1. Key Points

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The deep-sea bivalve Bathymodiolus japonicus acquires symbiotic bacteria into its cells by phagocytosis (*1) in its intracellular symbiosis (*2). The research group found that the protein complex mTORC1 (*3) is involved in the integration of intracellular nutrient-environment signals for the maintenance and digestion of the symbiotic bacteria.

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They also newly found that mTORC1, which integrates various intracellular signals and regulates cellular functions, also plays a role in intracellular symbiosis.

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Intracellular symbiosis is a biological phenomenon that has driven the evolution of eukaryotes, and mTORC1 may regulate intracellular symbiosis in other animals harboring microorganism, such as insects. Therefore, this research will provide important insights into the evolution of life and on the origin and maintenance of biodiversity.

2. Overview

The mechanism of the intracellular symbiosis in the bivalve B. japonicus (*4), which lives near methane-rich deep-sea sources, was studied by a joint research group of the Research Institute for Global Change, the Research Institute for Marine Resources Utilization, Institute for Extra-cutting edge Science and Technology Avant-garde Research of Japan Agency for Marine-Earth Science and Technology, School of Marine Biosciences of Kitasato University, School of Medical Sciences of Fukui University, Institute of Low Temperature Science of Hokkaido University, and Fukuoka Women's University. They were newly found that mTORC1, a regulatory protein complex that integrates host intracellular nutrient-environment signals, regulates the maintenance and digestion of symbiotic bacteria.

Bivalves and other animals live near deep-sea hydrothermal vents and methane-rich deep-sea seeps, which are considered important marine areas and have been identified as candidate offshore marine protected areas for biodiversity conservation. Many of these animals form symbiotic relationship with chemosynthetic bacteria (*5) (symbiotic bacteria) within the cells and obtain the organic material produced by the symbiotic bacteria (Fig. 1). However, the mechanism by which the host animals acquire and maintain the symbiotic bacteria that produce the nutrients needed for their survival, and obtain the nutrients from the symbiotic bacteria has been a major mystery.

The research team has found that the B. japonicus acquires symbiotic bacteria in phagosomes formed by phagocytosis of the gill cells. It has newly found that mTORC1 was on the surface of the phagosome membrane enclosing these symbiotic bacteria, recognizes and controls the degradation and maintenance of the bacteria for sensing the nutrients from symbiotic bacteria. This is the first study of its kind, and the study findings provide entirely new evidence that mTORC1 plays an important role in the intracellular symbiosis. mTORC1 is present in many living organisms and plays a role as a central regulator that controls various functions of cells. Therefore, the findings are significant outcome for understanding the function of mTORC1 and the establishment and evolution of the intracellular symbiosis. In the future, by focusing on studying the role of mTORC1 in regulating intracellular symbiosis, it is anticipated that a more detailed understanding will be achieved regarding the mechanisms underlying the establishment and evolution of intracellular symbiosis between animals and microorganisms.

Fig.1　 Intracellular symbiosis in Bathymodiolus japonicus Most B. japonicus have an intracellular symbiotic relationship with chemosynthetic bacteria in their gill tissues. Chemosynthetic bacteria are taken in from the external environment and form a symbiotic relationship. (The figure created by Nariyuki Yoshihara)

The research results will be published in Science Advances on August 24, 2012 (JST).
The research was supported by a Grant-in-Aid for Scientific Research (17K07519, 20K06779, 19K06799) from the Japan Society for the Promotion of Science.

Title：

mTORC1 regulates phagosome digestion of symbiotic bacteria for intracellular nutritional symbiosis in a deep-sea mussel

Authors：

Akihiro Tame^1,2,3, Tadashi Maruyama², Tetsuro Ikuta¹, Yoshihito Chikaraishi⁴, Nanako O. Ogawa⁵, Masashi Tsuchiya¹, Kiyotaka Takishita⁶, Miwako Tsuda⁷, Miho Hirai⁷, Yoshihiro Takaki⁷, Naohiko Ohkouchi⁵, Katsunori Fujikura¹, Takao Yoshida^1,2

Affiliation：

1

 Research Institute for Global Change, Japan Agency for Marine-Earth Science and Technology(JAMSTEC)

2

 School of Marine Biosciences, University of Kitasato

3

 Faculty of Medical Sciences, Life Science Research Laboratory, University of Fukui

4

 Institute of Low Temperature Science, Hokkaido University

5

 Research Institute for Marine Resources Utilization, Japan Agency for Marine-Earth Science and Technology(JAMSTEC)

6

 Department of Environmental Science, Fukuoka Women's University

7

 Institute for Extra-cutting-edge Science and Technology Avant-grade Research, Japan Agency for Marine-Earth Science and Technology(JAMSTEC)

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 Correspondence to: T. Yoshida

DOI:

10.1126/sciadv.adg8364