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author:

Shi, H. (Shi, H..) [1] | Ruan, L. (Ruan, L..) [2] | Chen, Z. (Chen, Z..) [3] | Liao, Y. (Liao, Y..) [4] | Wu, W. (Wu, W..) [5] | Liu, L. (Liu, L..) [6] | Xu, X. (Xu, X..) [7]

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Scopus

Abstract:

BACKGROUND: Lamellibrachia luymesi dominates cold sulfide-hydrocarbon seeps and is known for its ability to consume bacteria for energy. The symbiotic relationship between tubeworms and bacteria with particular adaptations to chemosynthetic environments has received attention. However, metabolic studies have primarily focused on the mechanisms and pathways of the bacterial symbionts, while studies on the animal hosts are limited. RESULTS: Here, we sequenced the transcriptome of L. luymesi and generated a transcriptomic database containing 79,464 transcript sequences. Based on GO and KEGG annotations, we identified transcripts related to sulfur metabolism, sterol biosynthesis, trehalose synthesis, and hydrolysis. Our in-depth analysis identified sulfation pathways in L. luymesi, and sulfate activation might be an important detoxification pathway for promoting sulfur cycling, reducing byproducts of sulfide metabolism, and converting sulfur compounds to sulfur-containing organics, which are essential for symbiotic survival. Moreover, sulfide can serve directly as a sulfur source for cysteine synthesis in L. luymesi. The existence of two pathways for cysteine synthesis might ensure its participation in the formation of proteins, heavy metal detoxification, and the sulfide-binding function of haemoglobin. Furthermore, our data suggested that cold-seep tubeworm is capable of de novo sterol biosynthesis, as well as incorporation and transformation of cycloartenol and lanosterol into unconventional sterols, and the critical enzyme involved in this process might have properties similar to those in the enzymes from plants or fungi. Finally, trehalose synthesis in L. luymesi occurs via the trehalose-6-phosphate synthase (TPS) and trehalose-6-phosphate phosphatase (TPP) pathways. The TPP gene has not been identified, whereas the TPS gene encodes a protein harbouring conserved TPS/OtsA and TPP/OtsB domains. The presence of multiple trehalases that catalyse trehalose hydrolysis could indicate the different roles of trehalase in cold-seep tubeworms. CONCLUSIONS: We elucidated several molecular pathways of sulfate activation, cysteine and cholesterol synthesis, and trehalose metabolism. Contrary to the previous analysis, two pathways for cysteine synthesis and the cycloartenol-C-24-methyltransferase gene were identified in animals for the first time. The present study provides new insights into particular adaptations to chemosynthetic environments in L. luymesi and can serve as the basis for future molecular studies on host-symbiont interactions and biological evolution. © 2023. The Author(s).

Keyword:

Adaptation to deep-sea chemosynthetic environment Cholesterol Cold seep Cycloartenol-C-24-methyltransferase Cysteine Fungi Sulfate Transcriptome Trehalase

Community:

  • [ 1 ] [Shi, H.]State Key Laboratory Breeding Base of Marine Genetic Resources, Key Laboratory of Marine Genetic Resources of Ministry of Natural Resources, Third Institute of Oceanography, Ministry of Natural Resources, Fujian Key Laboratory of Marine Genetic Resources, No. 178 Daxue Road, Xiamen, Fujian 361005, China
  • [ 2 ] [Ruan, L.]State Key Laboratory Breeding Base of Marine Genetic Resources, Key Laboratory of Marine Genetic Resources of Ministry of Natural Resources, Third Institute of Oceanography, Ministry of Natural Resources, Fujian Key Laboratory of Marine Genetic Resources, No. 178 Daxue Road, Xiamen, Fujian 361005, China
  • [ 3 ] [Ruan, L.]College of Marine Biology, Xiamen ocean vocational college, Xiamen, 361100, China
  • [ 4 ] [Ruan, L.]Co-Innovation Center of Jiangsu Marine Bio-Industry Technology, Jiangsu Ocean University, Lianyungang222005, China
  • [ 5 ] [Chen, Z.]State Key Laboratory Breeding Base of Marine Genetic Resources, Key Laboratory of Marine Genetic Resources of Ministry of Natural Resources, Third Institute of Oceanography, Ministry of Natural Resources, Fujian Key Laboratory of Marine Genetic Resources, No. 178 Daxue Road, Xiamen, Fujian 361005, China
  • [ 6 ] [Liao, Y.]State Key Laboratory Breeding Base of Marine Genetic Resources, Key Laboratory of Marine Genetic Resources of Ministry of Natural Resources, Third Institute of Oceanography, Ministry of Natural Resources, Fujian Key Laboratory of Marine Genetic Resources, No. 178 Daxue Road, Xiamen, Fujian 361005, China
  • [ 7 ] [Liao, Y.]School of Advanced Manufacturing, Fuzhou University, Fuzhou, 362200, China
  • [ 8 ] [Wu, W.]State Key Laboratory Breeding Base of Marine Genetic Resources, Key Laboratory of Marine Genetic Resources of Ministry of Natural Resources, Third Institute of Oceanography, Ministry of Natural Resources, Fujian Key Laboratory of Marine Genetic Resources, No. 178 Daxue Road, Xiamen, Fujian 361005, China
  • [ 9 ] [Wu, W.]Department of Biology and Guangdong Provincial Key Laboratory of Marine Biotechnology, Shantou University, Shantou, 515063, China
  • [ 10 ] [Liu, L.]State Key Laboratory Breeding Base of Marine Genetic Resources, Key Laboratory of Marine Genetic Resources of Ministry of Natural Resources, Third Institute of Oceanography, Ministry of Natural Resources, Fujian Key Laboratory of Marine Genetic Resources, No. 178 Daxue Road, Xiamen, Fujian 361005, China
  • [ 11 ] [Xu, X.]State Key Laboratory Breeding Base of Marine Genetic Resources, Key Laboratory of Marine Genetic Resources of Ministry of Natural Resources, Third Institute of Oceanography, Ministry of Natural Resources, Fujian Key Laboratory of Marine Genetic Resources, No. 178 Daxue Road, Xiamen, Fujian 361005, China

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Source :

BMC genomics

ISSN: 1471-2164

Year: 2023

Issue: 1

Volume: 24

Page: 175-

3 . 5

JCR@2023

3 . 5 0 0

JCR@2023

ESI HC Threshold:47

JCR Journal Grade:2

CAS Journal Grade:2

Cited Count:

WoS CC Cited Count: 0

SCOPUS Cited Count:

ESI Highly Cited Papers on the List: 0 Unfold All

WanFang Cited Count:

Chinese Cited Count:

30 Days PV: 2

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