen fixers
or biofertilizers and phosphate
[10,89]. solubilizers [88].
PGPR inoculants These bacteria
alternate are classified
with chemical as biofertiliz-
fertilizers and pesticides
ers and rhizobacteria that promote plant growth. PGPR can be defined as free-living bac-
as biofertilizers and/or antagonists of phytopathogens either directly or indirectly [90,91].
teria of the rhizosphere that enhance plant growth and function as specialists in biocon-
In generating
trol, biopesticides, orplant
various growth
biofertilizers regulators
[10,89]. and by alternate
PGPR inoculants mobilizing nutrients
with chemical in soils, plant
ferti-
growth is stimulated.
lizers and pesticidesThe PGPR action
as biofertilizers and/ormechanisms
antagonists of are not fully known
phytopathogens but are assumed
either directly
or indirectly
to include: [90,91]. In fixation
(i) Nitrogen generating[92];
various
(ii)plant growthphosphate
Organic regulators and andby mobilizing
inorganicnu- phosphate or
trients in soils, plant growth is stimulated. The PGPR action mechanisms are not fully
other nutrient solubilization [93]; phytohormones, such as auxins, cytokinins [94], and
known but are assumed to include: (i) Nitrogen fixation [92]; (ii) Organic phosphate and
gibberellins
inorganic [95]; (iv) development
phosphate or other nutrient of solubilization
siderophores [96]
[93]; and (v) plant
phytohormones, defense
such by controlling
as auxins,
or inhibiting
cytokinins phytopathogens,
[94], and gibberellins improving soil structure,
[95]; (iv) development and bioremediating
of siderophores [96] and (v) plantcontaminated
soils by sequestering
defense by controllingtoxic heavy metals
or inhibiting and destroying
phytopathogens, improvingxenobiotic
soil structure,compounds
and biore- (such as
mediating
pesticides) contaminated
[97,98]. The PGPR soils inoculant
by sequestering toxicinclude
strains heavy metals and destroying
species xenobi-Azospirillum,
of Azotobacter,
otic compounds (such as pesticides) [97,98]. The PGPR inoculant strains include species
Agrobacterium, Acinetobacter, Alcaligenes, Arthrobacter, Acetobacter, Achromobacter, Aerobacter,
of Azotobacter, Azospirillum, Agrobacterium, Acinetobacter, Alcaligenes, Arthrobacter, Acetobac-
Burkholderia, Beijerinckia,
ter, Achromobacter, Aerobacter, Bacillus, Clostridium,
Burkholderia, Delfitia,
Beijerinckia, Erwinia,
Bacillus, Enterobacter,
Clostridium, Xanthomonas,
Delfitia, Er-
Klebsiella,
winia, Enterobacter, Xanthomonas, Klebsiella, Flavobacterium, Micrococcus, Pantoea agglomer- Rhizobium,
Flavobacterium, Micrococcus, Pantoea agglomerans, Paenibacillus macerans,
ans, Paenibacillus
Pseudomonas, macerans,
Rhodobacter, Rhizobium,
Serratia, andPseudomonas, Rhodobacter,
Rhodospirrilum [23] Serratia,
(Figureand Rhodospirri-
2 and Table 1).
lum [23] (Figure 2 and Table 1).

Figure 2. Biofertilizer classification and involving microorganisms.

Figure 2. Biofertilizer classification and involved microorganisms.
Biology 2021, 10, 1111 8 of 22

