Comparative transcriptome analysis reveals changes in gene expression in sea cucumber (Holothuria leucospilota) in response to acute temperature stress

Li, Changlin; Zhao, Wang; Qin, Chuanxin; Yu, Gang; Ma, Zhenhua; Guo, Yu; Pan, Wanni; Fu, Zhengyi; Huang, Xingmei; Chen, Jisheng

doi:10.1016/j.cbd.2021.100883

Cited by 14 publications

(9 citation statements)

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“…We find that genes involved in energy-releasing catabolic pathways, including the citric acid cycle, fatty acid metabolism and free amino acids pathways, are consistently upregulated in the four tissues in captive COTS, suggesting an increased energy demand. The upregulation of energy metabolic pathways has been observed in marine organisms under environmental stress (Meng et al, 2013; Shekhar et al, 2013; Hui et al, 2014; Nie et al, 2017; Ma et al, 2019; Li et al, 2021) and in captive mussels (Roznere et al, 2021). Given that energy demand appears to decrease under severe stress in some animals (Sokolova et al, 2012), we suggest the apparent increased demand we observe here may reflect a state of moderate chronic stress in these starfish.…”

Section: Discussionmentioning

confidence: 99%

“…Genome-wide transcriptome analysis using RNA sequencing (RNA-Seq) is a highly sensitive approach that provides near-comprehensive quantification of changes in gene expression under different environmental conditions (Wang et al, 2009). Although RNA-Seq has been widely applied to studying responses of diverse animals to specific environmental stressors (Lv et al, 2013; Meng et al, 2013; Milan et al, 2013; Hui et al, 2014; Gleason and Burton, 2015; Oomen and Hutchings, 2017; Zhang et al, 2017; Wang et al, 2018; Li et al, 2019; Ma et al, 2019; Li et al, 2021), it has rarely been applied in the context of captivity (Alburaki et al, 2019; Roznere et al, 2021).…”

Section: Introductionmentioning

confidence: 99%

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Crown-of-thorns starfish in captivity experience sustained large-scale changes in gene expression

Morin

Jönsson

Wang

et al. 2022

Preprint

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Marine animals in the wild are often difficult to access, so that biologists have to extrapolate from the study of animals in captivity. However, the implicit assumption that physiological and cellular processes of animals in artificial environments are not significantly different from those in the wild has rarely been tested. Here we investigate the extent to which the biological state of an animal is impacted by captivity by comparing global gene expression in wild and captive crown-of-thorns starfish (COTS). We compare transcriptomes of three external tissues obtained from wild COTS with captive COTS maintained in aquaria for at least one week. On average, an astonishingly large 24% of the coding sequences in the genome are differentially expressed. Comparing transcriptomes from coelomocytes – cells in internal coelomic fluid – in wild and captive COTS, we find that 20% of the coding sequences in the genome rapidly change expression. These captive transcriptomes remained markedly different from the wild ones for more than 30 days in captivity, and showed no indication of reverting back to a wild state. Genes consistently upregulated in captivity include those involved in oxidative stress and energy metabolism, whereas genes downregulated are involved in intercellular signalling. These extensive changes in gene expression in captive COTS suggest that captivity has a profound and sustained impact on the physiology, behaviour and health of these echinoderms. The potential for such dramatic changes should be accounted for when designing studies seeking to understand wild animals.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Crown-of-thorns starfish in captivity experience sustained large-scale changes in gene expression

Morin

Jönsson

Wang

et al. 2022

Preprint

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“…In fact, several Hsp have been characterized from different sea cucumber species. Among these are Hsp 90, Hsp 70, Hsp 60 and members of the small Hsp family [28][29] [30][31] [32]. These genes have been reported to be expressed by cells in the intestine, coelomocytes and many other tissues.…”

Section: Heat Shock Proteinsmentioning

confidence: 99%

Molecular Characterization of the Stress Response of the Holothurian Central Nervous System

