Why is genus bacillus difficult to kill

Not shown are additional strains that are not assigned to a group. There has been much debate surrounding the nomenclature of this group of bacteria. Recently, Carroll et al. Further division into subspecies would designate B. Whilst this method may aid clarity, it is yet to be seen whether it will be accepted by the wider scientific community. This is partly due to how deeply the current terminology is ingrained in published literature and day-to-day usage and partly because B.

Therefore, its importance is preserved with the distinction as a separate species. Strains of B. Differentiating between strains proved difficult until the development of variable number tandem repeat VNTR analysis Jackson et al. Like other endospore-forming bacteria, B. Sporulation occurs in the environment under nutrient-depleted conditions and spores are highly resistant to degradation by factors such as UV light, heat, desiccation, chemical disinfectants and antimicrobial compounds Swick et al.

Transmission to a host is usually via cutaneous, inhalational and gastrointestinal routes. Within the host, B. An unusual route of infection, via intravenous injection of heroin contaminated with B. Spores are able to persist in the environment for long periods of time. This was evidenced by the decades-long contamination of Gruinard Island in Scotland, which was exposed to aerosolised spores of virulent B.

Viable spores were still recoverable in the s, so extensive treatment of the land with formaldehyde was undertaken to reduce the number of spores to a safe level determined by safely grazing sheep on the land for 5 months with no fatalities Manchee et al. In contrast, B. Contamination of food with pathogenic B. However, virulence varies greatly, depending on the pathogen strain and host immune status Chang et al.

For example, B. The two forms of disease are caused by the production of different toxins. Cereulide is associated with emetic symptoms Agata et al. Unlike B. Since , reports of atypical B. These strains are defined by their B. Within the B. Despite their ability to cause anthrax-like disease, they are more closely related to other B. There are two variants of B. The Bcbva variants are clustered together, derived from a single branch and their nearest neighbor is B.

The atypical B. Other close neighbors to both variants include B. Figure 2 shows the distribution of atypical and Bcbva strains in relation to B.

Figure 2. Distribution of atypical and Bcbva strains in Clade 1 of the B. In humans, isolated cases of pulmonary anthrax-like disease caused by atypical B. Of the seven total cases, six were ultimately fatal Table 1. There may have been earlier incidents of inhalational anthrax-like disease caused by atypical B. The infections and fatalities occurred in immunocompetent men with no known risk factors.

However, they were all metal workers and may have been particularly at risk of infection via the inhalation route. Occupational hazards, including high numbers of spores in dust generated and damage to the respiratory tract, could increase their susceptibility to respiratory disease Antonini et al. Additionally, two cases of cutaneous anthrax-like disease caused by B. The first incident occurred in a non-metal worker in Florida with an unknown cause of infection that resulted in development of a characteristic anthrax eschar Marston et al.

The second case was a lab-acquired infection of B. At least six different strains of atypical B. Table 1. Atypical and Bcbva strains discussed in this review including their place and source of origin, anthrax-like virulence plasmid content and disease caused.

Anthrax-like disease associated with B. Most B. However, an unusual strain originally designated B. This low immune response may contribute to the high number of associated mortalities Zimmermann et al. Several studies have examined the virulence of atypical B. It has been shown to cause fatal anthrax-like disease in both immunocompromised and immunocompetent mice and in guinea-pigs, whilst one study demonstrated it is avirulent in New Zealand white rabbits Wilson et al.

Few studies have directly compared B. These studies described similar levels of virulence between B. However, many reports have included comparisons with previously published data, which generally suggests that B.

Table 2. As with B. For example, the calculated LD 50 values in outbred mice via the intranasal route were 3. The emerging atypical B. These are highly related to the anthrax virulence plasmids pXO1 and pXO2. One of the traits that separate atypical B. Several different combinations of chromosomal and plasmid DNA occur in B. The essential requirement for full virulence is the expression of both tripartite anthrax toxin and a capsule protein or polysaccharide.

Table 3. Plasmid possession, virulence factor expression and ability to cause anthrax-like disease for different strains of B.