3.1. Phytohormones
Within the control of plant growth and production, phytohormones, such as ethylene, gib-
berellins, auxins, abscisic acid (ABA), and cytokinins, play a key role [98]. Gutierrez-Manero et al. [99]
have been reported that certain rhizospheric bacteria, such as Bacillus licheniformis and
Bacillus pumilus, are capable of producing gibberellins. Various PGPR inoculants, such
as Azospirillum brasilense, Paenibacillus polymyxa, Arthrobacter giacomelloi, Bradyrhizobium
japonicum, Bacillus licheniformi, and Pseudomonas fluorescens, have been reported for the
production of cytokinin [100,101]. Tissue expansion is encouraged by cytokinin, including
cell division and cell enlargement in the plant. The root to shoot ratio is found to be
reduced [102]. Auxin is an important phytohormone and controls multiple developmental
processes, including root cell division, root initiation, and cell enlargement [103]. Indole-3-
acetic acid (IAA) is produced by most rhizobacteria and stimulates plant growth promotion,
especially root initiation and elongation [104]. IAA provided by PGPR is reported to in-
crease root growth, modifying the plant (morphological functions) to uptake more nutrients
from the soil (Table 3). Ethylene is another important phytohormone and plays a major role
in the pathway of plant defense. Which inhibits root elongation and transport of auxins;
abscission of different organs contributes to fruit maturation and promotes senescence [105].
Azospirillum brasilense produces ethylene, which probably facilitates the growth of root
hair in tomato plants. Indeed A. brasilense inoculation had the mimicking effect of exoge-
nous ethylene supply to plants, while this effect was inhibited by the addition of inhibitor
for ethylene biosynthesis [106]. Lateral root extension and primary root elongation are
promoted by gibberellins [107]. For the development of gibberellins, PGPR inoculants
have been reported to produce gibberelline, several belonging to Acinetobacter calcoaceti-
cus, Achromobacter xylosoxidans, Azotobacter sp., Azospirillum sp., Rhizobia, Gluconobacter
diazotrophicus, Bacillus sp., and Herbaspirillum seropedicae [95]. Gutierrez-Manero et al. [99]
documented that four different forms of GA are produced by Bacillus licheniformis and B.
pumilus (Table 4).

Table 3. Plant growth promoting substance (acids) producing microorganisms.

Microorganisms Acids References

Bacillus pumils, B. subtilis, B. licheniformis, B. megaterium BHUPSB14, and Gibberellins, Ethylene, Cytokinin,
Paenibacillus polymyxa and ACC deaminase
Pseudomonas tabaci, P. putida, P. syringae, P. fluorescens, P. fluorescens G20-18, Ethylene, Indole-3-acetic acid,
P. fluorescens BHUPSB06, P. aeruginosa, P. cepacia, and P. corrugata Cytokinin, and ACC deaminase
Indole-3-acetic acid, Cytokinin, and
Rhizobium leguminosarum
HCN
Indole-3-acetic acid, Zeatin, and
Azospirillum brasilense and A. lipoferum, ethylene, Gibberellic acid (GA3), and
Abscisic acid (ABA)
[44,45,100]
Rhizobacterial isolates Auxins
Aeromonas veronii, Agrobacterium sp., Bradyrhizobium sp., Comamonas
acidovorans, Azotobacter chroococcum, Mesorhizobium ciceri, Azospirillum
Indole-3-acetic acid
amazonense, Rhizobium sp., Azotobacter sp., Kebsiellaoxytoca, Erwinia
herbicola, Bacillus subtilis, Serratia marcescens, and Enterobacter asburiae
Alcaligenes piechaudii and Enterobacter cloacae Indole-3-acetic acid, ACC deaminase
Variovorax paradoxus ACC deaminase
Pantoea agglomerans and Pantoea herbicola IAA and Auxin
GA3, indole-3-acetic acid, and
Gluconobacter diazotrophicus
gibberellin GA1
Biology 2021, 10, 1111 9 of 22

Table 4. Plant growth promoting and bio controlling enzymes and acids producing phosphate solubilizing microbes.

Microorganisms Enzymes Acids References

Lactic, malic, citric, itaconic,
Bacillus circulans, B.cereus, B. fusiformis, B.pumilus var.2, isovaleric, isobutyric, acetic,
B. megaterium, B. mycoides, B. polymyxa, B. coagulans B. gluconic, propionic,
Phytase and
chitinolyticus, B. subtilis, B. subtilisvar.2, B. licheniformis, heptonic, Caproic,
D-a-glycerophosphate
B. amyloliquefaciens, B. atrophaeus, Paenibacillus Isocaproic, Formic, valeric,
macerans, and B. japonicum succinic, Oxalic, oxalacetic,
malonic, and IAA
Bradyrhizobium sp., Phytate IAA
Burkholderia cepacia, Citrobacter sp., and Citrobacter
Acid phosphatase Gluconic acid
freundii
Escherichia intermedia and E. freundii - Lactic
Lactic, itaconic, isovaleric,
isobutyric, acetic,
2-ketogluconic, gluconic,
Enterobacter asburiae, E. aerogenes, E. cloacae, E.
Acid phosphatase succinic, acetic, glutamic,
aerogenes, and E. intermedium
oxaloacetic, pyruvic, malic,
fumaric, and
alpha-ketoglutaric [95,100,101]

