Degenerated vision, altered lipid metabolism, and expanded chemoreceptor repertoires enable Lindaspio polybranchiata to thrive in deep-sea cold seeps

Abstract Background Lindaspio polybranchiata, a member of the Spionidae family, has been reported at the Lingshui Cold Seep, where it formed a dense population around this nascent methane vent. We sequenced and assembled the genome of L. polybranchiata and performed comparative genomic analyses to i...

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Main Authors: Yujie Yan, Inge Seim, Yang Guo, Xupeng Chi, Zhaoshan Zhong, Dantong Wang, Mengna Li, Haining Wang, Huan Zhang, Minxiao Wang, Chaolun Li
Format: Article
Language:English
Published: BMC 2025-01-01
Series:BMC Biology
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Online Access:https://doi.org/10.1186/s12915-025-02112-2
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author Yujie Yan
Inge Seim
Yang Guo
Xupeng Chi
Zhaoshan Zhong
Dantong Wang
Mengna Li
Haining Wang
Huan Zhang
Minxiao Wang
Chaolun Li
author_facet Yujie Yan
Inge Seim
Yang Guo
Xupeng Chi
Zhaoshan Zhong
Dantong Wang
Mengna Li
Haining Wang
Huan Zhang
Minxiao Wang
Chaolun Li
author_sort Yujie Yan
collection DOAJ
description Abstract Background Lindaspio polybranchiata, a member of the Spionidae family, has been reported at the Lingshui Cold Seep, where it formed a dense population around this nascent methane vent. We sequenced and assembled the genome of L. polybranchiata and performed comparative genomic analyses to investigate the genetic basis of adaptation to the deep sea. Supporting this, transcriptomic and fatty acid data further corroborate our findings. Results We report the first genome of a deep-sea spionid, L. polybranchiata. Over long-term adaptive evolution, genes associated with vision and biological rhythmicity were lost, which may indirectly benefit oligotrophy by eliminating energetically costly processes. Compared to its shallow-sea relatives, L. polybranchiata has a significantly higher proportion of polyunsaturated fatty acids (PUFAs) and expanded gene families involved in the biosynthesis of unsaturated fatty acids and chromatin stabilization, possibly in response to high hydrostatic pressure. Additionally, L. polybranchiata has broad digestive scope, allowing it to fully utilize the limited food resources in the deep sea to sustain a large population. As a pioneer species, L. polybranchiata has an expanded repertoire of genes encoding potential chemoreceptor proteins, including ionotropic receptors (IRs) and gustatory receptor-like receptors (GRLs). These proteins, characterized by their conserved 3D structures, may enhance the organism’s ability to detect chemical cues in chemosynthetic ecosystems, facilitating rapid settlement in suitable environments. Conclusions Our results shed light on the adaptation of Lindaspio to the darkness, high hydrostatic pressure, and food deprivation in the deep sea, providing insights into the molecular basis for L. polybranchiata becoming a pioneer species.
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spelling doaj-art-875d30f01e014d1cb1e0153ce60508c82025-01-19T12:38:48ZengBMCBMC Biology1741-70072025-01-0123111810.1186/s12915-025-02112-2Degenerated vision, altered lipid metabolism, and expanded chemoreceptor repertoires enable Lindaspio polybranchiata to thrive in deep-sea cold seepsYujie Yan0Inge Seim1Yang Guo2Xupeng Chi3Zhaoshan Zhong4Dantong Wang5Mengna Li6Haining Wang7Huan Zhang8Minxiao Wang9Chaolun Li10CAS Key Laboratory of Marine Ecology and Environmental Sciences, and Center of Deep Sea Research, Institute of Oceanology, Chinese Academy of SciencesMarine Mammal and Marine Bioacoustics Laboratory, Institute of Deep-Sea Science and Engineering, Chinese Academy of SciencesCAS Key Laboratory of Marine Ecology and Environmental Sciences, and Center of Deep Sea Research, Institute of Oceanology, Chinese Academy of SciencesCAS Key Laboratory of Marine Ecology and Environmental Sciences, and Center of Deep Sea Research, Institute of Oceanology, Chinese Academy of SciencesCAS Key Laboratory of Marine Ecology and Environmental Sciences, and Center of Deep Sea Research, Institute of Oceanology, Chinese Academy of SciencesBGI ResearchCAS Key Laboratory of Marine Ecology and Environmental