Efficient Colonization of the Bean Bug Riptortus pedestris by an Environmentally Transmitted Burkholderia Symbiont

Across animals and plants, numerous metabolic and defensive adaptations are a direct consequence of symbiotic associations with beneficial microbes. Explaining how these partnerships are maintained through evolutionary time remains one of the central challenges within the field of symbiosis research. While genome erosion and co-cladogenesis with the host are well-established features of symbionts exhibiting intracellular localization and transmission, the ecological and evolutionary consequences of an extracellular lifestyle have received little attention, despite a demonstrated prevalence and functional importance across many host taxa. Using insect-bacteria symbioses as a model, we highlight the diverse routes of extracellular symbiont transfer. Extracellular transmission routes are unified by the common ability of the bacterial partners to survive outside their hosts, thereby imposing different genomic, metabolic and morphological constraints than would be expected from a strictly intracellular lifestyle. We emphasize that the evolutionary implications of symbiont transmission routes (intracellular versus extracellular) do not necessarily correspond to those of the transmission mode (vertical versus horizontal), a distinction of vital significance when addressing the genomic and physiological consequences for both host and symbiont.

Section: Transition From a Free-living State To Symbiosismentioning

confidence: 99%

An out-of-body experience: the extracellular dimension for the transmission of mutualistic bacteria in insects

et al. 2015

“…In the laboratory, we established a gut symbiontharboring (symbiotic) insect line and a symbiont-deficient (aposymbiotic) insect line by controlling the feeding of a solution containing in vitro-cultured Burkholderia cells to early Riptortus nymphs. A comparison of these two insect lines has revealed the effects of Burkholderia symbionts on host biology (11)(12)(13). Furthermore, Burkholderia symbionts are cultivatable in vitro and genetically manipulable (11)(12)(13), which has allowed the elucidation of several symbiotic factors for establishing associations using a genetically manipulated Burkholderia symbiont (14 -17).…”

mentioning

confidence: 99%

“…A comparison of these two insect lines has revealed the effects of Burkholderia symbionts on host biology (11)(12)(13). Furthermore, Burkholderia symbionts are cultivatable in vitro and genetically manipulable (11)(12)(13), which has allowed the elucidation of several symbiotic factors for establishing associations using a genetically manipulated Burkholderia symbiont (14 -17). In addition to the recognized features mentioned above, a unique advantage of this Riptortus-Burkholderia system is that a large number of naïve gut symbionts can be isolated from the Riptortus host, enabling the direct comparison of symbiotic and cultured Burkholderia cells using biochemical approaches.…”

mentioning

confidence: 99%

Insect Gut Symbiont Susceptibility to Host Antimicrobial Peptides Caused by Alteration of the Bacterial Cell Envelope

Son

Journal of Biological Chemistry

et al. 2015

Background:The elucidation of molecular changes of symbionts is important for understanding symbiotic adaptation. Results: Insect gut symbionts are highly susceptible to host immunity because of dramatic cell envelope changes. Conclusion: Cell envelope changes in gut symbionts are required for successful symbiosis with hosts. Significance: Biochemical analyses of intact gut symbionts revealed a novel mechanism of gut symbiosis.

“…Given its free-living nature, the Burkholderia symbiont is cultivable on standard microbiological media and thus can be genetically manipulated. The genetically manipulated symbiont strains can then easily be introduced into the host insects via feeding (5)(6)(7)(8). Because newly hatched R. pedestris nymphs are aposymbiotic, symbiotic and aposymbiotic insect lines are easily established by controlling the feeding of the Burkholderia cells (6,9,10).…”

mentioning

confidence: 99%

Purine Biosynthesis, Biofilm Formation, and Persistence of an Insect-Microbe Gut Symbiosis

Kwon

et al. 2014

Appl Environ Microbiol

cThe Riptortus-Burkholderia symbiotic system is an experimental model system for studying the molecular mechanisms of an insect-microbe gut symbiosis. When the symbiotic midgut of Riptortus pedestris was investigated by light and transmission electron microscopy, the lumens of the midgut crypts that harbor colonizing Burkholderia symbionts were occupied by an extracellular matrix consisting of polysaccharides. This observation prompted us to search for symbiont genes involved in the induction of biofilm formation and to examine whether the biofilms are necessary for the symbiont to establish a successful symbiotic association with the host. To answer these questions, we focused on purN and purT, which independently catalyze the same step of bacterial purine biosynthesis. When we disrupted purN and purT in the Burkholderia symbiont, the ⌬purN and ⌬purT mutants grew normally, and only the ⌬purT mutant failed to form biofilms. Notably, the ⌬purT mutant exhibited a significantly lower level of cyclic-di-GMP (c-di-GMP) than the wild type and the ⌬purN mutant, suggesting involvement of the secondary messenger c-di-GMP in the defect of biofilm formation in the ⌬purT mutant, which might operate via impaired purine biosynthesis. The host insects infected with the ⌬purT mutant exhibited a lower infection density, slower growth, and lighter body weight than the host insects infected with the wild type and the ⌬purN mutant. These results show that the function of purT of the gut symbiont is important for the persistence of the insect gut symbiont, suggesting the intricate biological relevance of purine biosynthesis, biofilm formation, and symbiosis.