Acid phosphatase,
Lactic, malic, citric, gluconic,
Pseudomonas putida, P. striata, P. fluorescens, P. calcis, P. Phytase, and
2-ketogluconic acid,
mendocina, and P. aeruginosa Phosphonoacetate
and tartaric
hydrolase
Proteus mirabilis Acid phosphatase
Serratia phosphoticum and S. marcescens Acid phosphatase Gluconic acid and IAA
Rhizobium meliloti, R. leguminosarum, R. leguminosarum
2-ketogluconic acid, HCN,
bv.phaseoli, R. leguminosarum bv. Trifolii, and R. Phytate
and IAA
leguminosarum bv. Viciae
Klebsiella aerogenes C-P Lyase
IAA, malic, succinic, and
Sinorhizobium meliloti Phytate
fumaric
Stenotrophomonas maltophilia Gluconic acid
Mesorhizobium cireri and M. mediterraneum Phytate
Acetobacter sp. Gluconic acid

3.2. Siderophore
Siderophore is an essential element for various biological processes in all organisms
in the biosphere. Bacteria, fungi, actinomycetes, and certain algae developing under low
iron stress synthesize siderophores. It is an iron-binding protein that has a molecular
weight range of 400–1500 Da [108]. According to the functional group, they are divided
into four families, i.e., carboxylates, catecholate, hydroxamates, and pyoverdines. About
270 siderophores were characterized structurally out of the 500 types [109]. Microbial
siderophores help to identify the complex of bacterial ferric siderophores and enhance
plant iron uptake [110] and are also significant in the presence of metals, such as nickel and
cadmium, in the uptake of iron by plants [111]. Ferric ion absorption through siderophore
is largely used in the soil, human body, and marine environments by pathogenic and
nonpathogenic microorganisms.
Organisms producing siderophore includes bacteria (Escherichia coli, Salmonella, Kleb-
siella pneumonia, Aerobacter aerogens, Mycobacterium sp., Yersinia, Enterobacter, Vibrio cholera,
Aeromonas and Vibrio anguillarum); Fungi include (Trametes versicolor, Aspergillus versicolor,
A. nidulans, Penicillium citrinum, P. chrysogenum, Ustilago sphaerogina, Rhizopus, Mucor,
Biology 2021, 10, 1111 10 of 22

Rhodotorula minuta, Debaromyces sp., and Saccharomyces cerevisiae) [44], Actinomycetes

constitute (Nocardia asteroids, Streptomyces griseus, and Actinomadura madurae), and Al-
gae (Anabaena cylindrica and Anabaena flosaquae) [45] (Table 2). Siderophore produced by
Azospirillum inoculation; it can modify the root morphology by releasing substances that
control plant growth [34,112].

3.3. Phytoremediation of Heavy Metals by PGPR

Phytoremediation is an energy proficient and cheap method of detoxification. Plant
metabolism is influenced by reducing the metal bioavailability by absorbing them in
the biomass of shoot [17]. Heavy metal phytoremediation is performed using PGPR.
Agricultural activities and industrialization are the major reasons for metal contamination.
Metal contamination of soil has a significant bearing on PGPR capacities. Upkeeping of
metal homeostasis opposition in bacteria is achieved via the synthesis of binding proteins,
sequestration, detoxification, reduced uptake, and active efflux [113]. Singh et al. [114]
revealed that heavy metal contamination of soil caused the blocking of functional molecules,
essential components dislodging in biomolecules, alteration of structure, and function
of enzymes/protein. Heavy metals additionally repress biochemical processes, such as
respiration and photosynthesis, resulting in a reduction of growth. The proliferation of
root hair and drastic expansion of the surface area of root resulted after the inoculation of
maize with Azospirillum brasilense [115]. Intense heavy metal tolerant Pseudomonas putida,
and P. fluorescens PGPR have been successfully assessed under states of contaminated soils
and hyperosmolarity [116]. In addition to PGPR, a significant part of phytoremediation is
performed by mycorrhizal fungi [117]. Streptomyces acidiscabies E13 strain applies positive
growth developing effects in nickel contaminated soil of cowpea most likely by producing
hydroxamate siderophores and binding of iron and nickel [112].