Sciences, and Center of Deep Sea Research, Institute of Oceanology, Chinese Academy of SciencesCAS Key Laboratory of Marine Ecology and Environmental Sciences, and Center of Deep Sea Research, Institute of Oceanology, Chinese Academy of SciencesCAS Key Laboratory of Marine Ecology and Environmental Sciences, and Center of Deep Sea Research, Institute of Oceanology, Chinese Academy of SciencesCAS Key Laboratory of Marine Ecology and Environmental Sciences, and Center of Deep Sea Research, Institute of Oceanology, Chinese Academy of SciencesCAS Key Laboratory of Marine Ecology and Environmental Sciences, and Center of Deep Sea Research, Institute of Oceanology, Chinese Academy of SciencesAbstract Background Lindaspio polybranchiata, a member of the Spionidae family, has been reported at the Lingshui Cold Seep, where it formed a dense population around this nascent methane vent. We sequenced and assembled the genome of L. polybranchiata and performed comparative genomic analyses to investigate the genetic basis of adaptation to the deep sea. Supporting this, transcriptomic and fatty acid data further corroborate our findings. Results We report the first genome of a deep-sea spionid, L. polybranchiata. Over long-term adaptive evolution, genes associated with vision and biological rhythmicity were lost, which may indirectly benefit oligotrophy by eliminating energetically costly processes. Compared to its shallow-sea relatives, L. polybranchiata has a significantly higher proportion of polyunsaturated fatty acids (PUFAs) and expanded gene families involved in the biosynthesis of unsaturated fatty acids and chromatin stabilization, possibly in response to high hydrostatic pressure. Additionally, L. polybranchiata has broad digestive scope, allowing it to fully utilize the limited food resources in the deep sea to sustain a large population. As a pioneer species, L. polybranchiata has an expanded repertoire of genes encoding potential chemoreceptor proteins, including ionotropic receptors (IRs) and gustatory receptor-like receptors (GRLs). These proteins, characterized by their conserved 3D structures, may enhance the organism’s ability to detect chemical cues in chemosynthetic ecosystems, facilitating rapid settlement in suitable environments. Conclusions Our results shed light on the adaptation of Lindaspio to the darkness, high hydrostatic pressure, and food deprivation in the deep sea, providing insights into the molecular basis for L. polybranchiata becoming a pioneer species.https://doi.org/10.1186/s12915-025-02112-2Deep-sea PolychaetaAdaptive evolutionHigh hydrostatic pressureVisual degenerationDigestive enzymesChemoreceptors
spellingShingle Yujie Yan
Inge Seim
Yang Guo
Xupeng Chi
Zhaoshan Zhong
Dantong Wang
Mengna Li
Haining Wang
Huan Zhang
Minxiao Wang
Chaolun Li
Degenerated vision, altered lipid metabolism, and expanded chemoreceptor repertoires enable Lindaspio polybranchiata to thrive in deep-sea cold seeps
BMC Biology
Deep-sea Polychaeta
Adaptive evolution
High hydrostatic pressure
Visual degeneration
Digestive enzymes
Chemoreceptors
title Degenerated vision, altered lipid metabolism, and expanded chemoreceptor repertoires enable Lindaspio polybranchiata to thrive in deep-sea cold seeps
title_full Degenerated vision, altered lipid metabolism, and expanded chemoreceptor repertoires enable Lindaspio polybranchiata to thrive in deep-sea cold seeps
title_fullStr Degenerated vision, altered lipid metabolism, and expanded chemoreceptor repertoires enable Lindaspio polybranchiata to thrive in deep-sea cold seeps
title_full_unstemmed Degenerated vision, altered lipid metabolism, and expanded chemoreceptor repertoires enable Lindaspio polybranchiata to thrive in deep-sea cold seeps
title_short Degenerated vision, altered lipid metabolism, and expanded chemoreceptor repertoires enable Lindaspio polybranchiata to thrive in deep-sea cold seeps
title_sort degenerated vision altered lipid metabolism and expanded chemoreceptor repertoires enable lindaspio polybranchiata to thrive in deep sea cold seeps
topic Deep-sea Polychaeta
Adaptive evolution
High hydrostatic pressure
Visual degeneration
Digestive enzymes
Chemoreceptors
url https://doi.org/10.1186/s12915-025-02112-2
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