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

Tame, Akihiro; Maruyama, Tadashi; Ikuta, Tetsuro; Chikaraishi, Yoshihito; Ogawa, Nanako O.; Tsuchiya, Masashi; Takishita, Kiyotaka; Tsuda, Miwako; Hirai, Miho; Takaki, Yoshihiro; Ohkouchi, Naohiko; Fujikura, Katsunori; Yoshida, Takao

doi:10.1126/sciadv.adg8364

Cited by 3 publications

(1 citation statement)

References 62 publications

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“…The contradicts in the number of new born endosymbionts and digested endosymbionts suggested that lysosome-mediated digestion could play other roles in addition to providing nutrients. Recently, it is showed that the digestion of symbionts could be regulated by mTORC1 through nutrient signaling pathway and promoted under reduced nutrient supply (either by death of endosymbionts or removal of methane) [40][41][42] . We therefore speculated that lysosome-mediated symbiont digestion may be a secondary option to obtain nutrition under normal circumstance, but an efficient way to control the symbiont population and obtain nutrition under abrupt stresses or other emergencies.…”

Section: Discussionmentioning

confidence: 99%

Cooperation between bacteriocytes and endosymbionts drives function and development of symbiotic cells in mussel holobionts

Chen,

Li,

Zhong

et al. 2023

Preprint

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Symbiosis drives the adaptation and evolution in multicellular organisms. Modeling the function and development of symbiotic cells/organs in holobionts is yet challenging. Here, we surveyed the molecular function and developmental trajectory of bacteriocyte lineage in non-model deep-sea mussels by constructing a high-resolution single-cell expression atlas of gill tissue. We show that mussel bacteriocytes optimized immune genes to facilitate recognition, engulfment, and elimination of endosymbionts, and interacted with them intimately in sterol, carbohydrate, and ammonia metabolism. Additionally, the bacteriocytes could arise from three different stem cells as well as bacteriocytes themselves. In particular, we showed that the molecular functions and developmental process of bacteriocytes were guided by the same set of regulatory networks and dynamically altered regarding to symbiont abundance via sterol-related signaling. The coordination in the functions and development of bacteriocytes and between the host and symbionts underlies the interdependency of symbiosis, and drives the deep-sea adaptation of mussels.

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Section: Discussionmentioning

confidence: 99%

Cooperation between bacteriocytes and endosymbionts drives function and development of symbiotic cells in mussel holobionts

Chen,

Li,

Zhong

et al. 2023

Preprint

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Different parts of the mussel Gigantidas haimaensis holobiont responded differently to deep‐sea sampling stress

YAN,

WEI,

LAN

et al. 2024

Integr. Zool.

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Acute environmental changes cause stress during conventional deep‐sea biological sampling without in situ fixation and affect gene expressions of samples collected. However, the degree of influence and underlying mechanisms are hardly investigated. Here, we conducted comparative transcriptomic analyses between in situ and onboard fixed gills and between in situ and onboard fixed mantles of deep‐sea mussel Gigantidas haimaensis to assess the effects of incidental sampling stress. Results showed that transcription, translation, and energy metabolism were upregulated in onboard fixed gills and mantles, thereby mobilizing rapid gene expression to tackle the stress. Autophagy and phagocytosis that related to symbiotic interactions between the host and endosymbiont were downregulated in the onboard fixed gills. These findings demonstrated that symbiotic gill and nonsymbiotic mantle responded differently to sampling stress, and symbiosis in the gill was perturbed. Further comparative metatranscriptomic analysis between in situ and onboard fixed gills revealed that stress response genes, peptidoglycan biosynthesis, and methane fixation were upregulated in the onboard fixed endosymbiotic Gammaproteobacteria inside the gills, implying that energy metabolism of the endosymbiont was increased to cope with sampling stress. Furthermore, comparative analysis between the mussel G. haimaensis and the limpet Bathyacmaea lactea transcriptomes resultedidentified six transcription factor orthologs upregulated in both onboard fixed mussel mantles and limpets, including sharply increased early growth response protein 1 and Kruppel‐like factor 5. They potentially play key roles in initiating the response of sampled deep‐sea macrobenthos to sampling stress. Our results clearly show that in situ fixed biological samples are vital for studying deep‐sea environmental adaptation.

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Amino acid nitrogen isotopic compositions show seep copepods gain nutrition from host animals

Ishikawa,

Chen,

Hashimoto

et al. 2024

Mar. Ecol. Prog. Ser.

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Deep-sea chemosynthetic ecosystems harbour high biomass centred around animals with chemoautotrophic symbionts. Despite being intensively studied over the last 4 decades, microscopic animals associated with and/or parasitic on dominating holobionts remain understudied. Here, we combine bulk tissue isotope analysis for carbon and nitrogen and compound-specific isotope analysis of amino acids (CSIA-AA) for nitrogen to elucidate the relationship between 2 copepod-host pairs from the Off Hatsushima hydrothermal seep in Sagami Bay, Japan: the vesicomyid clam Phreagena okutanii and Hyphalion sagamiense living on its mantle, and the tubeworm Lamellibrachia columna and Dirivultus kaiko found on its plume. Bulk tissue isotope analyses found overall large variations in δ13C and δ15N values across both associations, and did not allow conclusions on the trophic relationship between each pair. In contrast, CSIA-AA for Phreagena-Hyphalion clearly showed trophic positions (TPGlu/Phe) increasing from gill (symbiont) to adductor muscle (host tissue) to H. sagamiense. In the case of Lamellibrachia-Dirivultus, a similar increase in TPGlu/Phe was found from the plume to D. kaiko. These results show that both H. sagamiense and D. kaiko are nutritionally dependent on their respective hosts and therefore should be considered parasites despite being from copepod families that are typically not recognised as parasitic. Our CSIA-AA results represent the first use of this technique to document host-parasite relationships in chemosynthetic ecosystems. Understanding the role of parasites is of great importance in reconstructing energy flow in ecosystems, and our results underscore the promising nature of CSIA-AA in revealing their otherwise hidden relationships.

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

Cited by 3 publications

References 62 publications

Cooperation between bacteriocytes and endosymbionts drives function and development of symbiotic cells in mussel holobionts

Cooperation between bacteriocytes and endosymbionts drives function and development of symbiotic cells in mussel holobionts

Different parts of the mussel Gigantidas haimaensis holobiont responded differently to deep‐sea sampling stress

Amino acid nitrogen isotopic compositions show seep copepods gain nutrition from host animals

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