3.4. Antibiotic
Several bacterial antibiotics were used, such as aldehydes, hydrogen cyanide, alco-
hols, sulfides and ketones, diacetyl phloroglucinol, xanthobaccin, 2,4-diacetylphloroglucinol
(DAPG), viscosinamide, mupirocin, pyocyanin, phenazine-1-carboxylic acid, phenazine-
1-carboxamide (PCN), phenazine-1-carboxylic acid (PCA), hydroxy phenazines, zwitter-
micin A, butyrolactones, pyrrolnitrin, pyoluteorin, phenazine-1-carboxylic acid, kanosamine,
oligomycin A, 2,4-diacetyl phloroglucinol, oomycin A, pyrrolnitrin [35,118], Agrocin 84,
Agrocin 434 [119], herbicolin, phenazine [120], pyoluteorin, oomycin, siderophores, pyrrolni-
trin, and hydrolytic enzymes, such as laminarinase, chitinase, Q-1,3-glucanase, lipase, and
protease, as well as small molecules, such as hydrogen cyanide (HCN).
Bacillus sp. produces by circulin, polymyxin, and colistin, the majority of active com-
pounds gram-negative and gram-positive bacteria along with many fungi [121].
Siddiqui et al. [122] reported the effect of Rhizobium to have higher colonization and
siderophores production. Pseudomonas sp., producing HCN and DAPG, are contributing
to the biological control of tomato canker bacteria [123]. Expression of various antibiotics
by Pseudomonas was reported; phenazine, pyoluteorin [118], lipopeptide antibiotics [124] 2,
4-diacetylphloroglucinol [123] and bacterial antibiotic manufacturers are genetically manip-
ulated, which is a powerful method for deciding their role in the suppression of diseases.
Arabidopsis thaliana infected with Pseudomonas syringae gets protection against surfactin, which
is produced by Bacillus subtilis. In addition, it protected the pathogen and also necessary for
root colonization [125].

4. Biofertilizer Carrier
The carrier is the significant group of inoculants, which help deliver the appropriate
volume of PGPM in superior physiological state. Assorted materials are used as inoculants
carriers for having improved biological effectiveness, endurance, and shielding bacteria
from abiotic and biotic stresses. The comprising elements of the carrier materials can be
organic, inorganic, or synthetic. An appropriate carrier is chosen, depending on properties
Biology 2021, 10, 1111 11 of 22

such as availability, low cost, easy use, packageability, and mixability. Additionally, the
gas exchange must be allowed by the carrier, especially oxygen, which must have a high
water-holding capacity and increased content of organic matter [126]. The physical form
of biofertilizer is characterized by the carrier used. The mixture of soil carrier materials is
utilized as dry inoculants, such as coal clays, peat, inert materials (bentonite, perlite, kaolin,
silicates, and vermiculite), organic materials (sawdust, wheat bran, soybean meal, and
composts), or inorganic soil (volcanic pumice or diatomite earth and lapillus). A variety
of liquid inoculants, such as organic oils, oil-in-water suspensions, broth cultures, and
minerals, can be utilized as carriers. Suitable carrier material for both bacterial inoculants
and the plants themselves must be non-toxic. Moreover, Stephens and Rask [127]; Ferreira
and Castro [128] expressed the properties of the carrier as promptly, plentifully, and
locally assessable at less cost, easily sterilizable and neutral with a readily adjustable
pH. The last choice of carrier incorporates properties, such as survival during storage,
microbial multiplication, planting machinery, and sufficient cost, the general strategy
of cultivation (Table 5).

Table 5. Microbial inoculants carrier types as biofertilizer.

Materials Category Reference

Preservative and Culture media ( liquid and powder) Bacterial cultures (lyophilized)
Alginate and xanthan gum Biopolymer
Black ash, paddy husk, black ash plus husk mixture, husk powder
and pressmud, soybean and peanut oils, farmyard manure, plant
debris, wheat bran, composts, spent mushroom composts, sugar Waste materials (Plant) Bashan and
industry waste, agricultural waste material, soybean meal, coconut de-Bashan, [129]
shell powder, and teak leaf powder
Lignite, pressmud, charcoal, inorganic soil, coal, clays and peat Soils
Carrageenan, polyacrylamide, calcium sulfate, polysaccharide-like
Inert materials
alginate, ground rock phosphate, vermiculite, and perlite

Tilak [130] wrote about Farmyard manure (FYM) using blends, such as FYM + char-
coal and soil, FYM + soil, and FYM + charcoal + soil, account for high viable counts of
Azospirillum and survival up to 31 weeks. For the production of inoculants, carriers such as
vermiculite clay, farmyard manure, coconut shell powder, teak leaf powder, and compost
were used [131]. Locally accessible materials, such as coffee waste, soil, lignite, pressmud,
and charcoal, were found to be superior to other carriers, which includes peat for Azospir-
illum, with the survival of 200 days and the decline rate in Azospirillum population was
much lower in pressmud [132]. Singaravadivel and Anthoni Raj [133] reported that black
ash plus husk mixture, pressmud, husk powder, black ash, and paddy husk were suitable
and efficient carriers for Rhizobium and were also comparable with peat and lignite.