Table 4. Genetic and phenotypic differences between strains of B. The anthrax toxin responsible for pathology and eventual fatality during the course of disease is a tripartite AB toxin comprised of protective antigen PA , lethal factor LF and edema factor EF. Expression of this toxin is essential for full virulence. The molecular mechanisms of anthrax toxin have been reviewed Young and Collier, ; Moayeri and Leppla, ; Friebe et al. Briefly, PA binds to receptors on the surface of host cells and is cleaved by furin-like proteases.

Truncated PA monomers assemble into heptamers and octamers, which embed into the cell membrane, creating a pre-pore formation. This causes an osmotic imbalance, which interferes with cell signaling pathways and renders white blood cells ineffective but is not cytotoxic Leppla, Presumably, expression of these genes results in production of toxin components homologous to those found in B. In one study, Marston et al. These data, coupled with the characteristic presentation of the disease [for example, formation of a black eschar Marston et al.

The second component required for full virulence is an extracellular capsule. As summarized in Table 3 , there are several capsules that can potentially be expressed by atypical B. The first is a hyaluronic acid HA capsule, which may be expressed by atypical B.

Functional genes for the hasACB operon have been identified in atypical B. Expression of this capsule was observed in atypical B. In addition to the HA capsule, several atypical strains are capable of producing a unique exopolysaccharide Bps capsule. Homologs of the genes are found in other species, including Streptococcus pyogenes , allowing gene functions to be putatively assigned Oh et al.

Atypical B. It encodes the capBCA genes, for expression of the polyglutamate capsule. This unusual proteinaceous capsule is required for full virulence in B. In addition to the Bcbva strains, one atypical strain isolated in the United States, B.

Two further strains, B. However, these strains have not yet been shown to express the polyglutamate capsule. When visualized by microscopy, the HA capsule can be observed forming a large protective layer around vegetative bacilli in strains of both atypical B.

In mouse models, for both atypical B. These data suggest that encapsulation with HA alone along with anthrax toxin expression is sufficient to enable B. Compared to the HA capsule, the Bps capsule is a less important virulence factor. When visualized by microscopy, the exopolysaccharide encapsulates the bacilli in a much thinner layer than the HA capsule Oh et al. In mouse models, deletion of the HA capsule from B. There are no known cases of anthrax-like disease in humans or other mammals caused by anthrax-toxin expressing B.

In addition to capsules and anthrax toxins, the emerging B. For example, the pBC plasmid in B. Each protein contains a PA binding domain that facilitates entry into the host cell. However, whilst the certhrax derives its toxicity from a mART domain, this is inactive in LF which possesses a functional metalloprotease domain Figure 3 ; Visschedyk et al.

Therefore, the two proteins cause toxicity via different mechanisms. The target for certhrax is vinculin which is part of the cytoskeletal complex and is involved in focal adhesion Simon and Barbieri, Certhrax demonstrated 60x greater toxicity against RAW Figure 3. Domain organization of lethal factor from B. This is inactivated in lethal factor by an insertion. Lethal factor derives its toxicity from a metalloprotease domainwhich is absent in certhrax.

The PA homolog in atypical B. Furthermore, PA2 is a weak virulence factor in mouse models compared to PA and is a poor antigen for immunization Oh et al. Whilst currently these virulence factors appear inconsequential, further structural or functional changes may enhance their significance as virulence factors in atypical B. Another structural feature is the S-layer or surface layer which can play a role in virulence.

Other virulence factors, such as hemolysis, motility and penicillin resistance are differentially expressed by atypical B. Further genetic elements unique to different B. Two genomic elements in B. AtxA is a global regulator of virulence factors and its complex matrix of interactions has been reviewed Fouet, AtxA is active in B.

At least 45 genes are known to be under the control of the PlcR-PapR regulon, regulating a number of virulence factors such as enterotoxins, hemolysins and various proteases Agaisse et al. It is proposed that the inactivated PlcR-PapR regulon and absence of accessory virulence factor expression contributes to the ability of B. All other species in the B. Wild type B. In the atypical B. Despite this, these strains are capable of causing anthrax-like disease.

The mechanisms for this are poorly understood and are an area of ongoing research. A functioning PlcR-PapR regulon may also adversely affect sporulation efficacy; a study by Mignot et al.

