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

Kohei Oguchi; Toshiyuki Harumoto; Tatsuya Katsuno; Yu Matsuura; Soma Chiyoda; Takema Fukatsu

doi:10.1016/j.isci.2024.109731

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

iScience. 2024 Apr 16;27(5):109731. doi: 10.1016/j.isci.2024.109731. eCollection 2024 May 17.

Authors

Kohei Oguchi^{1

2}, Toshiyuki Harumoto^{3

4}, Tatsuya Katsuno^{5

6}, Yu Matsuura⁷, Soma Chiyoda², Takema Fukatsu^{1

8

9}

Affiliations

¹ Bioproducion Research Institute, National Institute of Advanced Industrial Science and Technology (AIST), Tsukuba, Japan.
² Misaki Marine Biological Station (MMBS), School of Science, The University of Tokyo, Miura, Japan.
³ Hakubi Center for Advanced Research, Kyoto University, Kyoto, Japan.
⁴ Graduate School of Biostudies, Kyoto University, Kyoto, Japan.
⁵ Center for Anatomical Studies, Graduate School of Medicine, Kyoto University, Kyoto, Japan.
⁶ KOKORO-Biology Group, Laboratories for Integrated Biology, Graduate School of Frontier Biosciences, Osaka University, Suita, Japan.
⁷ Tropical Biosphere Research Center, University of the Ryukyus, Nishihara, Okinawa, Japan.
⁸ Department of Biological Sciences, Graduate School of Science, the University of Tokyo, Tokyo, Japan.
⁹ Graduate School of Life and Environmental Sciences, University of Tsukuba, Tsukuba, Japan.

Abstract

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.

Keywords: Microbial cell structure; Microbiology.