5. Biopesticides
Compared to conventional pesticides, biopesticides pose less risk to humans and the
environment, gaining global attention as a new instrument for destroying or controlling
pest species such as weeds, plant diseases, and insects [134,135]. Most biopesticides are
advantageous for non-target biological safety and higher selectivity [136]. Biopesticides are
types of pesticides that are produced from naturally occurring substances that control pests
in an eco-friendly way via nontoxic mechanisms. Microorganism-derived biopesticides
(Nucleopolyhedrosis virus and Bacillus thuringiensis, Trichoderma), plants (Azadirachta and
Chrysanthemum), and animals (nematodes) contain their products (microbial products and
phytochemicals) or by-products (semiochemicals) and live species (natural enemies) [137].
Biopesticides are categorized into three main categories: (i) pest-controlled microorgan-
isms (microbial pesticides), (ii) naturally occurring pest-controlled substances (biochemical
pesticides), and (iii) plant-controlled pesticides with added genetic material (PIPs). The
Biology 2021, 10, 1111 12 of 22

use of biopesticides has increased by about 10% each year globally [138]. Biopesticides are
natural or organically inferred agents, applied similarly to chemical pesticides, but accom-
plish environment-friendly pest management. All pest management products, particularly
microbial agents, are helpful in control but need to be correctly formulated and used [139]
(Figure 3 and Tables 1 and 6).

Table 6. Microbial-based biopesticides.

Micro Plant Disease Nematicides

Organisms Pest Control Weed Control Control Control Fungicides Reference

Bacillus pumilus,
Bacillus thuringiensis, B. B. subtilis,
thuringiensis var. kurstaki, B. Pseudomonas Bacillus amyloliq-
thuringiensis var. israelensis, B. Xanthomonas spp., Bacillus firmus, uefaciens, B.
Bacteria thuringiensis var. tenebrionis, B. campestris pv. Streptomyces Pasteuria licheniformis, B.
thuringiensis var. aizawai, B. Poannua griseoviridis, penetrans, and pumilus, and B.
thuringiensis japonensis, B. popilliae, and Pasteuria usage subtilis
B. lentimorbus, B. sphaericus, Burkholderia
Erwinia amylovora, and B. pumilus cepacia
Ampelomyces
quisqualis,
Candida sp.,
Clonostachys Paecilomyces
Colletotrichum rosea f. lilacinus,
Beauveria bassiana, Metarhizium gloeosporioides, catenulate, Myrothecium
anisopliae, Entomophaga, Zoopthora, Chondrostereum Coniothyrium verrucaria,
Fungi Paecilomyces fumosoroseus, purpureum and minitans, Verticillium
Normuraea, Lecanicillium lecanii, L. Cylindrobasid- Pseudozyma chlamydospo-
longisporum, Lagenidium giganteum, ium flocculosa,
and Verticillium lecanii rium, and
laeve Trichoderma Pochonia
harzianum, T. chlamydosporia
koningii, T.
viride, and [24,25,137,
Chaetomium 140–146].
cupreum

Protozoa Nosema locustae, Thelohania, and

Vairimorpha
Steinernema feltiae, S. carpocapsae, S.
Nematodes glaseri, S. riobravis, and
Heterorhabditis heliothidis
Tussock moth NPV, Pine sawfly
NPV, Granulosis viruses, Codling
moth granulosis virus (GV), Gypsy
moth nuclear polyhedrosis (NPV),
Nuclear polyhedrosis viruses,
non-occluded baculoviruses,
Adoxophyes orana granulovirus
(GV)+ Homona magnanima GV,
Cydia pomonella granulovirus,
Nucleopolyhedrovirus Neodiprion
Virus abietis, Heliothis zea NPV,
Anagrapha falcifera NPV, Spodoptera
exigua NPV, Mamestra configurata
NPV, Ectropis obliqua hypulina
NPV, Laphygma exigua NPV,
Prodenia litura NPV, Buzura
suppressaria NPV, Gynaephora
ruoergensis NPV, Mythimna
separata NPV, Periplaneta fuliginosa
densovirus virus, Pieris rapae GV,
Mythimna separata GV, and Plutella
xylostella GV