However, this was contradicted by a later study, which showed rapid and complete sporulation is achievable in B. The reason for this discrepancy has not been elucidated and may be due to experimental differences for example, the first study used homologous recombination to restore a functioning plcR gene on the chromosome, whereas the second study produced PlcR-PapR from a plasmid.

However, there is evidence to suggest AtxA and PlcR are active under different growth conditions Passalacqua et al. The full understanding of these inconsistencies and the precise mechanisms of both genetic regulatory systems could be an important area for future research.

AtxA2 is capable of upregulating Bps capsule production and, to a lesser extent, HA capsule and tripartite toxin production. Deletion of AtxA2 results in a reduction in virulence in mouse models and deletion of both orthologs results in a mutant that is unable to sporulate Scarff et al. For Bcbva strains, the PlcR-PapR regulon has been inactivated by a frameshift mutation, which is different than the nonsense mutation in B. Phenotypically, the Bcbva strains are consistent with an inactive PlcR-PapR regulon such as non-hemolytic and no phospholipase C activity.

Both atypical B. This phenotype is caused by mutations in flagella genes that are functional in the B. One outlier is Bcbva strain DRC, which has an early stop codon in the fliP gene, rendering it immotile Antonation et al. Whilst no motility genes were identified as under the control of the PlcR-PapR regulon by Gohar et al.

Further investigation is required to determine whether the PlcR-PapR regulon plays a role in the motility of these bacteria.

Any person thought to have been exposed to B. Methods used for identifying B. They should be simple to perform and possible to perform at the site of sampling [ 19 ]. Moreover, the assay should enable the detection of both spores and vegetative forms. Therefore, the real challenge is to optimize the B. Van Tongeren et al.

They isolated from one microbial sample multiple strains belonging to the B. The authors emphasized that there is a real challenge in rapid detection of anthrax bacilli from that type of microbiological material. Differentiating B. Public security requires shorter times of detection of anthrax contamination. Methods depending on antigen detection allow the result to be obtained within several hours [ 19 ] but may show a lack of sensitivity and specificity as well as crossreaction with other strains of the Bacillus genus, thus giving false positive results.

The nucleic acid based method e. So far, there is no method that can be considered reliable. Phages may have potential to be used in B. Most phage-based assays exploit the phage [ 77 ]. The phage test is a standard method for identification of B.

This routine identification test takes 2—4 days [ 5 ]. The presence of a polypeptide capsule inhibiting B.

The synthesis of the capsule blocks the GamR receptor on the bacterial cell surface responsible for phage binding [ 79 ]. Detection of B. The method allows for direct detection of B. Spores are refractory to phage because they do not show the GamR on their surface; therefore spores may be detected only in the germinating state. A higher phage titer gives a stronger detection signal. Abshire et al. It may indicate that natural phage resistance of B.

Kan et al. They observed that the gene product p23 of the Wip1 bacteriophage is a receptor-binding protein on the phage surface. The presence of this protein and narrow host range of the Wip1 phage may provide new tools for the identification of B. The anthrax spores should be detected before the occurrence of symptoms, especially by the use of continuous monitoring of spore content in the air [ 81 ].

The system should be sensitive and selective to avoid false alarms of bioterrorist attack. Brigati et al. This method is not ideal due to the possibility of clones crossreacting to other species belonging to the Bacillus genus.

Also, sensors that use filamentous phages may be useful in B. Applying filamentous phages in these methods is justified for these phages are suspected to be the most stable nucleoproteins in nature.

This method enabled in situ detection. Schuch et al. The detection is based on light emission in the presence of luciferin and luciferase and the release of ATP from lysed bacterial cells.

It is based on the ability of PlyG to kill germinating spores and is applied using a hand-held luminometer. Moreover, a method based on the binding of B. Shabani et al. It is based on the immobilization of the phage and its high specificity to B. Therefore, therapeutic intervention should be initiated as early as possible [ 89 ]. The antimicrobial chemotherapy recommended for the treatment of patients with inhalational anthrax is effective, but long-term therapy may cause antibiotic resistance in B.

