Transcriptomic analysis reveals insights into deep-sea adaptations of the dominant species, Shinkaia crosnieri (Crustacea: Decapoda: Anomura), inhabiting both hydrothermal vents and cold seeps

Abstract

Background Hydrothermal vents and cold seeps are typical deep-sea chemosynthetically-driven ecosystems that allow high abundance of specialized macro-benthos. To gather knowledge about the genetic basis of adaptation to these extreme environments, species shared between different habitats, especially for the dominant species, are of particular interest. The galatheid squat lobster, Shinkaia crosnieri Baba and Williams, 1998, is one of the few dominant species inhabiting both deep-sea hydrothermal vents and cold seeps. In this study, we performed transcriptome analyses of S. crosnieri collected from the Iheya North hydrothermal vent (HV) and a cold seep in the South China Sea (CS) to provide insights into how this species has evolved to thrive in different deep-sea chemosynthetic ecosystems. Results We analyzed 5347 orthologs between HV and CS to identify genes under positive selection through the maximum likelihood approach. A total of 82 genes were identified to be positively selected and covered diverse functional categories, potentially indicating their importance for S. crosnieri to cope with environmental heterogeneity between deep-sea vents and seeps. Among 39,806 annotated unigenes, a large number of differentially expressed genes (DEGs) were identified between HV and CS, including 339 and 206 genes significantly up-regulated in HV and CS, respectively. Most of the DEGs associated with stress response and immunity were up-regulated in HV, possibly allowing S. crosnieri to increase its capability to manage more environmental stresses in the hydrothermal vents. Conclusions We provide the first comprehensive transcriptomic resource for the deep-sea squat lobster, S. crosnieri , inhabiting both hydrothermal vents and cold seeps. A number of stress response and immune-related genes were positively selected and/or differentially expressed, potentially indicating their important roles for S. crosnieri to thrive in both deep-sea vents and cold seeps. Our results indicated that genetic adaptation of S. crosnieri to different deep-sea chemosynthetic environments might be mediated by adaptive evolution of functional genes related to stress response and immunity, and alterations in their gene expression that lead to different stress resistance. However, further work is required to test these proposed hypotheses. All results can constitute important baseline data for further studies towards elucidating the adaptive mechanisms in deep-sea crustaceans. Electronic supplementary material The online version of this article (10.1186/s12864-019-5753-7) contains supplementary material, which is available to authorized users.

Population Genetic Structure and Gene Expression Plasticity of the Deep-Sea Vent and Seep Squat Lobster Shinkaia crosnieri

“…Although the samples we used were different from those used in Cheng et al (2019), some DEGs identified in our study showed the same expression patterns as in Cheng et al (2019), including cystathionine gamma-lyase (CSE) and heat shock protein 22 (HSP) ( Table 6), indicating they might reflect true differences between the two populations. Nevertheless, subsampling of our data clearly revealed a requirement of a larger sample size to capture the DEGs of the two populations ( Figure 6A).…”

“…Afterward, comparison was conducted to determine an appropriate sample size for the reliable DEGs. In addition, DEGs obtained in our study were also compared with those reported in Cheng et al (2019).…”

“…When only three replicates were used in a simulation with our data, only about half of the DEGs were detected. Moreover, when less data per sample were available (2.3 Gb of 100-bp data) (Cheng et al, 2019), even fewer DEGs (545) could be detected. Our results are consistent with the results of another study that indicated at least six replicates should be used in order to obtain sufficient DEGs for a study of the treatment effects (Schurch et al, 2016).…”

“…Indeed, Cheng et al (2020) identified 54 outlier SNPs potentially under positive selection, but only five were in the protein-coding regions. More recently, Cheng et al (2019) compared the transcriptomes of S. crosnieri collected from the same seep and vent populations, but with only three individuals from each population. They detected 545 differentially expressed genes (DEGs) and 82 protein-coding genes (PCGs) that have potentially undergone positive selection.…”

Adaptations to thermal stress in social insects: recent advances and future directions

“…genetic diversity, isoforms, molecular functions, and cellular functions) and quantitative (e.g. the number of genes that are differentially expressed) differences in responses to environmental pressures in a variety of organisms, including plants, insects, molluscs, crustaceans, and fish (Ye et al ., 2014; Zhao et al ., 2014; Cañas et al ., 2015; Faddeeva et al ., 2015; Cheng, Hui, & Sha, 2019; Jesus et al ., 2019). In recent years, DGE studies in social insects have highlighted a number of genes that are involved in colony organisation and adaptation to environmental constraints (Ferreira et al ., 2013; Helmkampf et al ., 2016; Lucas, Romiguier, & Keller, 2017; Willot et al ., 2018; Holman et al ., 2019).…”