5.1. Microbial Pesticides

Microbial pesticides are early developed and genetically modified. Organisms, such
as algae, protozoans, fungi, viruses, or bacteria, are widely used. They develop pest-
specific toxin, that causes disease, prevents the development of other microorganisms
through antagonism or different nontoxic mechanism of action, compared to traditional
chemical pesticides [147]. Normally, used microbial biopesticides are living microorgan-
isms, pathogenic to the pest of interest, which include bioinsecticides (Bt), bioherbicides
(Phytophthora), and bio fungicides (Pseudomonas, Trichoderma, and Bacillus) [148]. Mi-
Biology 2021, 10, x 13 of 23
Biology 2021, 10, 1111 13 of 22

and phytochemicals) or by-products (semiochemicals) and live species (natural enemies)

crobialBiopesticides
[137]. biopesticidesare
comprise of microorganisms
categorized suchcategories:
into three main as protozoa,
(i) bacteria, fungi, viruses,
pest-controlled micro-
and oomycetes, which are generally used to control weeds, pestiferous insects, and plant
organisms (microbial pesticides), (ii) naturally occurring pest-controlled substances (bio-
pathogens biologically. In the market, 74% are guaranteed by bacterial biopesticides, 10%
chemical pesticides), and (iii) plant-controlled pesticides with added genetic material
by fungal biopesticides, 10% by viral biopesticides, 8% by predator biopesticides, and 3%
(PIPs). The use of biopesticides has increased by about 10% each year globally [138]. Bi-
by others for a wide range of crops [149]. By generating toxic metabolites or various other
opesticides are natural or organically inferred agents, applied similarly to chemical pesti-
modes, microbial pesticides can suppress different target pests [147]. The species used as
cides, but accomplish environment-friendly pest management. All pest management
microbial insecticides are generally nonpathogenic and nontoxic to all living organisms
products, particularly microbial agents, are helpful in control but need to be correctly for-
and not so firmly confined closely to the targeted pests [150].
mulated and used [139] (Figure 3 and Tables 1 and 6).

Figure 3. Biopesticides classification and involving microorganisms.

Figure 3. Biopesticides classification and involving microorganisms.

Table 6. Microbial-based biopesticides.

5.1.1. Bacteria
Micro Bacterial biopesticides are used to monitor weeds, plant diseases, nematodes, and in-
Reference
sects. Pest is controlled in Plant
various Diseasedelivering
manners: Nematicidestoxins, outcompeting and harming
Organis Pest Control Weed Control Fungicides
pathogens, promoting shoot and Control
root growth, and Control
producing anti-fungal compounds. Ex-
ms
amples of bacterial biopesticides are Pseudomonas syringae, which controls bacterial spots,
Bacillus
B. Bacillus thuringiensis (Bt), which targets larvae. Bacillus thuringiensis (Berliner), the ento-
and
Bacillus thuringiensis,
pumilus, B.
mopathogenic
thuringiensis var. kurstaki, B. bacterium, commonly recognized as a microbial biopesticide, Bacillus which, during
bacterialB. subtilis,
sporulation, generates crystal protein (d-endotoxin) whenamyloliquefacingested by the suscepti-
thuringiensis var. israelensis,
ble insects triggers lysis of gut Pseudomonas
cells [140]. Bacillus
Spore firmus,
formers, such as Pseudomonas aeroginosa,
thuringiensis var. tenebrionis, B. Xanthomonas iens, B.
Serratia marcesens, Bacillus spp,
thuringiensis, and Pasteuria
Bacillus popilliae, are used commercially for
Bacteria thuringiensis var. aizawai, B. campestris pv. licheniformis,
their efficacy and safety [141]. Streptomyces
Pseudomonades, penetrans,
includingandP. fluorescence, P. syringae,
[24,25,137,1
and
thuringiensis japonensis, B. Poannua B. pumilus,
P. aeruginosa, are used to develop biopesticides.Pasteuria
griseoviridis, usage of Pseudomonas aureofaciens
Some strains 40–146].
popilliae, B. lentimorbus, B. and B.
control plant pathogens, causing and
soft rots and damping-off [151]. Over half of mortality in
sphaericus, Erwinia amylovora, and subtilis
Helicoverpa armigera and Spodoptera litura is by Pseudomonas sp., Bacillus subtilis, B. megaterium,
Burkholderia
B. pumilus and B. amyloliquefaciens [24]. Microbes
cepacia like B. subtilis, B. pumilus, B. licheniformis, and B. amy-
loliquefaciens are marketed as biopesticides
Beauveria bassiana, Metarhizium Colletotrichum Ampelomyces Bacillus sphaericus has been reported to have
[142].Paecilomyces
Fungi a dual role in larvicidal toxicity to Culex pipien, the blood-feeding mosquito, and the abil-
anisopliae, Entomophaga,Zoopthora, gloeosporioides, quisqualis, lilacinus,
Biology 2021, 10, 1111 14 of 22