Drugs used for postexposure prophylaxis are penicillin G, amoxicillin, doxycycline, ciprofloxacin, and ofloxacin administered for 60 days or more [ 24 ]. Penicillin has been considered the drug of choice, and it is very rare that resistance to this antibiotic is found in naturally occurring strains [ 9 ].

Ciprofloxacin, penicillin, and doxycycline are recommended for the treatment of humans and as prophylactics after exposure to the spores [ 91 ].

Many in vitro studies show that B. However, the organism is resistant to cephalosporins, trimethoprim, and sulphonamides. Cavallo et al. All of them were resistant to cotrimoxazole but susceptible to antibiotics such as doxycycline, vancomycin, clindamycin, rifampicin, imipenem, or teicoplanin.

As a result of long-term antibiotic treatment B. In the case of B. We suppose that, due to problems with antibiotic treatments and improvement in bacterial drug resistance, these strains may be used as potential biowarfare agents. Therefore, for public safety, there must be known an agent to which these bacteria are susceptible.

Treatment with antibiotics beginning 1 day after the exposure to an aerosol with anthrax spores can protect against death. However, optimal protection isprovided bycombining antibiotics with vaccination. Vaccination is the best form of mass protection. The first anthrax animal vaccine was developed by Pasteur in Pasteur attenuated B.

Human vaccines emerged in the middle of the 20th century [ 9 ]. Human anthrax vaccine anthrax vaccine adsorbed, AVA , currently licensed for use in the United States and the United Kingdom, consists primarily of protective antigen PA absorbed onto aluminum hydroxide [ 96 , 97 ]. This vaccine was tested in guinea pigs, rabbits, and rhesus macaques by Fellows et al. The currently available vaccines have a chemically complicated composition and it is believed that they are insufficiently purified [ ].

AVA was originally prepared for individuals in high-risk occupations, like veterinarians, farmers, and laboratory personnel working with B. The use of appropriate animal models provides better understanding of the pathogenesis of human anthrax and the development of appropriate methods of prevention and treatment.

Rabbits and nonhuman primates NHPs , for example, rhesus macaques, are commonly used as animal models of inhalational anthrax.

The pathological changes observed in rabbits and NHPs are similar to those observed in humans [ ]. Savransky et al. Guinea pigs have alsobeen used in anthrax vaccine studies. Another popular animal model used to test the sensitivity to virulent B. The mouse model is useful in studies on host resistance to anthrax and on pathogenesis, how the agent establishes infection in the host, and characteristics of the spore and vegetative bacilli. It is known that different mouse strains have various sensitivities to infection by both B.

Interestingly, the susceptibility of mouse strains to lethal toxin LT does not necessarily correlate with its susceptibility to infection. The rat and hamster, meanwhile, are important animal models for understanding the B. The first phage therapy studies on B. The B. The animals were inoculated intraperitoneally with 0. The authors found that, only in the group inoculated with B. The results of this study also showed that only the phage, in high titer, quickly and permanently lysed the strain of anthrax used in the experiments.

Phages may be applied in phage therapy in the case of B. For better effectiveness of therapy, phages active against B. In this case phages may bind to the cell surface receptor of the bacteria and destroy these dangerous bacteria [ 54 , ]. Besides the whole phage particles, also endolysins can be applied in the therapy of anthrax. Endolysins are enzymes encoded in the bacteriophage genome and specifically lyse the peptidoglycan of the bacterial cell wall during the phage lytic cycle [ ].

The enzymes may create new opportunities for the construction and production of genetically engineered enzymes for bacteria elimination, biocontrol, and experimental therapies. The endolysin PlyG isolated from the phage may be applied against B. Susceptibility of B. The authors decided to use isolates of streptomycin-resistant B. Lytic activity of lysin against this strain was the same as in the case of B. In the study of Schuch et al. The application of lysin significantly rescued mice in comparison to untreated animals.

However, both Novobiocin 3. What is more is that the authors have demonstrated that RSVF1 strain that became resistant to the phage remains sensitive to PlyG. In bacterial culture, application of lysin caused morphological changes of bacterial cells and ultimately led to cell lysis. Also, purified lysin encoded by the Tsamsa phage is suggested to be used in B. Inal suggested that in the case of anthrax infections lysin should be applied as soon as possible, before the lethal level of toxin is reached [ 32 ].

