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

Jiao Cheng,Zhongli Sha,Min Hui

doi:10.1186/s12864-019-5753-7

Abstract

BackgroundHydrothermal 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.ResultsWe 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.ConclusionsWe 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.

Highlights

Hydrothermal vents and cold seeps are typical deep-sea chemosynthetically-driven ecosystems that allow high abundance of specialized macro-benthos
De novo assembly and functional annotation of S. crosnieri transcriptomes A total of 430,940,036 raw reads were generated from S. crosnieri transcriptomes, of which 222,129,956 raw reads from vent samples and 208,810,080 raw reads from seep samples
This study represented a first step in understanding the deep-sea adaptation mechanism of the galatheid squat lobster S. crosnieri at the molecular level, and provided a comprehensive transcriptomic resource for molecular studies of this species

Summary

Introduction

Hydrothermal vents and cold seeps are typical deep-sea chemosynthetically-driven ecosystems that allow high abundance of specialized macro-benthos. 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. 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. The discoveries of chemosynthetic ecosystems (hydrothermal vents, cold seeps and other deep-sea sites of organic enrichment) have revolutionized our perceptions of life in the deep sea [1]. Despite sharing the similar process of chemosynthesis, hydrothermal vents seem more severe and ephemeral than cold seeps as environments for organisms [3]. Apart from geological settings and the chemicals used for energy, hydrothermal vents have an appreciable temperature gradient from the maximum of emitting hot water (ca. 350 °C) to the minimum of ambient cold water (2 °C–3 °C), but no such gradient in cold seeps [7]

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