Bacillus thuringiensis as a Biofertilizer and Biostimulator: a Mini-Review of the Little-Known Plant Growth-Promoting Properties of Bt

Abstract

Bacillus thuringiensis (Bt) is a gram-positive spore-forming soil microorganism. Because the insecticidal activities of Bt are well known, it has been used as a tool for insect pest control worldwide. The beneficial features of Bt are not limited to its role as an insecticide; it is also used to control phytopathogenic fungi via chitinolytic activity. Bt-related studies are mostly focused on its biocontrol properties. However, studies focusing on the biostimulation and biofertilizer features of Bt, including its interactions with plants, are limited. Bt is a successful endophyte in many plants and can directly promote their development or indirectly induce plant growth by suppressing diseases. Although there are various commercial biopesticide Bt-based products, there are no commercial Bt-based plant growth-promoting rhizobacteria products on the biofertilizer market. As novel Bt strain exploration increases, there will likely be new Bt-based products with powerful biofertilizer activities in the future. The objective of this paper is to review, discuss, and evaluate the exceptional features of Bt as a plant growth promoter.

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Current Microbiology
https://doi.org/10.1007/s00284-019-01705-9
REVIEW ARTICLE
Bacillus thuringiensis asaBiofertilizer andBiostimulator:
aMini‑Review oftheLittle‑Known Plant Growth‑Promoting Properties
ofBt
UgurAzizoglu1
Received: 7 March 2019 / Accepted: 8 May 2019
© Springer Science+Business Media, LLC, part of Springer Nature 2019
Abstract
Bacillus thuringiensis (Bt) is a gram-positive spore-forming soil microorganism. Because the insecticidal activities of Bt are
well known, it has been used as a tool for insect pest control worldwide. The beneficial features of Bt are not limited to its
role as an insecticide; it is also used to control phytopathogenic fungi via chitinolytic activity. Bt-related studies are mostly
focused on its biocontrol properties. However, studies focusing on the biostimulation and biofertilizer features of Bt, including
its interactions with plants, are limited. Bt is a successful endophyte in many plants and can directly promote their develop-
ment or indirectly induce plant growth by suppressing diseases. Although there are various commercial biopesticide Bt-based
products, there are no commercial Bt-based plant growth-promoting rhizobacteria products on the biofertilizer market. As
novel Bt strain exploration increases, there will likely be new Bt-based products with powerful biofertilizer activities in the
future. The objective of this paper is to review, discuss, and evaluate the exceptional features of Bt as a plant growth promoter.
Introduction
Plant growth-promoting bacteria (PGPB) are generally
obtained from soils [1, 2] and can also be isolated from phyl-
losphere [3]. Many species of bacteria such as Alcaligenes,
Agrobacterium, Azospirillum, Azotobacter, Arthrobacter,
Bacillus, Bradyrhizobium, Burkholderia, Caulobacter,
Chromobacterium, Enterobacter, Erwinia, Flavobacterium,
Herbaspirillum, Klebsiella, Mesorhizobium, Micrococcus,
Pseudomonas, Rhizobium, Rhodococcus, and Serratia
enhance plant growth and are thus termed PGPB [4–16].
Though it is believed that Bacillus has less rhizocompetence
than other PGPB, studies of the genetic diversity of Bacillus
in soil near roots inferred that rhizocompetence is character-
istic of the strain but not specific to the genus or species [2,
17]. Bacillus species including Lysinibacillus sphaericus,
B. amyloliquefaciens B. cereus, B. mycoides, B. subtilis, B.
pasteurii, B. pumilus, and B. thuringiensis may reduce the
incidence or severity of plant diseases through the elicitation
of induced systemic resistance against pathogens of plants;
hence, these bacteria can indirectly promote the plant growth
[18–21].