Porter et al. The enzyme has muramidase activity, whereas PlyG is an amidase [ ]. It is presumed that this lysin may be a new defensive tool in the face of bioterrorism danger. Lysins have some advantages over phages as the capsule is not an obstacle for PlyG to access the bacterial cell wall and may destroy encapsulated forms of bacilli.

They show high specificity, not disturbing another bacterial species, and strong enzymatic activity; moreover the enzymes allow destruction of bacteria within seconds or minutes [ ].

In in vivo experiments it was showed that PlyG applied in mice intraperitoneally did not cause evident toxic effects [ 86 ]. Another prevalence of these enzymes is that the resistance to them is induced rarely or not at all in comparison with whole phage particles.

What is more is that it was observed that purified lysin isolated from Tsamsa phage was characterized by broader lytic activity than it was observed in the case of phage host range [ 56 ]. This phenomenon may be useful for biocontrol and decontamination not only in the case of B.

Sozhamannan et al. Similarly, Inal stated that a phage cocktail which has the ability to lyse most B. Also, Porter et al. It was suggested that phages, especially a combination of different phages, may be used in a spray form applied to skin and clothes surface and into the respiratory tract [ 86 ]. Although the use of phagesagainst B. Anthrax spores are not metabolically active, and they may be inactivated by physical methods gamma irradiation, ultraviolet light, and high pressure that are not safe for humans [ 71 , ].

There is a need to find a method of disinfection that is highly effective and safe. This form of B. The spore cortex is protected by a proteinous coat against, for example, lysozyme. In the germinating state the porosity of coat is increased even during 10 minutes of incubation in conditions inducing germination [ 86 ]. Fu et al. Application of phages isolated from soil in the aerosol form to germinated spores of the B. But using this strain guarantees safety—especially laboratory personnel who work on the B.

As was observed, phages that are used against anthrax spores should be resistant to harsh environmental conditions, for example, dryness, ultraviolet radiation, extreme temperatures, and bodily fluids,to maintain ability to kill bacteria [ 71 ].

This feature would be important especially in the case of the disinfection application of spores because of their high resistance to different factors. There may exist the possibility to use other pathogens belonging to the B. Bacteriophage typing may be useful for detecting food contamination with B.

The FDA approved the use of bacteriophages in order to guarantee food disinfection [ , ]. There is a possibility and permission to apply bacteriophages providing food safety.

To inhibit B. Bacteriophages infecting B. This high specificity may constitute a disadvantage in using phages against foodborne pathogens, due to the complex composition of bacteria that contaminate food. A broad spectrum of inhibition of bacterial growth has been shown for Bcv3 phage. It lysed bacteria belonging to the B. New phages with proven activity against B.

But it is extremely important that in their genomes phages do not encode genes responsible for lysogeny, toxin production, and genes affecting the pathogenicity of bacteria and antibiotic resistance [ 72 ]. The lack of them makes phage application safe for humans and increases phage application as a strategy of biocontrol of bacteria belonging to the B.

Endolysins may be successfully applied in the case of B. For example, the LysB4 lysin isolated from the B4 bacteriophage was reported as the first endopeptidase among endolysins obtained from the B. Interestingly, the enzyme not only shows broad lytic activity against B. This feature enables the enzyme to be an effective antibacterial agent active especially against foodborne pathogens.

Yuan et al. The authors showed that this agent may be potentially used for disinfection purposes, had high temperature resistance, and showed a broad lytic spectrum low lytic activity against B. High thermostability may be useful in lysin application against food poisoning caused by B. This endolysin may also be considered in anthrax treatment. The lytic protein E33L that caused the lysis of B. It was an N-acetylmuramoyl-L-alanine amidase, active against both B.

What is more is that the protein was active against B. An advantage of this agent is that the enzyme does not seem to be degradable by bacterial proteases, and furthermore it showed significantly higher lytic activity than Bacillus -phage-encoded endolysins. The biothreat danger is a real possibility, and regardless of how the attack occurs through water, air, mail, food contamination, soil, insects, and public transport people should have a foolproof tool for rapid detection and identification and a possibility to treat patients from these dangerous probably drug-resistant pathogens.

