Interactions among deep-sea mussels and their epibiotic and endosymbiotic chemoautotrophic bacteria: Insights from multi-omics analysis

Yi-Tao Lin; Ting Xu; Jack Chi-Ho Ip; Yanan Sun; Ling Fang; Tiangang Luan; Yu Zhang; Pei-Yuan Qian; Jian-Wen Qiu

doi:10.24272/j.issn.2095-8137.2022.279

Volume 44 Issue 1

Jan. 2023

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Yi-Tao Lin, Ting Xu, Jack Chi-Ho Ip, Yanan Sun, Ling Fang, Tiangang Luan, Yu Zhang, Pei-Yuan Qian, Jian-Wen Qiu. Interactions among deep-sea mussels and their epibiotic and endosymbiotic chemoautotrophic bacteria: Insights from multi-omics analysis. Zoological Research, 2023, 44(1): 106-125. doi: 10.24272/j.issn.2095-8137.2022.279

Citation:

Yi-Tao Lin, Ting Xu, Jack Chi-Ho Ip, Yanan Sun, Ling Fang, Tiangang Luan, Yu Zhang, Pei-Yuan Qian, Jian-Wen Qiu. Interactions among deep-sea mussels and their epibiotic and endosymbiotic chemoautotrophic bacteria: Insights from multi-omics analysis. Zoological Research, 2023, 44(1): 106-125. doi: 10.24272/j.issn.2095-8137.2022.279

Citation:

Yi-Tao Lin, Ting Xu, Jack Chi-Ho Ip, Yanan Sun, Ling Fang, Tiangang Luan, Yu Zhang, Pei-Yuan Qian, Jian-Wen Qiu. Interactions among deep-sea mussels and their epibiotic and endosymbiotic chemoautotrophic bacteria: Insights from multi-omics analysis. Zoological Research, 2023, 44(1): 106-125. doi: 10.24272/j.issn.2095-8137.2022.279

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Interactions among deep-sea mussels and their epibiotic and endosymbiotic chemoautotrophic bacteria: Insights from multi-omics analysis

doi: 10.24272/j.issn.2095-8137.2022.279

Yi-Tao Lin^{1, 2, #},
Ting Xu^{2, 3, #},
Jack Chi-Ho Ip^{1, 2, #},
Yanan Sun^{1, 2},
Ling Fang⁴,
Tiangang Luan^{5, 6},
Yu Zhang^{7
,
,},
Pei-Yuan Qian^{2, 3
,
,},
Jian-Wen Qiu^{1, 2
,
,}

1.
Department of Biology, Hong Kong Baptist University, Hong Kong SAR, China
2.
Southern Marine Science and Engineering Guangdong Laboratory (Guangzhou), Guangzhou, Guangdong 511458, China
3.
Department of Ocean Science, Hong Kong University of Science and Technology, Hong Kong SAR, China
4.
Instrumental Analysis & Research Center, Sun Yat-Sen University, Guangzhou, Guangdong 510875, China
5.
State Key Laboratory of Biocontrol, School of Life Sciences, Sun Yat-Sen University, Guangzhou, Guangdong 510875, China
6.
Institute of Environmental and Ecological Engineering, Guangdong University of Technology, Guangzhou, Guangdong 510006, China
7.
College of Life Sciences and Oceanography, Shenzhen University, Shenzhen, Guangdong 518060, China

All raw sequencing data for the metagenomes, metatranscriptomes, and symbiont genomes were deposited in the National Center for Biotechnology Information Sequence Read Archive (NCBI: PRJNA785362), National Genomics Data Center (GSA: PRJCA012895), and Science Data Bank (CSTR: 31253.11.sciencedb.06106). The mass spectrometry proteomics data were deposited in the ProteomeXchange (PRIDE identifier: PXD03067). The metagenome assemblies and annotations were deposited in Figshare DOI: 10.6084/m9.figshare.17693405.
Supplementary data to this article can be found online.
The authors declare that they have no competing interests.
J.W.Q., P.Y.Q., and Y.Z. designed the project. Y.T.L. and T.X. collected the samples. T.X. performed the DNA and RNA extraction. Y.T.L., T.X., J.C.H.I., and Y.S. conducted sequencing, assembly, and annotation of the metagenome and metatranscriptome. Y.T.L. extracted the proteins. L.F. and T.L. conducted the LC-MS/MS. Y.T.L., T.X., and J.C.-H.I. analyzed the proteome. Y.T.L., T.X., J.C.H.I., Y.Z., and J.W.Q. drafted the manuscript. All authors read and approved the final version of the manuscript.
#Authors contributed equally to this work

Funds: This study was supported by the Southern Marine Science and Engineering Guangdong Laboratory (Guangzhou) (GML2019ZD0409, SMSEGL20SC02), Research Grants Council of Hong Kong (12101021), and Guangdong Natural Science Foundation (2020A1515011117)

More Information

Corresponding author: E-mail: biozy@szu.edu.cn; boqianpy@ust.hk; qiujw@hkbu.edu.hk
Received Date: 2022-10-19
Accepted Date: 2022-10-31

Published Online: 2022-11-22

Publish Date: 2023-01-18

Abstract

Abstract

Endosymbiosis with Gammaproteobacteria is fundamental for the success of bathymodioline mussels in deep-sea chemosynthesis-based ecosystems. However, the recent discovery of Campylobacteria on the gill surfaces of these mussels suggests that these host-bacterial relationships may be more complex than previously thought. Using the cold-seep mussel (Gigantidas haimaensis) as a model, we explored this host-bacterial system by assembling the host transcriptome and genomes of its epibiotic Campylobacteria and endosymbiotic Gammaproteobacteria and quantifying their gene and protein expression levels. We found that the epibiont applies a sulfur oxidizing (SOX) multienzyme complex with the acquisition of soxB from Gammaproteobacteria for energy production and switched from a reductive tricarboxylic acid (rTCA) cycle to a Calvin-Benson-Bassham (CBB) cycle for carbon assimilation. The host provides metabolic intermediates, inorganic carbon, and thiosulfate to satisfy the materials and energy requirements of the epibiont, but whether the epibiont benefits the host is unclear. The endosymbiont adopts methane oxidation and the ribulose monophosphate pathway (RuMP) for energy production, providing the major source of energy for itself and the host. The host obtains most of its nutrients, such as lysine, glutamine, valine, isoleucine, leucine, histidine, and folate, from the endosymbiont. In addition, host pattern recognition receptors, including toll-like receptors, peptidoglycan recognition proteins, and C-type lectins, may participate in bacterial infection, maintenance, and population regulation. Overall, this study provides insights into the complex host-bacterial relationships that have enabled mussels and bacteria to thrive in deep-sea chemosynthetic ecosystems.
- Bathymodioline,
- Chemosynthesis,
- Cold seep,
- Deep-sea adaptation,
- Symbiosis

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References(102)

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