Bacillus thuringiensis (Bt) is a unique soil bacterium that
is gram-positive aerobic or facultative spore-forming and is
included in the genus Bacillus. Bt-related studies are mostly
focused on its insecticidal activity due to its entomopath-
ogenic properties. Meanwhile, studies focusing on the
biostimulation and biofertilizer features of Bt, including its
interactions with plants, are limited. In fact, differences in
the soil and bacterial colonies associated with plants may be
a sign of the intrinsic variability of Bt regarding its ability
to interact with plants [2]. It was also reported that Bt can
successfully colonize cabbage, cotton, soybean, and rice as
an endophyte [22–24]. The efficient Bt colonization in cab-
bage seedling roots may affect productivity and may be the
main route of Bt interaction with the plants [23, 24]. Bt can
also colonize the roots of some legumes, which leads to an
increase of nodulation and growth [24, 25]. Bt can directly
promote the growth of plants and can also indirectly induce
growth by suppressing plant diseases. This mini-review
addresses Bt’s little-known features as a plant growth pro-
moter in addition to its well-known properties.
* Ugur Azizoglu
azizogluugur@hotmail.com; azizoglu@erciyes.edu.tr
1 Department ofCrop andAnimal Production, Safiye
Cikrikcioglu Vocational School, Kayseri University, Kayseri,
Turkey

U.Azizoglu
1 3
Bacillus thuringiensis asaBioinsecticide
A Short History ofBacillus thuringiensis
In 1901, Bt was isolated by Japanese scientist Shigetane
Ishiwatari. He named it sotto disease because it caused dis-
ease in larvae of Bombyx mori. In 1908, Iwabuchi named it
Bacillus sotto. In 1911, Berliner isolated the same bacteria in
the Thuringia region of Germany from Ephestia kuehniella
and named it Bacillus thuringiensis [26–28]. Following his
detailed studies on Bt in 1915, Berliner detected the pres-
ence of various inclusions of Bt along with its endospores
[29, 30]. In 1927, Mattes [31] observed the same inclusions
of Bt, but it was not until 1953 that the insecticidal property
of these inclusions was clearly recognized [32]. The impor-
tance of parasporal crystal proteins and their insecticidal
activity was noted by Thomas Angus [33]. In 1955, Han-
nay and Fitz-James [34] discovered that the toxic parasporal
crystals were made of proteins [33–35].
Genomics ofBacillus thuringiensis
Bt strains have a genome consisting of approximately 6 mil-
lion base pairs [36] and may possess 2–11 plasmids with
lengths varying between 2 and 272kb [37, 38]. Genes
encoding insecticidal crystal proteins (ICP) are located on
these plasmids [39]. There are multiple mobile elements
around the cry genes found on large or small plasmids.
These plasmids can be transferred from one Bt organism to
another via conjugation-like mechanisms [40].
Expression oftheCry Genes
There is an asymmetric cell division during the sporula-
tion stage of Bt, which consists of seven stages [41]. An
important feature of the sporulation stage is the formation
of parasporal crystals. The insecticidal toxins (Cry toxins)
are usually expressed as δ-endotoxin and specifically act
on some pest insect species [28, 42, 43]. Genes encoding
these toxins are termed cry genes [44, 45]. One significant
common feature of the cry genes is that they are expressed
during the stationary growth phase. These proteins start to
appear during the 3rd phase of sporulation and persist until
the end of the 7th phase [41, 46].
Insecticidal Proteins ofBacillus thuringiensis
Up to now, 806 Bt cry genes have been sequenced and cat-
egorized into 75 different toxin groups (Cry1, Cry2,….
Cry75) based on their amino acid sequence [47]. Every Cry
toxin group (e.g., Cry1 and Cry75 toxin groups) has less
than 45% amino acid similarity with other toxins in other
Cry toxin groups. The individuals in groups that are desig-
nated with uppercase letters (e.g., Cry1A, Cry1B) have more
than 45% but less than 78% amino acid similarity to each
other. The individuals in groups designated with lowercase
letters (e.g., Cry1Aa, Cry1Ac, and Cry1Ab) have more than
78% but less than 95% amino acid similarity to each other
[44, 48]. Additionally, three cyt families (cyt1–cyt3) con-
sisting of 40 cyt genes have been characterized in Bt [47].
