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

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.

Influence of Lysogeny of Tectiviruses GIL01 and GIL16 on Bacillus thuringiensis Growth, Biofilm Formation, and Swarming Motility

“…Although B. thuringiensis is an insect pathogen, the ecology of this bacterium is still obscure (2,4). B. thuringiensis is usually referred to as a soildwelling microorganism, but it has also been isolated from different environmental habitats, including phylloplane, rhizosphere, endophytic, and aquatic environments (4,5). Due to this ubiquitous distribution, B. thuringiensis might have a hidden ecological role beyond a bacterium-insect interaction and pathogenicity.…”

“…These parasporal crystals are mainly composed of insecticidal toxin proteins, also known as Cry toxins, which are responsible for the entomopathogenic activity that has propelled B. thuringiensis to be the main biological agent used against insects representing agricultural pests (3). Although B. thuringiensis is an insect pathogen, the ecology of this bacterium is still obscure (2,4). B. thuringiensis is usually referred to as a soildwelling microorganism, but it has also been isolated from different environmental habitats, including phylloplane, rhizosphere, endophytic, and aquatic environments (4,5).…”

Infection of Tribolium castaneum with Bacillus thuringiensis: Quantification of Bacterial Replication within Cadavers, Transmission via Cannibalism, and Inhibition of Spore Germination

“…In the spore stage, Bt can endure unfavorable conditions for many years (18). When nutrients become available again, for example in the insect gut, spores can germinate instantly and colonize the host (11,16).…”

“…However, this bacterium is equipped with a diverse arsenal of virulence factors and other adaptations specifically designed for overcoming host defenses and growth and reproduction in cadavers (10,11), indicating that Bt coevolved with its insect hosts. Once ingested by the host, spores germinate in response to nutrients (12,13) and vegetative cells proliferate, contributing to tissue damage and host death (14)(15)(16).…”

“…In the spore stage, Bt can endure unfavorable conditions for many years (18). When nutrients become available again, for example in the insect gut, spores can germinate instantly and colonize the host (11,16).Numerous successful infections and disease phenotypes have been reported in laboratory experiments and in field applications; however, the ecology of Bt and its role in the environment still remain rather puzzling (11,19). Despite its obvious adaptations to insect hosts, Bt spores are found abundantly in diverse environments, such as soil, freshwater, the rhizosphere, and the phylloplane, where its hosts are not always present (11).…”