ity to excrete extracellular alkaline protease (AP) in the medium used for growth [152].
Streptomyces griseoviridis is the first biofungicides available to combat root infecting fungi
in greenhouse crops. Despite such products’ long-term accomplishments, the global de-
mand for new biopesticides remains [153,154]. Bacillus thuringiensis is sporulated, and it
contains the proteins Cyt and Cry. Commercialized insecticides are products made up
of 2% Bt, a combination of spores and protein crystals [155]. Bacillus thuringiensis can be
more effective on Aedes aegypti, while the strain of B. sphaericus may be more effective on
various mosquitoes, such as Culex quinquefasciatus [156]. In vegetables, it is recommended
to use Bacillus thuringiensis (Bt) to manage insects, such as the velvet bean caterpillar, cab-
bage looper diamondback moth, and armyworm [143]. Sunitha et al. [157] found that the
biopesticides based on B. thuringiensis are moderately active against Metarhizium anisopliae,
while newer pesticides, such as spinosad and indoxacarb, were highly effective in control-
ling Maruca vitrata. Schunemann et al. [143] recommended various trade products of B.
thuringiensis to control insect pests of agriculture, including mosquito species. Most formu-
lations of spore-crystal toxins are obtained from a variety of strains, such as B. thuringiensis
var. kurstaki, B. thuringiensis var. tenebrionis, B. thuringiensis var. israelensis, B. thuringiensis
var. aizawai, and B. thuringiensis var. San Diego [143].

5.1.2. Fungi
In killing mites, weeds, nematodes, insects, or other fungi, new fungal biopesticides
are used. Like bacteria, they produce toxins, such as bacteria, that outcompete targeted
pathogens. These can also paralyze plant pathogens or insects by attacking them. Tricho-
derma harzianum, targeting Pythium, Rhizoctonia, and Fusarium, is also a fungicide [158].
Fungal species, such as Paecilomyces fumosoroseus, Beauveria bassiana, Verticillium lecani, No-
muraea rileyi, and Metarhizium anisopliae are used in insect control [25]. Beauverin peptide
isolated from Beauveria bassiana is active against larvae of mosquito [159]. Fungal pathogens
Metarhizium anisopliae and Beauveria bassiana have a lengthy- history in the perspective of
agricultural pests. Current molecular techniques allow for the characterization and monitor-
ing isolates of fungi, as well as for recognizing fungal isolates in the environment [160,161].
The codling moth and colorado potato beetle were regulated using Beauveria bassiana [162].
Biopesticides, such as M. anisopliae are commercially available, which controls several
insect species [163]. Destruxins, a toxin produced by M. anisopliae, which has two separate
virulence mechanisms, includes invading and destroying the insects, and third mechanisms
by invading the ticks by a strategy of integument breakdown [164].

5.1.3. Nematodes
Several round colorless parasites, nematodes, and microscopic worms of the plant
cause severe crop damage. Though targeting plants, some are essentially advantageous
in attacking soil-dwelling insect pests, such as root weevils and cutworms [155]. Nema-
tode biopesticides, such as Steinernema sp. and Heterorhabditis sp., that attack the hosts as
contagious juveniles (IJs) are widely used [165]. Heterorhabditis megidis, H. bacteriophora,
Steinernema scapterisci, S. carpocapsae, S. riobrave, S. glaseri, and S. feltiae are common ento-
mogenous nematodes used as insecticides [144].

5.1.4. Protozoa
Protozoans are single-celled organisms surviving both in soil and water. Most species
are parasites of insects, typically feeding on bacteria, while others feed on organic decay.
More than any other insects, lepidopteran and orthopteran, hoppers especially are killed
by Vairimorpha and Nosema comparing to other insects [166]. Nosema locustae spores
enter and feed on the grasshopper body cavity. Mortality can take up to 3–4 weeks [167].

