title: Insecticide applications to soil contribute to the development of Burkholderia mediating insecticide resistance in stinkbugs.
abstract: Some soil Burkholderia strains are capable of degrading the organophosphorus insecticide, fenitrothion, and establish symbiosis with stinkbugs, making the host insects fenitrothion-resistant. However, the ecology of the symbiotic degrading Burkholderia adapting to fenitrothion in the free-living environment is unknown. We hypothesized that fenitrothion applications affect the dynamics of fenitrothion-degrading Burkholderia, thereby controlling the transmission of symbiotic degrading Burkholderia from the soil to stinkbugs. We investigated changes in the density and diversity of culturable Burkholderia (i.e. symbiotic and nonsymbiotic fenitrothion degraders and nondegraders) in fenitrothion-treated soil using microcosms. During the incubation with five applications of pesticide, the density of the degraders increased from less than the detection limit to around 10(6)/g of soil. The number of dominant species among the degraders declined with the increasing density of degraders; eventually, one species predominated. This process can be explained according to the competitive exclusion principle using V(max) and K(m) values for fenitrothion metabolism by the degraders. We performed a phylogenetic analysis of representative strains isolated from the microcosms and evaluated their ability to establish symbiosis with the stinkbug Riptortus pedestris. The strains that established symbiosis with R. pedestris were assigned to a cluster including symbionts commonly isolated from stinkbugs. The strains outside the cluster could not necessarily associate with the host. The degraders in the cluster predominated during the initial phase of degrader dynamics in the soil. Therefore, only a few applications of fenitrothion could allow symbiotic degraders to associate with their hosts and may cause the emergence of symbiont-mediated insecticide resistance.
authors.affiliation: Environmental Biofunction Division, National Institute for Agro-Environmental Sciences (NIAES), 3-1-3 Kannondai, Tsukuba, Ibaraki, 305-8604, Japan.
authors.forename: Kanako
authors.initials: K
authors.lastname: Tago
authors.affiliation: Bioproduction Research Institute, Hokkaido Center, National Institute of Advanced Industrial Science and Technology (AIST), 2-17-2-1 Tsukisamu-higashi, Toyohira-ku, Sapporo, Hokkaido, 062-8517, Japan.|Graduate School of Agriculture, Hokkaido University, Kita 8, Nishi 5, Kita-ku, Sapporo, Hokkaido, 060-8589, Japan.
authors.forename: Yoshitomo
authors.initials: Y
authors.lastname: Kikuchi
authors.affiliation: Laboratory for Mathematical Modeling of Immune System, RIKEN Center for Integrative Medical Science Center (IMS-RCAI), 1-7-22 Suehiro-cho, Tsurumi-ku, Yokohama City, Kanagawa, 230-0045, Japan.
authors.forename: Sinji
authors.initials: S
authors.lastname: Nakaoka
authors.affiliation: Graduate School of Integrated Arts and Sciences, Hiroshima University, 1-7-1 Kagamiyama, Higashi-Hiroshima, Hiroshima, 739-8521, Japan.
authors.forename: Chie
authors.initials: C
authors.lastname: Katsuyama
authors.affiliation: Environmental Biofunction Division, National Institute for Agro-Environmental Sciences (NIAES), 3-1-3 Kannondai, Tsukuba, Ibaraki, 305-8604, Japan.
authors.forename: Masahito
authors.initials: M
authors.lastname: Hayatsu
mesh_terms: D000818:Animals; D019117:Burkholderia / Q000235:genetics* / Q000378:metabolism; D004269:DNA, Bacterial / Q000235:genetics; D005278:Fenitrothion / Q000378:metabolism; D020062:Heteroptera / Q000382:microbiology*; D007305:Insecticide Resistance / Q000235:genetics*; D007306:Insecticides; D008962:Models, Theoretical; D008969:Molecular Sequence Data; D010802:Phylogeny; D017422:Sequence Analysis, DNA; D012987:Soil; D012988:Soil Microbiology; D013559:Symbiosis
chemical_list: D004269:DNA, Bacterial; D007306:Insecticides; D012987:Soil; D005278:Fenitrothion
keywords: Burkholderia; organophosphorus insecticide degradation; pest stinkbugs; population dynamics; symbiotic gut bacteria