Intracellularity, extracellularity, and squeezing in the symbiotic organ underpin nurturing and functioning of bacterial symbiont in leaf beetles

Summary: Cassidine leaf beetles are associated with genome-reduced symbiotic bacteria Stammera involved in pectin digestion. Stammera cells appear to be harbored in paired symbiotic organs located at the foregut-midgut junction either intracellularly or extracellularly, whereas the symbiont is extra...

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Main Authors: Kohei Oguchi, Toshiyuki Harumoto, Tatsuya Katsuno, Yu Matsuura, Soma Chiyoda, Takema Fukatsu
Format: Article
Language:English
Published: Elsevier 2024-05-01
Series:iScience
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S2589004224009532
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author Kohei Oguchi
Toshiyuki Harumoto
Tatsuya Katsuno
Yu Matsuura
Soma Chiyoda
Takema Fukatsu
author_facet Kohei Oguchi
Toshiyuki Harumoto
Tatsuya Katsuno
Yu Matsuura
Soma Chiyoda
Takema Fukatsu
author_sort Kohei Oguchi
collection DOAJ
description Summary: Cassidine leaf beetles are associated with genome-reduced symbiotic bacteria Stammera involved in pectin digestion. Stammera cells appear to be harbored in paired symbiotic organs located at the foregut-midgut junction either intracellularly or extracellularly, whereas the symbiont is extracellular in the ovary-accessory glands of adult females and during caplet transmission in eggs. However, using fluorescence and electron microscopy, an intracellular symbiotic configuration of Stammera was observed in Notosacantha species. Detailed inspection of other cassidine species revealed fragmented cell membrane and cytoplasm of the symbiotic organs, wherein Stammera cells are in an intermediate status between intracellularity and extracellularity. We also identified a mitochondria-rich region adjacent to the symbiont-filled region and well-developed muscle fibers surrounding the whole symbiotic organ. Based on these observations, we discuss why the Stammera genome has been reduced so drastically and how symbiont-derived pectinases are produced and supplied to the host’s alimentary tract for plant cell wall digestion.
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spelling doaj.art-0da530e2cf754a99b01b6a1486042e212024-04-27T04:43:11ZengElsevieriScience2589-00422024-05-01275109731Intracellularity, extracellularity, and squeezing in the symbiotic organ underpin nurturing and functioning of bacterial symbiont in leaf beetlesKohei Oguchi0Toshiyuki Harumoto1Tatsuya Katsuno2Yu Matsuura3Soma Chiyoda4Takema Fukatsu5Bioproducion Research Institute, National Institute of Advanced Industrial Science and Technology (AIST), Tsukuba, Japan; Misaki Marine Biological Station (MMBS), School of Science, The University of Tokyo, Miura, Japan; Corresponding authorHakubi Center for Advanced Research, Kyoto University, Kyoto, Japan; Graduate School of Biostudies, Kyoto University, Kyoto, JapanCenter for Anatomical Studies, Graduate School of Medicine, Kyoto University, Kyoto, Japan; KOKORO-Biology Group, Laboratories for Integrated Biology, Graduate School of Frontier Biosciences, Osaka University, Suita, JapanTropical Biosphere Research Center, University of the Ryukyus, Nishihara, Okinawa, JapanMisaki Marine Biological Station (MMBS), School of Science, The University of Tokyo, Miura, JapanBioproducion Research Institute, National Institute of Advanced Industrial Science and Technology (AIST), Tsukuba, Japan; Department of Biological Sciences, Graduate School of Science, the University of Tokyo, Tokyo, Japan; Graduate School of Life and Environmental Sciences, University of Tsukuba, Tsukuba, Japan; Corresponding authorSummary: Cassidine leaf beetles are associated with genome-reduced symbiotic bacteria Stammera involved in pectin digestion. Stammera cells appear to be harbored in paired symbiotic organs located at the foregut-midgut junction either intracellularly or extracellularly, whereas the symbiont is extracellular in the ovary-accessory glands of adult females and during caplet transmission in eggs. However, using fluorescence and electron microscopy, an intracellular symbiotic configuration of Stammera was observed in Notosacantha species. Detailed inspection of other cassidine species revealed fragmented cell membrane and cytoplasm of the symbiotic organs, wherein Stammera cells are in an intermediate status between intracellularity and extracellularity. We also identified a mitochondria-rich region adjacent to the symbiont-filled region and well-developed muscle fibers surrounding the whole symbiotic organ. Based on these observations, we discuss why the Stammera genome has been reduced so drastically and how symbiont-derived pectinases are produced and supplied to the host’s alimentary tract for plant cell wall digestion.http://www.sciencedirect.com/science/article/pii/S2589004224009532MicrobiologyMicrobial cell structure
spellingShingle Kohei Oguchi
Toshiyuki Harumoto
Tatsuya Katsuno
Yu Matsuura
Soma Chiyoda
Takema Fukatsu
Intracellularity, extracellularity, and squeezing in the symbiotic organ underpin nurturing and functioning of bacterial symbiont in leaf beetles
iScience
Microbiology
Microbial cell structure
title Intracellularity, extracellularity, and squeezing in the symbiotic organ underpin nurturing and functioning of bacterial symbiont in leaf beetles
title_full Intracellularity, extracellularity, and squeezing in the symbiotic organ underpin nurturing and functioning of bacterial symbiont in leaf beetles
title_fullStr Intracellularity, extracellularity, and squeezing in the symbiotic organ underpin nurturing and functioning of bacterial symbiont in leaf beetles
title_full_unstemmed Intracellularity, extracellularity, and squeezing in the symbiotic organ underpin nurturing and functioning of bacterial symbiont in leaf beetles
title_short Intracellularity, extracellularity, and squeezing in the symbiotic organ underpin nurturing and functioning of bacterial symbiont in leaf beetles
title_sort intracellularity extracellularity and squeezing in the symbiotic organ underpin nurturing and functioning of bacterial symbiont in leaf beetles
topic Microbiology
Microbial cell structure
url http://www.sciencedirect.com/science/article/pii/S2589004224009532
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