Venom-gland transcriptomic, venomic, and antivenomic profiles of the spine-bellied sea snake (Hydrophis curtus) from the South China Sea

Abstract Background A comprehensive evaluation of the -omic profiles of venom is important for understanding the potential function and evolution of snake venom. Here, we conducted an integrated multi-omics-analysis to unveil the venom-transcriptomic and venomic profiles in a same group of spine-bel...

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Main Authors: Hong-Yan Zhao, Lin Wen, Yu-Feng Miao, Yu Du, Yan Sun, Yin Yin, Chi-Xian Lin, Long-Hui Lin, Xiang Ji, Jian-Fang Gao
Format: Article
Language:English
Published: BMC 2021-07-01
Series:BMC Genomics
Subjects:
Online Access:https://doi.org/10.1186/s12864-021-07824-7
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record_format Article
collection DOAJ
language English
format Article
sources DOAJ
author Hong-Yan Zhao
Lin Wen
Yu-Feng Miao
Yu Du
Yan Sun
Yin Yin
Chi-Xian Lin
Long-Hui Lin
Xiang Ji
Jian-Fang Gao
spellingShingle Hong-Yan Zhao
Lin Wen
Yu-Feng Miao
Yu Du
Yan Sun
Yin Yin
Chi-Xian Lin
Long-Hui Lin
Xiang Ji
Jian-Fang Gao
Venom-gland transcriptomic, venomic, and antivenomic profiles of the spine-bellied sea snake (Hydrophis curtus) from the South China Sea
BMC Genomics
Omics
Hydrophis curtus
Snake venom
Transcriptome
Proteome
Antivenomic
author_facet Hong-Yan Zhao
Lin Wen
Yu-Feng Miao
Yu Du
Yan Sun
Yin Yin
Chi-Xian Lin
Long-Hui Lin
Xiang Ji
Jian-Fang Gao
author_sort Hong-Yan Zhao
title Venom-gland transcriptomic, venomic, and antivenomic profiles of the spine-bellied sea snake (Hydrophis curtus) from the South China Sea
title_short Venom-gland transcriptomic, venomic, and antivenomic profiles of the spine-bellied sea snake (Hydrophis curtus) from the South China Sea
title_full Venom-gland transcriptomic, venomic, and antivenomic profiles of the spine-bellied sea snake (Hydrophis curtus) from the South China Sea
title_fullStr Venom-gland transcriptomic, venomic, and antivenomic profiles of the spine-bellied sea snake (Hydrophis curtus) from the South China Sea
title_full_unstemmed Venom-gland transcriptomic, venomic, and antivenomic profiles of the spine-bellied sea snake (Hydrophis curtus) from the South China Sea
title_sort venom-gland transcriptomic, venomic, and antivenomic profiles of the spine-bellied sea snake (hydrophis curtus) from the south china sea
publisher BMC
series BMC Genomics
issn 1471-2164
publishDate 2021-07-01
description Abstract Background A comprehensive evaluation of the -omic profiles of venom is important for understanding the potential function and evolution of snake venom. Here, we conducted an integrated multi-omics-analysis to unveil the venom-transcriptomic and venomic profiles in a same group of spine-bellied sea snakes (Hydrophis curtus) from the South China Sea, where the snake is a widespread species and might generate regionally-specific venom potentially harmful to human activities. The capacity of two heterologous antivenoms to immunocapture the H. curtus venom was determined for an in-depth evaluation of their rationality in treatment of H. curtus envenomation. In addition, a phylogenetic analysis by maximum likelihood was used to detect the adaptive molecular evolution of full-length toxin-coding unigenes. Results A total of 90,909,384 pairs of clean reads were generated via Illumina sequencing from a pooled cDNA library of six specimens, and yielding 148,121 unigenes through de novo assembly. Sequence similarity searching harvested 63,845 valid annotations, including 63,789 non-toxin-coding and 56 toxin-coding unigenes belonging to 22 protein families. Three protein families, three-finger toxins (3-FTx), phospholipase A2 (PLA2), and cysteine-rich secretory protein, were detected in the venom proteome. 3-FTx (27.15% in the transcriptome/41.94% in the proteome) and PLA2 (59.71%/49.36%) were identified as the most abundant families in the venom-gland transcriptome and venom proteome. In addition, 24 unigenes from 11 protein families were shown to have experienced positive selection in their evolutionary history, whereas four were relatively conserved throughout evolution. Commercial Naja atra antivenom exhibited a stronger capacity than Bungarus multicinctus antivenom to immunocapture H. curtus venom components, especially short neurotoxins, with the capacity of both antivenoms to immunocapture short neurotoxins being weaker than that for PLA2s. Conclusions Our study clarified the venom-gland transcriptomic and venomic profiles along with the within-group divergence of a H. curtus population from the South China Sea. Adaptive evolution of most venom components driven by natural selection appeared to occur rapidly during evolutionary history. Notably, the utility of commercial N. atra and B. multicinctus antivenoms against H. curtus toxins was not comprehensive; thus, the development of species-specific antivenom is urgently needed.
