Insect's intestinal organ for symbiont sorting.
Symbiosis has significantly contributed to organismal adaptation and diversification. For establishment and maintenance of such host-symbiont associations, host organisms must have evolved mechanisms for selective incorporation, accommodation, and maintenance of their specific microbial partners. Here we report the discovery of a previously unrecognized type of animal organ for symbiont sorting. In the bean bug Riptortus pedestris, the posterior midgut is morphologically differentiated for harboring specific symbiotic bacteria of a beneficial nature. The sorting organ lies in the middle of the intestine as a constricted region, which partitions the midgut into an anterior nonsymbiotic region and a posterior symbiotic region. Oral administration of GFP-labeled Burkholderia symbionts to nymphal stinkbugs showed that the symbionts pass through the constricted region and colonize the posterior midgut. However, administration of food colorings revealed that food fluid enters neither the constricted region nor the posterior midgut, indicating selective symbiont passage at the constricted region and functional isolation of the posterior midgut for symbiosis. Coadministration of the GFP-labeled symbiont and red fluorescent protein-labeled Escherichia coli unveiled selective passage of the symbiont and blockage of E. coli at the constricted region, demonstrating the organ's ability to discriminate the specific bacterial symbiont from nonsymbiotic bacteria. Transposon mutagenesis and screening revealed that symbiont mutants in flagella-related genes fail to pass through the constricted region, highlighting that both host's control and symbiont's motility are involved in the sorting process. The blocking of food flow at the constricted region is conserved among diverse stinkbug groups, suggesting the evolutionary origin of the intestinal organ in their common ancestor.
Graduate School of Agriculture, Hokkaido University, Sapporo 060-8589, Japan;
Tsubasa
T
Ohbayashi
Graduate School of Agriculture, Hokkaido University, Sapporo 060-8589, Japan; Bioproduction Research Institute, Hokkaido Center, National Institute of Advanced Industrial Science and Technology, Sapporo 062-8517, Japan;
Kazutaka
K
Takeshita
Graduate School of Agriculture, Hokkaido University, Sapporo 060-8589, Japan; Bioproduction Research Institute, Hokkaido Center, National Institute of Advanced Industrial Science and Technology, Sapporo 062-8517, Japan;
Wataru
W
Kitagawa
Department of Liberal Arts, The Open University of Japan, Chiba 261-8586, Japan;
Naruo
N
Nikoh
Bioproduction Research Institute, National Institute of Advanced Industrial Science and Technology, Tsukuba 305-8566, Japan;
Ryuichi
R
Koga
Bioproduction Research Institute, National Institute of Advanced Industrial Science and Technology, Tsukuba 305-8566, Japan;
Xian-Ying
XY
Meng
Environmental Biofunction Division, National Institute for Agro-Environmental Sciences, Tsukuba 305-8604, Japan;
Kanako
K
Tago
Environmental Management Research Institute​, National Institute of Advanced Industrial Science and Technology, Tsukuba 305-8569, Japan;
Tomoyuki
T
Hori
Environmental Biofunction Division, National Institute for Agro-Environmental Sciences, Tsukuba 305-8604, Japan;
Masahito
M
Hayatsu
Graduate School of Agriculture, Hokkaido University, Sapporo 060-8589, Japan;
Kozo
K
Asano
Graduate School of Agriculture, Hokkaido University, Sapporo 060-8589, Japan; Bioproduction Research Institute, Hokkaido Center, National Institute of Advanced Industrial Science and Technology, Sapporo 062-8517, Japan;
Yoichi
Y
Kamagata
Global Research Laboratory, College of Pharmacy, Pusan National University, Pusan 609-735, Korea.
Bok Luel
BL
Lee
Bioproduction Research Institute, National Institute of Advanced Industrial Science and Technology, Tsukuba 305-8566, Japan;
Takema
T
Fukatsu
Graduate School of Agriculture, Hokkaido University, Sapporo 060-8589, Japan; Bioproduction Research Institute, Hokkaido Center, National Institute of Advanced Industrial Science and Technology, Sapporo 062-8517, Japan; y-kikuchi@aist.go.jp.
Yoshitomo
Y
Kikuchi
D000284:Administration, Oral; D000818:Animals; D019117:Burkholderia / Q000502:physiology*; D004396:Coloring Agents / Q000737:chemistry; D004064:Digestive System / Q000382:microbiology; D004926:Escherichia coli / Q000378:metabolism; D019143:Evolution, Molecular; D005407:Flagella / Q000502:physiology; D041981:Gastrointestinal Tract / Q000382:microbiology; D049452:Green Fluorescent Proteins / Q000378:metabolism; D020062:Heteroptera / Q000382:microbiology*; D007313:Insecta; D007422:Intestines / Q000382:microbiology*; D008164:Luminescent Proteins / Q000378:metabolism; D046529:Microscopy, Electron, Transmission; D016296:Mutagenesis; D009154:Mutation; D010802:Phylogeny; D010957:Plasmids / Q000378:metabolism; D013559:Symbiosis / Q000235:genetics*; D000097573:Red Fluorescent Protein
D004396:Coloring Agents; D049452:Green Fluorescent Proteins; D008164:Luminescent Proteins; D000097573:Red Fluorescent Protein
Burkholderia; flagellar motility; gut symbiosis; partner choice; stinkbug