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Bacillus thuringiensis Is an Environmental Pathogen and Host-Specificity Has Developed as an Adaptation to Human-Generated Ecological Niches.

Argôlo-Filho RC, Loguercio LL - Insects (2013)

Bottom Line: Bacillus thuringiensis (Bt) has been used successfully as a biopesticide for more than 60 years.As a result, we propose an integrated view to account for Bt ecology.These conditions provided the selective pressure for development of new hosts for pathogenic interactions, and so, host specificity of certain strains.

View Article: PubMed Central - PubMed

Affiliation: Department of Biological Sciences, State University of Santa Cruz (UESC), Rod, Ilhéus-Itabuna, Km-16, Ilhéus-BA 45662-900, Brazil. ronaldoargolo@yahoo.com.br.

ABSTRACT
Bacillus thuringiensis (Bt) has been used successfully as a biopesticide for more than 60 years. More recently, genes encoding their toxins have been used to transform plants and other organisms. Despite the large amount of research on this bacterium, its true ecology is still a matter of debate, with two major viewpoints dominating: while some understand Bt as an insect pathogen, others see it as a saprophytic bacteria from soil. In this context, Bt's pathogenicity to other taxa and the possibility that insects may not be the primary targets of Bt are also ideas that further complicate this scenario. The existence of conflicting research results, the difficulty in developing broader ecological and genetics studies, and the great genetic plasticity of this species has cluttered a definitive concept. In this review, we gathered information on the aspects of Bt ecology that are often ignored, in the attempt to clarify the lifestyle, mechanisms of transmission and target host range of this bacterial species. As a result, we propose an integrated view to account for Bt ecology. Although Bt is indeed a pathogenic bacterium that possesses a broad arsenal for virulence and defense mechanisms, as well as a wide range of target hosts, this seems to be an adaptation to specific ecological changes acting on a versatile and cosmopolitan environmental bacterium. Bt pathogenicity and host-specificity was favored evolutionarily by increased populations of certain insect species (or other host animals), whose availability for colonization were mostly caused by anthropogenic activities. These have generated the conditions for ecological imbalances that favored dominance of specific populations of insects, arachnids, nematodes, etc., in certain areas, with narrower genetic backgrounds. These conditions provided the selective pressure for development of new hosts for pathogenic interactions, and so, host specificity of certain strains.

No MeSH data available.


Related in: MedlinePlus

Simplified view of complex lifestyle of Bacillus thuringiensis (Bt) in different environmental niches. Vertebrates and invertebrates are only examples of a much wider range of possible hosts. The soil (1) is usually the largest reservoir of Bt, because it receives the highest amount of propagules from other environments. From it, Bt can colonize the rhizosphere (2) feeding on roots exudates. If eaten by soil invertebrates such as worms, insects and nematodes (3), Bt can infect in a paratenic way, colonizing the gut and feces, or in a pathogenic way, killing the host and growing in the cadaver. Thus Bt is re-introduced into the environment through these two ways. Rhizosphere colonization favors endophytic colonization (4) which protects the plant from some herbivores, while helps Bt to proliferate in plant tissues and infecting herbivores in paratenic (5) or pathogenic (6) ways. Besides endophytism, Bt can reach the surface of the plants from the soil due to the germination process, by splashes of rain water, and through the feces of animals that carry it, such as insects and birds (7). The infected fallen leaves can re-introduce Bt in soil and water (8). The rain may also carry the Bt to water bodies from soil and plants (9). In water the Bt can infect and proliferate in vertebrates or invertebrates and persiste in this environment by associating with substrates as aquatic plants and sediments (10). Faeces from animals that feed on contaminated plants or insects can serve as a source of nutrients for Bt growth, and they can act as a source of infection for coprophagous (11). It is known that ticks and mites are also Bt hosts (12), but the natural mechanism of infection is unknown. It is possible to observe a wide range of strategies for Bt occupy different niches and disperse in environment with or without causing disease.
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insects-05-00062-f001: Simplified view of complex lifestyle of Bacillus thuringiensis (Bt) in different environmental niches. Vertebrates and invertebrates are only examples of a much wider range of possible hosts. The soil (1) is usually the largest reservoir of Bt, because it receives the highest amount of propagules from other environments. From it, Bt can colonize the rhizosphere (2) feeding on roots exudates. If eaten by soil invertebrates such as worms, insects and nematodes (3), Bt can infect in a paratenic way, colonizing the gut and feces, or in a pathogenic way, killing the host and growing in the cadaver. Thus Bt is re-introduced into the environment through these two ways. Rhizosphere colonization favors endophytic colonization (4) which protects the plant from some herbivores, while helps Bt to proliferate in plant tissues and infecting herbivores in paratenic (5) or pathogenic (6) ways. Besides endophytism, Bt can reach the surface of the plants from the soil due to the germination process, by splashes of rain water, and through the feces of animals that carry it, such as insects and birds (7). The infected fallen leaves can re-introduce Bt in soil and water (8). The rain may also carry the Bt to water bodies from soil and plants (9). In water the Bt can infect and proliferate in vertebrates or invertebrates and persiste in this environment by associating with substrates as aquatic plants and sediments (10). Faeces from animals that feed on contaminated plants or insects can serve as a source of nutrients for Bt growth, and they can act as a source of infection for coprophagous (11). It is known that ticks and mites are also Bt hosts (12), but the natural mechanism of infection is unknown. It is possible to observe a wide range of strategies for Bt occupy different niches and disperse in environment with or without causing disease.

