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author:

Shi, Hong (Shi, Hong.) [1] | Ruan, Lingwei (Ruan, Lingwei.) [2] | Chen, Zimeng (Chen, Zimeng.) [3] | Liao, Yifei (Liao, Yifei.) [4] | Wu, Wenhao (Wu, Wenhao.) [5] | Liu, Linmin (Liu, Linmin.) [6] | Xu, Xun (Xu, Xun.) [7]

Indexed by:

Scopus SCIE

Abstract:

BackgroundLamellibrachia 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.ResultsHere, 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.ConclusionsWe 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.

Keyword:

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

Community:

  • [ 1 ] [Shi, Hong]Minist Nat Resources, State Key Lab Breeding Base Marine Genet Resources, Key Lab Marine Genet Resources, Fujian Key Lab Marine Genet Resources,Inst Oceanog, 178 Daxue Rd, Xiamen 361005, Fujian, Peoples R China
  • [ 2 ] [Ruan, Lingwei]Minist Nat Resources, State Key Lab Breeding Base Marine Genet Resources, Key Lab Marine Genet Resources, Fujian Key Lab Marine Genet Resources,Inst Oceanog, 178 Daxue Rd, Xiamen 361005, Fujian, Peoples R China
  • [ 3 ] [Chen, Zimeng]Minist Nat Resources, State Key Lab Breeding Base Marine Genet Resources, Key Lab Marine Genet Resources, Fujian Key Lab Marine Genet Resources,Inst Oceanog, 178 Daxue Rd, Xiamen 361005, Fujian, Peoples R China
  • [ 4 ] [Liao, Yifei]Minist Nat Resources, State Key Lab Breeding Base Marine Genet Resources, Key Lab Marine Genet Resources, Fujian Key Lab Marine Genet Resources,Inst Oceanog, 178 Daxue Rd, Xiamen 361005, Fujian, Peoples R China
  • [ 5 ] [Wu, Wenhao]Minist Nat Resources, State Key Lab Breeding Base Marine Genet Resources, Key Lab Marine Genet Resources, Fujian Key Lab Marine Genet Resources,Inst Oceanog, 178 Daxue Rd, Xiamen 361005, Fujian, Peoples R China
  • [ 6 ] [Liu, Linmin]Minist Nat Resources, State Key Lab Breeding Base Marine Genet Resources, Key Lab Marine Genet Resources, Fujian Key Lab Marine Genet Resources,Inst Oceanog, 178 Daxue Rd, Xiamen 361005, Fujian, Peoples R China
  • [ 7 ] [Xu, Xun]Minist Nat Resources, State Key Lab Breeding Base Marine Genet Resources, Key Lab Marine Genet Resources, Fujian Key Lab Marine Genet Resources,Inst Oceanog, 178 Daxue Rd, Xiamen 361005, Fujian, Peoples R China
  • [ 8 ] [Ruan, Lingwei]Xiamen Ocean Vocat Coll, Coll Marine Biol, Xiamen 361100, Peoples R China
  • [ 9 ] [Ruan, Lingwei]Jiangsu Ocean Univ, Coinnovat Ctr Jiangsu Marine Bioind Technol, Lianyungang 222005, Peoples R China
  • [ 10 ] [Liao, Yifei]Fuzhou Univ, Sch Adv Mfg, Fuzhou 362200, Peoples R China
  • [ 11 ] [Wu, Wenhao]Shantou Univ, Dept Biol, Shantou 515063, Peoples R China
  • [ 12 ] [Wu, Wenhao]Shantou Univ, Guangdong Prov Key Lab Marine Biotechnol, Shantou 515063, Peoples R China

Reprint 's Address:

  • [Shi, Hong]Minist Nat Resources, State Key Lab Breeding Base Marine Genet Resources, Key Lab Marine Genet Resources, Fujian Key Lab Marine Genet Resources,Inst Oceanog, 178 Daxue Rd, Xiamen 361005, Fujian, Peoples R China;;[Ruan, Lingwei]Minist Nat Resources, State Key Lab Breeding Base Marine Genet Resources, Key Lab Marine Genet Resources, Fujian Key Lab Marine Genet Resources,Inst Oceanog, 178 Daxue Rd, Xiamen 361005, Fujian, Peoples R China;;[Ruan, Lingwei]Xiamen Ocean Vocat Coll, Coll Marine Biol, Xiamen 361100, Peoples R China;;[Ruan, Lingwei]Jiangsu Ocean Univ, Coinnovat Ctr Jiangsu Marine Bioind Technol, Lianyungang 222005, Peoples R China

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Source :

BMC GENOMICS

ISSN: 1471-2164

Year: 2023

Issue: 1

Volume: 24

3 . 5

JCR@2023

3 . 5 0 0

JCR@2023

ESI Discipline: MOLECULAR BIOLOGY & GENETICS;

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: 1

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