The control of B. We suggest that phages whole particles or their purified endolysins may constitute a good prospect in this area. The past two decades have proved that bioterrorism is a real threat which needs to be properly controlled. Recent developments in phage therapy confirm that it may provide a reliable countermeasure preventing serious consequences of a terrorist attack using deadly bacteria, especially those resistant to antibiotics.

Phage-mediated elimination of Bacillus cereus group bacteria, especially B. The authors declare that there is no conflict of interests regarding the publication of this paper.

This is an open access article distributed under the Creative Commons Attribution License , which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Article of the Year Award: Outstanding research contributions of , as selected by our Chief Editors. Read the winning articles. Journal overview. Special Issues. Received 30 Apr Revised 25 Jun Accepted 25 Jul Published 28 Aug Abstract Anthrax is an infectious fatal disease with epidemic potential.

Introduction Shortly after the September 11 terrorist attacks using captured planes, letters containing anthrax spores were posted to news media and the US Senate. Pathogenesis of B. Epidemiology of B. Inability to infect encapsulated cells [ 4 ].

Infects all tested nonencapsulated strains [ 50 ], but does not infect other Bacillus strains. Preparing bioluminescent reporter bacteriophage for B. Encodes a fosfomycin resistance gene [ 58 ].

Not active against B. Identification of B. AP50 Lytic Belongs to Tectiviridae [ 55 ], isolated from soil. Infects only B. Does not lyse strains belonging to different Bacillus spp. The lysogenic mutant AP50c is characterized by very high killing efficiency [ 63 ].

Narrow host range [ 64 ]. It does not infect the B. Probable use in therapy of anthrax. It is suggested to be used in typing and biocontrol of B.

Fah Lytic Belongs to Siphoviridae [ 66 ]. Narrower lytic spectrum. Worm intestinal phage 1 Wip1 Lytic Belongs to Tectiviridae [ 67 ]. It was isolated from the intestinal tract of Eisenia fetida worms. Exhibits a narrow host range highly specific to B. Does not infect the B.

Potentially useful diagnostic tool for efficient identification of B. Giraffe phage? Belongs to Siphoviridae isolated from giraffe faeces in a zoo Long Island [ 68 ]. This phage shows a rapid lysis phenotype. Lyses the ciprofloxacin-resistant B. Possible use in therapy when infection is caused by antibiotic-resistant B. F7 Lytic Isolated from bovine faeces. Belongs to Siphoviridae [ 51 ].

F9 Lytic Isolated from bovine faeces. Belongs to Siphoviridae. Has the largest sequenced genomes of Bacillus siphovirus. Purified endolysin encoded in genome of this phage has broader spectrum than the phage. The largest siphovirus known to infect Bacillus strains [ 54 ]. Infects also strains belonging to B. Did not lyse the B. Moderate specificity to B.

Use of purified phage endolysin in B. Table 1. Bacillus anthracis phages and their characteristics. Figure 1. In addition, blood cultures should be repeated to ensure clearance of bacteremia. CT scans maybe helpful in detecting recurrent emboli in cases of endocarditis or in detecting loculated infections. Although, a non-specific parameter, sedimentation rate or C-reactive protein maybe helpful especially in the setting of endocarditis, osteomyelitis, or other deep seated infections.

In certain settings wherein adequate debridement has been performed, persistent isolation of Bacillus species is an indication for repeat susceptibility testing to ensure that the organism remains sensitive to the antibiotic being administered.

The main preventative measure for gastroenteritis caused by B. The heat-resistant spores of B. Flash frying or brief rewarming of rice before serving is not adequate to destroy the preformed, heat-stable toxin.

Biocidal agents to decontaminate Bacillus are being investigated. Animal studies demonstrated the protective and therapeutic effect of BCTP in vivo. Decontamination of Bacillus spores prior to or after exposure effectively reduce the morbidity and mortality from B. Bacillus cereus phage typing as an epidemiological tool in outbreaks of food poisoning.

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