topic Omics
Hydrophis curtus
Snake venom
Transcriptome
Proteome
Antivenomic
url https://doi.org/10.1186/s12864-021-07824-7
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spelling doaj-14419c2dc3d441f4862d55d47b554b502021-07-11T11:32:31ZengBMCBMC Genomics1471-21642021-07-0122112210.1186/s12864-021-07824-7Venom-gland transcriptomic, venomic, and antivenomic profiles of the spine-bellied sea snake (Hydrophis curtus) from the South China SeaHong-Yan Zhao0Lin Wen1Yu-Feng Miao2Yu Du3Yan Sun4Yin Yin5Chi-Xian Lin6Long-Hui Lin7Xiang Ji8Jian-Fang Gao9Hangzhou Key Laboratory for Animal Adaptation and Evolution, College of Life and Environmental Sciences, Hangzhou Normal UniversityHangzhou Key Laboratory for Animal Adaptation and Evolution, College of Life and Environmental Sciences, Hangzhou Normal UniversityHangzhou Key Laboratory for Animal Adaptation and Evolution, College of Life and Environmental Sciences, Hangzhou Normal UniversityHainan Key Laboratory of Herpetological Research, College of Fisheries and Life Science, Hainan Tropical Ocean UniversityHangzhou Key Laboratory for Animal Adaptation and Evolution, College of Life and Environmental Sciences, Hangzhou Normal UniversityHangzhou Key Laboratory for Animal Adaptation and Evolution, College of Life and Environmental Sciences, Hangzhou Normal UniversityHainan Key Laboratory of Herpetological Research, College of Fisheries and Life Science, Hainan Tropical Ocean UniversityHangzhou Key Laboratory for Animal Adaptation and Evolution, College of Life and Environmental Sciences, Hangzhou Normal UniversityMOE Key Laboratory of Utilization and Conservation for Tropical Marine Bioresources, Hainan Tropical Ocean UniversityHangzhou Key Laboratory for Animal Adaptation and Evolution, College of Life and Environmental Sciences, Hangzhou Normal UniversityAbstract Background A comprehensive evaluation of the -omic profiles of venom is important for understanding the potential function and evolution of snake venom. Here, we conducted an integrated multi-omics-analysis to unveil the venom-transcriptomic and venomic profiles in a same group of spine-bellied sea snakes (Hydrophis curtus) from the South China Sea, where the snake is a widespread species and might generate regionally-specific venom potentially harmful to human activities. The capacity of two heterologous antivenoms to immunocapture the H. curtus venom was determined for an in-depth evaluation of their rationality in treatment of H. curtus envenomation. In addition, a phylogenetic analysis by maximum likelihood was used to detect the adaptive molecular evolution of full-length toxin-coding unigenes. Results A total of 90,909,384 pairs of clean reads were generated via Illumina sequencing from a pooled cDNA library of six specimens, and yielding 148,121 unigenes through de novo assembly. Sequence similarity searching harvested 63,845 valid annotations, including 63,789 non-toxin-coding and 56 toxin-coding unigenes belonging to 22 protein families. Three protein families, three-finger toxins (3-FTx), phospholipase A2 (PLA2), and cysteine-rich secretory protein, were detected in the venom proteome. 3-FTx (27.15% in the transcriptome/41.94% in the proteome) and PLA2 (59.71%/49.36%) were identified as the most abundant families in the venom-gland transcriptome and venom proteome. In addition, 24 unigenes from 11 protein families were shown to have experienced positive selection in their evolutionary history, whereas four were relatively conserved throughout evolution. Commercial Naja atra antivenom exhibited a stronger capacity than Bungarus multicinctus antivenom to immunocapture H. curtus venom components, especially short neurotoxins, with the capacity of both antivenoms to immunocapture short neurotoxins being weaker than that for PLA2s. Conclusions Our study clarified the venom-gland transcriptomic and venomic profiles along with the within-group divergence of a H. curtus population from the South China Sea. Adaptive evolution of most venom components driven by natural selection appeared to occur rapidly during evolutionary history. Notably, the utility of commercial N. atra and B. multicinctus antivenoms against H. curtus toxins was not comprehensive; thus, the development of species-specific antivenom is urgently needed.https://doi.org/10.1186/s12864-021-07824-7OmicsHydrophis curtusSnake venomTranscriptomeProteomeAntivenomic