Some Bt strains produce nonparasporal insecticidal proteins
during vegetative growth termed VIP (Vegetative Insecti-
cidal Proteins). Up to the present, 146 different vip genes
have been categorized into four types: Vip1, Vip2, Vip3,
and Vip4 [47].
Bacillus thuringiensis asaPlant Growth Promoter
Generally, bacterial strains that have useful effects on plant
growth are considered PGPB [25, 49]. PGPB are beneficial
microorganisms that help plant development [e.g., by pro-
ducing indole-3-acetic acid (IAA), 1-aminocyclopropane-
1-carboxylate-deaminase (ACC-deaminase), phosphate-
solubilizing enzyme (PSE), and siderophores (SD)], exhibit
antimicrobial activity against plant pathogens (e.g., by pro-
ducing bacteriocin, zwittermicin, fengycin, chitinase, and
cell wall-degrading enzyme) (Fig.1) [3, 49–51]. Azospiril-
lum, Bacillus, Bradyrhizobium, Herbaspirillum, Rhizobium,
and Pseudomonas are well-known bacteria as a plant growth
promoter and they interact with plant roots [4, 52–54].
Phytohormones have important functions in plant
growth and development as regulators and signals. They
are produced by bacteria that colonize plant roots and
play key roles in plant growth, plant pathology, and
plant–microorganism interactions [51, 55–57]. IAA is a
phytohormone of the auxin class and is the most physi-
ologically, biochemically, and genetically studied plant
growth hormone [51, 58]. Bacillus strains can promote
the growth of wheat and maize by producing IAA, ACC-
deaminase, and SD as well as PSE [54, 59, 60]. Some
Bt strains colonize plant roots and have plant growth-
promoting properties [3, 14, 25, 49, 61, 62]. Gomes etal.
[62] reported that IAA-producing Bt strain C25 isolated
from the cabbage plant (Brassica oleracea) significantly
enhanced the growth of Lactuca sativa in the greenhouse.
Similarly, Mishra etal. [25] reported that coinoculation of
Rhizobium leguminosarum-PR1 with IAA-producing Bt
strain KR1 significantly enhances the growth of pea and
lentil plants compared with inoculation of R. legumino-
sarum-PR1 alone. The coinoculation of Bradyrhizobium
japonicum-SB1 with Bt strain KR1 also promoted the
growth of soybean and increased shoot weight, nodule
number, root weight, root volume, and total biomass com-
pared to the rhizobial inoculation and control [49, 63].

Bacillus thuringiensis asaBiofertilizer andBiostimulator: aMini-Review oftheLittle-Known…
1 3
Furthermore, Bai etal. [61] reported that Bt strain NEB17
coinoculated with B. japonicum significantly improved
nodulation, growth, and yield parameters in soybean.
ACC is a precursor amino acid of the naturally occur-
ring compound ethylene, an important plant hormone
for natural development and stress response. This hor-
mone regulates many plant developmental processes [51].
There are various microorganisms that have ACC-deam-
inase, the enzyme that converts ACC to α-ketobutyrate
and ammonium [51, 64, 65]. ACC-deaminase has been
detected in different Bacillus spp., and can stimulate
root elongation during seed germination. Application of
ACC-deaminase-producing Bt strains is of great interest
to promoting growth in plants. Praça etal. [22] empha-
sized that effective colonization of Bt on the surface of
seedling roots can affect physiology of host plants and
that this bacterium may act as a growth promoter. Sharma
and Saharan [3] reported that the Bt strain SNKr10, which
was isolated from the spinach phyllosphere in different
regions of India, exhibited the ability to grow in high
concentrations of heavy metals. They also confirmed that
this strain showed significant ACC-deaminase activity
and that 100% of Vigna radiata seeds germinated in the
presence of SNKr10. Armada etal. [14] confirmed that
a mixture of arbuscular mycorrhizal fungal strains and
native Bt strains improved the growth of Lavandula den-
tata in drought conditions. They also verified that native
Bt strains isolated from the same soil used in the experi-
ment produced ACC-deaminase.