Mentions: For a microorganism to be considered pathogenic, it must display some specific features and abilities such as (i) occupy the same host’s niche; (ii) persist in it; (iii) overcome the host defenses; and (iv) colonize its tissues and/or impair its physiology [83]. For this, the pathogens have the so called virulence factors, which provide the mechanisms by which they can overcome the host resistance and cause disease. The life cycle of an environmental pathogen may involve different habitats, hosts and niches with different availability of nutrients, which makes it metabolically versatile [11]. This versatility is required for the movement of the pathogen through different niches and different hosts [84]. In this regard, Bt has several factors (such as enzymes, toxins, antimicrobial compounds and structural proteins) that allow dwelling in a diverse array of environments and reaching various target organisms/hosts (Figure 1), turning this bacterium into a well-succeeded environmental pathogen [1,6,18,34,36].


Bacillus thuringiensis Is an Environmental Pathogen and Host-Specificity Has Developed as an Adaptation to Human-Generated Ecological Niches.

Argôlo-Filho RC, Loguercio LL - Insects (2013)

Simplified view of complex lifestyle of Bacillus thuringiensis (Bt) in different environmental niches. Vertebrates and invertebrates are only examples of a much wider range of possible hosts. The soil (1) is usually the largest reservoir of Bt, because it receives the highest amount of propagules from other environments. From it, Bt can colonize the rhizosphere (2) feeding on roots exudates. If eaten by soil invertebrates such as worms, insects and nematodes (3), Bt can infect in a paratenic way, colonizing the gut and feces, or in a pathogenic way, killing the host and growing in the cadaver. Thus Bt is re-introduced into the environment through these two ways. Rhizosphere colonization favors endophytic colonization (4) which protects the plant from some herbivores, while helps Bt to proliferate in plant tissues and infecting herbivores in paratenic (5) or pathogenic (6) ways. Besides endophytism, Bt can reach the surface of the plants from the soil due to the germination process, by splashes of rain water, and through the feces of animals that carry it, such as insects and birds (7). The infected fallen leaves can re-introduce Bt in soil and water (8). The rain may also carry the Bt to water bodies from soil and plants (9). In water the Bt can infect and proliferate in vertebrates or invertebrates and persiste in this environment by associating with substrates as aquatic plants and sediments (10). Faeces from animals that feed on contaminated plants or insects can serve as a source of nutrients for Bt growth, and they can act as a source of infection for coprophagous (11). It is known that ticks and mites are also Bt hosts (12), but the natural mechanism of infection is unknown. It is possible to observe a wide range of strategies for Bt occupy different niches and disperse in environment with or without causing disease.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4592628&req=5

