Insecticide-Degrading <i>Burkholderia</i> Symbionts of the Stinkbug Naturally Occupy Various Environments of Sugarcane Fields in a Southeast Island of Japan

Abstract

The stinkbug Cavelerius saccharivorus, which harbors Burkholderia species capable of degrading the organophosphorus insecticide, fenitrothion, has been identified on a Japanese island in farmers’ sugarcane fields that have been exposed to fenitrothion. A clearer understanding of the ecology of the symbiotic fenitrothion degraders of Burkholderia species in a free-living environment is vital for advancing our knowledge on the establishment of degrader-stinkbug symbiosis. In the present study, we analyzed the composition and abundance of degraders in sugarcane fields on the island. Degraders were recovered from field samples without an enrichment culture procedure. Degrader densities in the furrow soil in fields varied due to differences in insecticide treatment histories. Over 99% of the 659 isolated degraders belonged to the genus Burkholderia. The strains related to the stinkbug symbiotic group predominated among the degraders, indicating a selection for this group in response to fenitrothion. Degraders were also isolated from sugarcane stems, leaves, and rhizosphere in fields that were continuously exposed to fenitrothion. Their density was lower in the plant sections than in the rhizosphere. A phylogenetic analysis of 16S rRNA gene sequences demonstrated that most of the degraders from the plants and rhizosphere clustered with the stinkbug symbiotic group, and some were identical to the midgut symbionts of C. saccharivorus collected from the same field. Our results confirmed that plants and the rhizosphere constituted environmental reservoirs for stinkbug symbiotic degraders. To the best of our knowledge, this is the first study to investigate the composition and abundance of the symbiotic fenitrothion degraders of Burkholderia species in farmers’ fields.

Insecticide applications to soil contribute to the development of Burkholderia mediating insecticide resistance in stinkbugs

“…was identified (Tago et al . ); the farmers' sugarcane fields had been regularly treated with fenitrothion for years, and up to 10 5 CFU/g soil of fenitrothion degraders, most of which were assigned to the SBE group, were present in soils of the sugarcane fields. These results observed in the microcosm and field experiments suggest that the degraders placed in the SBE group could quickly increase under the selective constraints.…”

“…The dominance of the SBE group among the degraders was consistent with the situation in soils of farmers' sugarcane fields, where the stinkbug C. saccharivorus harbouring fenitrothion degraders belonging to Burkholderia spp. was identified (Tago et al 2015); the farmers' sugarcane fields had been regularly treated with fenitrothion for years, and up to 10 5 CFU/g soil of fenitrothion degraders, most of which were assigned to the SBE group, were present in soils of the sugarcane fields. These results observed in the microcosm and field experiments suggest that the degraders placed in the SBE group could quickly increase under the selective constraints.…”

Specifics of pesticides effects on the phytopathogenic bacteria

“…Plants are a source of microorganisms-destructors insecticides, especially rhyzosphere. Burkholderia genera strains with the ability to degradation of organic phosphorus fenitrotion insecticide, which are genetically related with representatives of soil and phylosphere microflora, was isolated and identified out of resistant insects [26]. In this case resulting in phytophage resistance acquired through symbiosis with OPC (organophosphorous compounds) bacteria-destructors.…”

Isolation of oxalotrophic bacteria associated with Varroa destructor mites

“…In this respect, one intriguing observation is that the closest relatives to VD8, VD19 and VD14 are insecticide‐degrading Burkholderia strains originally isolated from Cavelerius saccharivorus that were subjected to strong selective pressure by the organophosphorus insecticide, fenitrothion (Tago et al . ). Such evidence strengthens the hypothesis of a related cluster of Burkholderia spp.…”

“…; Tago et al . and references therein). Our results suggest that this association may extend to some members of the class Arachnida, like varroa, within the phylum Arthropoda .…”