Bacillus thuringiensis asBiological Fertilizer
Biological fertilizer can be defined as a substance that
increases a plant’s mineral nutrient intake and transportation
when applied to seed. Biofertilizers contain viable microor-
ganisms that can be found on the plant surface or in the soil,
rhizosphere colonies, or plant interior [50, 51]. Several plant
growth-promoting rhizobacteria products are available on
the commercial market as biofertilizer products; however, as
far as I know, currently, there are no commercial Bt-based
plant growth-promoting products (Table1).
Although phosphate (P) is present in high amounts in
many types of soils, it is an important limiting factor of plant
growth. The reason plants only uptake P in low amounts is
that, although phosphate exists in the soil, it exists in the
undissolved form; plants can only uptake phosphate in two
dissolved forms, as monobasic or dibasic ions [51, 66].
Phosphate solubilization can be improved through vari-
ous mechanisms, such as hydrolysis or processes involving
enzymes like phosphatases and phytases [67]. Bacillus spp.
are known as one of the most significant phosphate-solubi-
lizing bacteria (PSB) [68, 69]. PSB convert the nonsoluble
phosphate to the soluble form by enzymatic activity [70].
Organic phosphorus in soil is mineralized by acid phos-
phatases and phytases that play important roles in dephos-
phorylation reactions [51, 71]. The most common mecha-
nism of PGPB regarding dissolution of phosphorus in the
rhizosphere is enhancement of nutritional ability to the host
plant [51, 72]. It was reported that Bt and B. subtilis strains
Fig. 1 Mode of action of Bt
as plant growth-promoting
bacterium (PGPB). ACC ACC-
deaminase, Bac bacteriocin, SD
siderophore, FG fengycin, IAA
indole-3-acetic acid, PSE phos-
phate solubilization enzymes,
VOCs volatile compounds
modified from Jouzani etal.
[49]
Sporulaon in
Bacillus thuringiensis
Phyllosphere
Rhizosphere
Spore
Plant pathogenic bacteria
Root pathogenic fungi
•Cry
•Spore
•Chinase
•Bacteriocin
•Fengycin
Root pathogen
Indirect growth effect
•Chinase
•Bacteriocin
•Fengycin
•VOCs
Direct growth effect
ACC –Deaminase
Siderophore
IAA
Phosphate Solubilizaon
ACC-Deaminase
Bac IAA
PSE
ChiSD
VOCs FG
Cry
Bt
Soil

U.Azizoglu
1 3
isolated from the wheat rhizosphere exhibited high PGPR
activity, including phosphate solubilization and biostimula-
tion [49, 73]. Raddadi etal. [51, 74] identified different acid
phosphatase genes based on sequence similarity in B. cereus
and 16 Bt strains. A 99% homology was found between the
B. cereus ATCC 14579T acid phosphatase gene and the
acid phosphatase genes in Bt strains [51, 74]. Almost all
living organisms require iron (Fe) as a cofactor for enzymes
[75–77]. Fe deficiency is an abiotic stress. Fe dissolution
is quite difficult, particularly in calcareous soil, and iron
deficiency is an important factor resulting in reduced crop
yield [78, 79]. Plants release soluble organic compounds that
Table 1 Plant growth-
promoting rhizobacteria-based
some commercial biofertilizers
[81–86]
Product name Microorganism Producer
Amnite A 100®Azotobacter sp.
Bacillus sp.
Rhizobium sp.
Chaetomium sp.
Pseudomonas sp.
Cleveland Biotech
Armour-Zen®B. cinerea
S. sclerotiorum Borty-Zen 2010 Ltd
Azo-Green A.brasilense Omega Ecotech Products India Private Limited
Azotobacterin®A. brasilense B-4485 JSC
Bactofil A10®A. brasilense
A. vinelandii
B. megaterium
B. polymyxa
P. fluorescens
Agro Bio Hungary kft
Bioativo®PGPR consortia Embrafos Ltda
Bioboots®D. acidovorans
Bradyrhizobium sp.
Brett-Young Seeds
CataPult™ Bacillus sp. Vanadis Bioscience Pty. Ltd.
