Sulfur, sterol and trehalose metabolism in the deep-sea hydrocarbon seep tubeworm Lamellibrachia luymesi
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, metab...
| Main Authors: | , , , , , , |
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| Format: | Article |
| Language: | English |
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BMC
2023-04-01
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| Series: | BMC Genomics |
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| Online Access: | https://doi.org/10.1186/s12864-023-09267-8 |
| _version_ | 1797850184516894720 |
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| author | Hong Shi Lingwei Ruan Zimeng Chen Yifei Liao Wenhao Wu Linmin Liu Xun Xu |
| author_facet | Hong Shi Lingwei Ruan Zimeng Chen Yifei Liao Wenhao Wu Linmin Liu Xun Xu |
| author_sort | Hong Shi |
| collection | DOAJ |
| description | 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. |
| first_indexed | 2024-04-09T18:57:24Z |
| format | Article |
| id | doaj.art-b37c002bc51345709082323743919ba0 |
| institution | Directory Open Access Journal |
| issn | 1471-2164 |
| language | English |
| last_indexed | 2024-04-09T18:57:24Z |
| publishDate | 2023-04-01 |
| publisher | BMC |
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| series | BMC Genomics |
| spelling | doaj.art-b37c002bc51345709082323743919ba02023-04-09T11:08:45ZengBMCBMC Genomics1471-21642023-04-0124111810.1186/s12864-023-09267-8Sulfur, sterol and trehalose metabolism in the deep-sea hydrocarbon seep tubeworm Lamellibrachia luymesiHong Shi0Lingwei Ruan1Zimeng Chen2Yifei Liao3Wenhao Wu4Linmin Liu5Xun Xu6State 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 ResourcesState 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 ResourcesState 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 ResourcesState 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 ResourcesState 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 ResourcesState 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 ResourcesState 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 ResourcesAbstract 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.https://doi.org/10.1186/s12864-023-09267-8Adaptation to deep-sea chemosynthetic environmentCold seepTranscriptomeSulfateCysteineCholesterol |
| spellingShingle | Hong Shi Lingwei Ruan Zimeng Chen Yifei Liao Wenhao Wu Linmin Liu Xun Xu Sulfur, sterol and trehalose metabolism in the deep-sea hydrocarbon seep tubeworm Lamellibrachia luymesi BMC Genomics Adaptation to deep-sea chemosynthetic environment Cold seep Transcriptome Sulfate Cysteine Cholesterol |
| title | Sulfur, sterol and trehalose metabolism in the deep-sea hydrocarbon seep tubeworm Lamellibrachia luymesi |
| title_full | Sulfur, sterol and trehalose metabolism in the deep-sea hydrocarbon seep tubeworm Lamellibrachia luymesi |
| title_fullStr | Sulfur, sterol and trehalose metabolism in the deep-sea hydrocarbon seep tubeworm Lamellibrachia luymesi |
| title_full_unstemmed | Sulfur, sterol and trehalose metabolism in the deep-sea hydrocarbon seep tubeworm Lamellibrachia luymesi |
| title_short | Sulfur, sterol and trehalose metabolism in the deep-sea hydrocarbon seep tubeworm Lamellibrachia luymesi |
| title_sort | sulfur sterol and trehalose metabolism in the deep sea hydrocarbon seep tubeworm lamellibrachia luymesi |
| topic | Adaptation to deep-sea chemosynthetic environment Cold seep Transcriptome Sulfate Cysteine Cholesterol |
| url | https://doi.org/10.1186/s12864-023-09267-8 |
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