5.1.5. Viruses
Baculoviruses are a family of viral biopesticides believed to infect insects and arthro-
pods related to them. Potential pesticides are the family Baculoviridae. This biopesticide is
Biology 2021, 10, 1111 15 of 22

used in many parts of the world for the prevention of destructive caterpillar pests [168].
Nucleopolyhedro virus (NPVs) and Granulovirus (GVs) are found to be the two main
genera of the Baculoviridae family [169]. These viruses are valuable, causing minimum
damage, suitable for the crop, and management of pests, since only a few species of Lepi-
doptera larvae are infected, due to host specificity. The corn earworm Heliothis/Helicoverpa
sp. by nuclear polyhedrosis virus and the codling moth of Cydia pomonella by granulosis
virus are some examples. In contrast with traditional synthetic insecticides, Baculoviruses
can control lepidopteran pests causing slight or no damage to the targeted species. The
first viral biopesticide detected is the Heliothis nuclear polyhedrosis virus (NPV) [145].
Expression vectors, developed based on baculoviruses, were used in the production of
viral pesticides using Autographa californica nucleopolyhedro virus (AcMNPV). Autographa
gemmatalis control the soybean velvet bean caterpillar [146].

5.2. Biochemical Pesticides

Biochemical pesticides are equivalent to the naturally occurring or compounds, de-
rived synthetically, that are used in pest control. The influence of growth and develop-ment
of insect pests is achieved by the biochemical pesticides which are nontoxic in action de-
stroying or attacking pest. Pheromones are substances that attract or repel pest or growth
regulators of plant growth produced by biochemical pesticides that interfere in mating
and growth of pests, including elements, such as insect sex pheromones interfering in
mating, as well as attracting insect pests to traps using extracts of the scented plant. Chem-
ical substances, such as pheromones, are emitted by living organisms that are used in
sending messages to the same species individuals of mostly opposite sex [170]. Minimal
crop damage can be achieved by using sex pheromones and plant protection measures
by recognizing the crops and insects for further required action. The remarkably effective
synthetic attractant is used in a low population, often use pheromone traps or a technique
called “attracting and killing”.

5.3. Plant Incorporated Protectants (PIPS)

Substances producing pesticides (PIPs) are introduced into the target crop plant ge-
nome, thereby providing the plant with capability of killing the pest. Scientists insert a
insecticidal protein gene of Bacillus thuringiensis into the plant’s genetic material thereby
allow the plants to kill the pest. Environmental Protection Agency controls the protein,
genetic material, and not the plant itself [170].

6. Conclusions
Biofertilizers based on microbial inoculants are attractive because they act in fix-
ing nitrogen, phosphate, sulfate, potassium, zinc, and solubilize nutrients and enhance
plant growth by hormonal action or antibiosis and decomposing organic residues. Plant
reinforcers and phytostimulators can be used by plants to improve their growth when
insufficient quantities of nitrogens are present. Moreover, they emerged from the soil
and appeared to be competent in the rhizosphere. Plant growth-promoting rhizobacteria
with numerous activities, such as nitrogen fixation, phytohormone production, micro- and
macro-mineral solubilization, enzymes production, or fungicidal compounds of antibiotics
synthesis. Siderophores, a competition with detrimental microorganisms, have bioremedia-
tion potentials by detoxifying contaminants, such as pesticides, heavy metals, and regulate
phytopathogens, as biopesticides. They also improve and maintain the soil rhizosphere
biologically by microbes, such as bacteria, fungi, algae, and actinomycetes. This review
discusses the idea of single or consortiums have multiple activities, such as nitrogen-fixing,
phosphate, sulfate, and zinc solubilization, through enzyme and acid production. The
effect of microorganisms as biofertilizers and the role of biopesticides enhance plant growth
by rendering them as tolerant to pests and to improve the crop health and food safety.
Biology 2021, 10, 1111 16 of 22

Author Contributions: Conceptualization, R.S. and O.O.B.; writing—original draft preparation, R.S.;
writing—review and editing, O.O.B.; visualization, O.O.B.; supervision, O.O.B.; funding acquisition,
O.O.B. All authors have read and agreed to the published version of the manuscript.
Funding: This research received no external funding.
Institutional Review Board Statement: Not applicable.
Informed Consent Statement: Not applicable.
Acknowledgments: The authors like to thank the North-West University for a postdoctoral bursary.
Conflicts of Interest: The authors declare that they have no conflict of interest, either financial or
commercial wise.

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