Cell-Tech®Rhizobia Novozymes BioAg Inc
Ceres®P. fluorescens Biovitis
FZB24®B. subtilis FZB24 Abitep GmbH
Galltrol–A®A. radiobacter (strain K 84) AgBioChem
Inomix® Biostimulant B. polymyxa
B. subtilis LAB (Labiotech)
Micosat F® Cereali Streptomyces spp ST 60
B. subtilis BS 82
P. durus PD 76
Zoo Assets Srl
Nitragin Gold®Rhizobia Novozymes BioAg Inc
Nitrofix®Azospirillum sp Labiafam S.A
NitroGuard®Bacillus sp Mapleton Agri Biotec Pty Ltd
Nodulator®B. japonicum BASF Canada Inc.
Nogall™ A. radiobacter (strain K1026) Becker Underwood Pty. Ltd. RMB
Norbac 84C A. radiobacter (strain K84) New BioProducts, Inc.
Pix Plus B. cereus (strain BP01) + Mepi-
quat Chloride
Arysta LifeScience North America, LLC
Rhizocell GC B. amyloliquefaciens IT45 Lallemand Inc.
Rhizosum® K F. aurantia Biosym Technologies
Rhizosum® Micros Azospirillum sp. Biosym Technologies
Rhizosum® N A. vinelandii Biosym Technologies
Rhizosum® P B. megaterium Biosym Technologies
RhizoVital® 42 B. amyloliquefaciens FZB42 Abitep GmbH
Sonata®B. pumilus (strain QST 2808) AgraQuest, Inc.
Trichobacter®A. brasilense
A. chroococcum
B. megaterium
R. loti
Trichodex
TwinN®Diazotrophic bacteria Mapleton Agri Biotec Pty Ltd

Bacillus thuringiensis asaBiofertilizer andBiostimulator: aMini-Review oftheLittle-Known…
1 3
bind Fe3+ and aid in its dissolution [51]. Most plants have
an iron transport mechanism for iron uptake, including an
iron–siderophore complex [80].
Siderophores bind iron, resulting in iron deficiency to
plant pathogens. The result is improvement in plant growth
by the killing of plant pathogens through iron sequestration
[87]. Some rhizosphere bacteria produce siderophores via
the nonribosomal synthetic peptide pathway [88]. Sidero-
phore production is a characteristic of the Bacillus group of
bacteria, including B. cereus, B. anthracis, and Bt [51, 79,
89–91]. Bt strains produce metabolites that play key role
in plant development, such as chelators and phyto-sidero-
phores. Wilson etal. [91] indicated that Bt ATCC 33679
produced catecholate-type siderophore, bacillibactin, which
binds iron with a considerable high affinity. In Bt strains,
siderophores may function by supplying iron to the plant or
by controlling growth of phytopathogenic fungi due to iron
competition [51, 79].
Conclusions andFuture Perspectives
PGPB can directly stimulate plant growth by providing
plants with fixed nitrogen, soluble phosphates, and sidero-
phores [92]. PGPB also stimulate plant growth through the
production of metabolites such as IAA and ACC [92]. These
bacteria can indirectly stimulate plant growth by preventing
the development of plant pathogens [92, 93]. The insecti-
cidal and chitinolytic features of Bt strains are already well
known; hence, most Bt-related studies have focused on direct
effects against pests due to economically relevant losses in
agriculture [23]. There are also limited studies on Bt’s abil-
ity to compete with plant pathogens, endophytic coloniza-
tion, and plant growth-promoting properties. Though plant
interactions of Bt strains have received limited attention,
increasing emerging evidence suggests that Bt may play an
active role in plant growth. The resistance of Bt spores is
a suitable agent to enhance plant growth even in extreme
environments such as high temperatures, high salt concen-
trations, high heavy metal concentration, and presence of
organic toxicants. This feature is advantageous compared
to nonsporulating PGPB [74]. Previous studies on the plant
growth-promoting activity of Bt have shown promising
results. “Bt-based plant growth-promoting products will
likely be available in the near future as a new biofertilizer
on the market”[49].
Compliance With Ethical Standards
Conflict of interest No potential conflict of interest was reported by
the author.
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