Cruz-González¹,

Quesada-Díaz²,

Miranda-Negrón³

et al. 2022

Preprint

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Injury to the central nervous system (CNS), in most vertebrate animals, results in permanent damage and lack of function, due to their limited regenerative capacities. In contrast, echinoderms can fully regenerate their radial nerve cord (RNC) following transection, with little or no scarring. Investigators have associated the regenerative capacity of some organisms with the stress response and inflammation produced by the injury. Here we explore the gene activation profile of the stressed holothurian CNS. To do this, we performed RNA sequencing on isolated RNC explants submitted to the stress of transection and enzyme dissection and compared them to explants kept in culture for 3 days following dissection. We describe stress-associated genes, including members of heat-shock families, ubiquitin-related pathways, transposons, and apoptosis that were differentially expressed. Surprisingly, the stress response does not induce apoptosis in this system. Other genes associated with stress in other animal models, such as hero proteins and those associated with the integrated stress response, were not found to be differentially expressed either. Our results provide a new viewpoint on the stress response in the nervous system of an organism with an amazing regenerative capacity. This is the first step to deciphering the molecular processes that allow echinoderms to undergo fully functional CNS regeneration while also providing a comparative view for students of the stress response in other organisms.

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“…In recent years, the RNA-Seq method has been widely adopted to investigate the gene response of aquatic animals to temperature stress ( Samanta et al, 2006 ; Jiang et al, 2014 ; Wang et al, 2019 ). Studies over the past 5 years have provided important information on the gene expressions of echinoderms that were exposed to temperature stress, and the RNA-Seq results have been used to identify a number of candidate genes associated with the immune response, apoptosis pathway, and metabolic pathways, such as those of the heat shock proteins ( HSPs ), calmodulin-1 ( Cam1 ), cyclophilins ( Cyps ) ( Gonzalez et al, 2017 ; Li et al, 2019 ; Shi et al, 2020 ; Li et al, 2021 ). MicroRNAs (miRNAs) are thecriticaly regulators of post-transcriptional gene expression, and they perform important roles in various biological functions such as metabolism, immunity and development ( Bartel, 2004 ; Nigam, 2014 ; Stepicheva and Song, 2015 ; Pan et al, 2021 ).…”

Section: Introductionmentioning

confidence: 99%

Expression Regulation Mechanisms of Sea Urchin (Strongylocentrotus intermedius) Under the High Temperature: New Evidence for the miRNA-mRNA Interaction Involvement

Han

Quan

et al. 2022

Front. Genet.

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In the context of global warming and continuous high temperatures in the northern part of China during summer, the mortality rate of our main breeding species, Strongylocentrotus intermedius, reached 80% in 2020. How sea urchins respond to high temperatures is of great concern to academia and industry. In this study, we examined the antioxidant enzyme activities of different color tube-footed sea urchins under heat stress and compared their transcriptome and microRNA (miRNA) profiles using RNA-Seq. The results showed that the antioxidant enzyme activities of sea urchins were altered by thermal stress, and the changes in peroxidase activities of red tube-footed sea urchins were particularly significant. Investigations revealed that 1,079 differentially expressed genes (DEGs), 11 DE miRNAs, and 104 “DE miRNA-DEG” pairs in total were detected in sea urchins under high temperature stress. Several mRNA and miRNAs were significantly changed (e.g. HSP70, DnaJ11, HYAL, CALR, miR-184-p5, miR-92a, miR-92c, and miR-124-p5), suggesting these genes and miRNAs exerted important functions in response to high temperature. At the transcriptional level, red tube-footed sea urchins were found to be more sensitive to high temperature and could respond to high temperature rapidly. DE miRNA-mRNA network showed that miR-92b-3p and PC-5p-7420 were the most corresponding miRNAs. Five mRNAs (DnaJ11, SAR1B, CALR, HYOU1, TUBA) may be potential markers of sea urchin response to high temperature. Possible interaction between miRNA-mRNA could be linked to protein folding in the endoplasmic reticulum, Phagosomes, and calcium transport. This study provides a theoretical basis for the molecular mechanism of sea urchin heat tolerance and information that will aid in the selection and breeding of sea urchins with high temperature tolerance.

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Comparative transcriptome analysis reveals changes in gene expression in sea cucumber (Holothuria leucospilota) in response to acute temperature stress

Cited by 14 publications

References 50 publications

Crown-of-thorns starfish in captivity experience sustained large-scale changes in gene expression

Crown-of-thorns starfish in captivity experience sustained large-scale changes in gene expression

Molecular Characterization of the Stress Response of the Holothurian Central Nervous System

Expression Regulation Mechanisms of Sea Urchin (Strongylocentrotus intermedius) Under the High Temperature: New Evidence for the miRNA-mRNA Interaction Involvement

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