Insights into the strategy of micro-environmental adaptation: Transcriptomic analysis of two alvinocaridid shrimps at a hydrothermal vent

Abstract

Diffusing fluid at a deep-sea hydrothermal vent creates rapid, acute physico-chemical gradients that correlate strongly with the distribution of the vent fauna. Two alvinocaridid shrimps, Alvinocaris longirostris and Shinkaicaris leurokolos occupy distinct microhabitats around these vents and exhibit different thermal preferences. S. leurokolos inhabits the central area closer to the active chimney, while A. longirostris inhabits the peripheral area. In this study, we screened candidate genes that might be involved in niche separation and microhabitat adaptation through comparative transcriptomics. The results showed that among the top 20% of overexpressed genes, gene families related to protein synthesis and structural components were much more abundant in S. leurokolos compared to A. longirostris. Moreover, 15 out of 25 genes involved in cellular carbohydrate metabolism were related to trehalose biosynthesis, versus 1 out of 5 in A. longirostris. Trehalose, a non-reducing disaccharide, is a multifunctional molecule and has been proven to act as a protectant responsible for thermotolerance in Saccharomyces cerevisiae. Putative positively selected genes involved in chitin metabolism and the immune system (lectin, serine protease and antimicrobial peptide) were enriched in S. leurokolos. In particular, one collagen and two serine proteases were found to have experienced strong positive selection. In addition, sulfotransferase-related genes were both overexpressed and positively selected in S. leurokolos. Finally, genes related to structural proteins, immune proteins and protectants were overexpressed or positively selected. These characteristics could represent adaptations of S. leurokolos to its microhabitat, which need to be confirmed by more evidence, such as data from large samples and different development stages of these alvinocaridid shrimps.

Fig 1

Maximum-likelihood phylogenetic tree of alvinocaridid shrimps based on COI (A) and 16S rRNA (B) genes. The sequences in red are from this study. Statistical supports is indicated as bootstrap values, and the values of less than 50 are omitted. Subfamilies are masked by different colours: Alvinocaridinae (blue), Mirocaridinae (yellow), Rimicaridinae (green). Heterocarpus ensifer (family: Pandalidae) serves as the outgroup. Accession numbers are labeled in parentheses. The tree scale bar represents the number of expected substitutions per site.

Fig 2. Validation of gene expression by absolute qPCR.

Six single-copy orthologues for each species were randomly selected and quantified in the cephalothorax of S. leurokolos (A), abdomen of S. leurokolos (B), cephalothorax of A. longirostris (C) and abdomen of A. longirostris (D). The histograms show the gene copy number per μl (mean ± SD) with three technical replicates quantified by qPCR. The line charts show the TPM value quantified with RSEM software. Gene names are indicated on the x-axis.