insects-05-00062-f001: Simplified view of complex lifestyle of Bacillus thuringiensis (Bt) in different environmental niches. Vertebrates and invertebrates are only examples of a much wider range of possible hosts. The soil (1) is usually the largest reservoir of Bt, because it receives the highest amount of propagules from other environments. From it, Bt can colonize the rhizosphere (2) feeding on roots exudates. If eaten by soil invertebrates such as worms, insects and nematodes (3), Bt can infect in a paratenic way, colonizing the gut and feces, or in a pathogenic way, killing the host and growing in the cadaver. Thus Bt is re-introduced into the environment through these two ways. Rhizosphere colonization favors endophytic colonization (4) which protects the plant from some herbivores, while helps Bt to proliferate in plant tissues and infecting herbivores in paratenic (5) or pathogenic (6) ways. Besides endophytism, Bt can reach the surface of the plants from the soil due to the germination process, by splashes of rain water, and through the feces of animals that carry it, such as insects and birds (7). The infected fallen leaves can re-introduce Bt in soil and water (8). The rain may also carry the Bt to water bodies from soil and plants (9). In water the Bt can infect and proliferate in vertebrates or invertebrates and persiste in this environment by associating with substrates as aquatic plants and sediments (10). Faeces from animals that feed on contaminated plants or insects can serve as a source of nutrients for Bt growth, and they can act as a source of infection for coprophagous (11). It is known that ticks and mites are also Bt hosts (12), but the natural mechanism of infection is unknown. It is possible to observe a wide range of strategies for Bt occupy different niches and disperse in environment with or without causing disease.
Mentions: For a microorganism to be considered pathogenic, it must display some specific features and abilities such as (i) occupy the same host’s niche; (ii) persist in it; (iii) overcome the host defenses; and (iv) colonize its tissues and/or impair its physiology [83]. For this, the pathogens have the so called virulence factors, which provide the mechanisms by which they can overcome the host resistance and cause disease. The life cycle of an environmental pathogen may involve different habitats, hosts and niches with different availability of nutrients, which makes it metabolically versatile [11]. This versatility is required for the movement of the pathogen through different niches and different hosts [84]. In this regard, Bt has several factors (such as enzymes, toxins, antimicrobial compounds and structural proteins) that allow dwelling in a diverse array of environments and reaching various target organisms/hosts (Figure 1), turning this bacterium into a well-succeeded environmental pathogen [1,6,18,34,36].

Bottom Line: Bacillus thuringiensis (Bt) has been used successfully as a biopesticide for more than 60 years.As a result, we propose an integrated view to account for Bt ecology.These conditions provided the selective pressure for development of new hosts for pathogenic interactions, and so, host specificity of certain strains.

View Article: PubMed Central - PubMed

Affiliation: Department of Biological Sciences, State University of Santa Cruz (UESC), Rod, Ilhéus-Itabuna, Km-16, Ilhéus-BA 45662-900, Brazil. ronaldoargolo@yahoo.com.br.

ABSTRACT
Bacillus thuringiensis (Bt) has been used successfully as a biopesticide for more than 60 years. More recently, genes encoding their toxins have been used to transform plants and other organisms. Despite the large amount of research on this bacterium, its true ecology is still a matter of debate, with two major viewpoints dominating: while some understand Bt as an insect pathogen, others see it as a saprophytic bacteria from soil. In this context, Bt's pathogenicity to other taxa and the possibility that insects may not be the primary targets of Bt are also ideas that further complicate this scenario. The existence of conflicting research results, the difficulty in developing broader ecological and genetics studies, and the great genetic plasticity of this species has cluttered a definitive concept. In this review, we gathered information on the aspects of Bt ecology that are often ignored, in the attempt to clarify the lifestyle, mechanisms of transmission and target host range of this bacterial species. As a result, we propose an integrated view to account for Bt ecology. Although Bt is indeed a pathogenic bacterium that possesses a broad arsenal for virulence and defense mechanisms, as well as a wide range of target hosts, this seems to be an adaptation to specific ecological changes acting on a versatile and cosmopolitan environmental bacterium. Bt pathogenicity and host-specificity was favored evolutionarily by increased populations of certain insect species (or other host animals), whose availability for colonization were mostly caused by anthropogenic activities. These have generated the conditions for ecological imbalances that favored dominance of specific populations of insects, arachnids, nematodes, etc., in certain areas, with narrower genetic backgrounds. These conditions provided the selective pressure for development of new hosts for pathogenic interactions, and so, host specificity of certain strains.

No MeSH data available.


Related in: MedlinePlus