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Exploring the molecular basis of adaptive evolution in hydrothermal vent crab Austinograea alayseae by transcriptome analysis.

ABSTRACT: Elucidating the genetic mechanisms of adaptation to the hydrothermal vent in organisms at genomic level is significant for understanding the adaptive evolution process in the extreme environment. We performed RNA-seq on four different tissues of a vent crab species, Austinograea alayseae, producing 725,461 unigenes and 134,489 annotated genes. Genes related to sensory, circadian rhythm, hormone, hypoxia stress, metal detoxification and immunity were identified. It was noted that in the degenerated eyestalk, transcription of phototransduction related genes which are important for retinal function was greatly reduced; three crucial neuropeptide hormones, one molt-inhibiting and two crustacean hyperglycemic hormone precursors were characterized with conserved domains; hypoxia-inducible factor 1 and two novel isoforms of metallothioneins in the vent crabs were discovered. An analysis of 6,932 orthologs among three crabs A. alayseae, Portunus trituberculutus and Eriocheir sinensis revealed 19 positive selected genes (PSGs). Most of the PSGs were involved in immune responses, such as crustins and anti-lipopolysaccharide factor, suggesting their function in the adaptation to environment. The characterization of the first vent crab transcriptome provides abundant resources for genetic and evolutionary studies of this species, and paves the way for further investigation of vent adaptation process in crabs.

SUBMITTER: Hui M

PROVIDER: S-EPMC5446156 | biostudies-literature | 2017

REPOSITORIES: biostudies-literature

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Exploring the molecular basis of adaptive evolution in hydrothermal vent crab Austinograea alayseae by transcriptome analysis.

Hui Min M Song Chengwen C Liu Yuan Y Li Chaolun C Cui Zhaoxia Z

PloS one 20170526 5

Elucidating the genetic mechanisms of adaptation to the hydrothermal vent in organisms at genomic level is significant for understanding the adaptive evolution process in the extreme environment. We performed RNA-seq on four different tissues of a vent crab species, Austinograea alayseae, producing 725,461 unigenes and 134,489 annotated genes. Genes related to sensory, circadian rhythm, hormone, hypoxia stress, metal detoxification and immunity were identified. It was noted that in the degenerat ...[more]

PMID: 28552991

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Project description:Deep-sea hydrothermal vent communities are dominated by invertebrates, namely, bathymodiolin mussels, siboglinid tubeworms, and provannid snails. Symbiosis is considered key to successful colonization by these sedentary species in such extreme environments. In the PACManus vent fields, snails, tubeworms, and mussels each colonized a niche with distinct geochemical characteristics. To better understand the metabolic potentials and genomic features contributing to host-environment adaptation, we compared the genomes of the symbionts of Bathymodiolus manusensis, Arcovestia ivanovi, and Alviniconcha boucheti sampled at PACManus, and we discuss their environmentally adaptive features. We found that B. manusensis and A. ivanovi are colonized by Gammaproteobacteria from distinct clades, whereas endosymbionts of B. manusensis feature high intraspecific heterogeneity with differing metabolic potentials. A. boucheti harbored three novel Epsilonproteobacteria symbionts, suggesting potential species-level diversity of snail symbionts. Genome comparisons revealed that the relative abundance of gene families related to low-pH homeostasis, metal resistance, oxidative stress resistance, environmental sensing/responses, and chemotaxis and motility was the highest in A. ivanovi's symbiont, followed by symbionts of the vent-mouth-dwelling snail A. boucheti, and was relatively low in the symbiont of the vent-periphery-dwelling mussel B. manusensis, which is consistent with their environmental adaptations and host-symbiont interactions. Gene families classified as encoding host interaction/attachment, virulence factors/toxins, and eukaryotic-like proteins were most abundant in symbionts of mussels and least abundant in those of snails, indicating that these symbionts may differ in their host colonization strategies. Comparison of Epsilonproteobacteria symbionts to nonsymbionts demonstrated that the expanded gene families in symbionts were related to vitamin B12 synthesis, toxin-antitoxin systems, methylation, and lipopolysaccharide biosynthesis, suggesting that these are vital to symbiont establishment and development in Epsilonproteobacteria IMPORTANCE Deep-sea hydrothermal vents are dominated by several invertebrate species. The establishment of symbiosis has long been thought to be the key to successful colonization by these sedentary species in such harsh environments. However, the relationships between symbiotic bacteria and their hosts and their role in environmental adaptations generally remain unclear. In this paper, we show that the distribution of three host species showed characteristic niche partitioning in the Manus Basin, giving us the opportunity to understand how they adapt to their particular habitats. This study also revealed three novel genomes of symbionts from the snails of A. boucheti Combined with a data set on other ectosymbiont and free-living bacteria, genome comparisons for the snail endosymbionts pointed to several genetic traits that may have contributed to the lifestyle shift of Epsilonproteobacteria into the epithelial cells. These findings could increase our understanding of invertebrate-endosymbiont relationships in deep-sea ecosystems.

Dataset Information

Exploring the molecular basis of adaptive evolution in hydrothermal vent crab Austinograea alayseae by transcriptome analysis.

Publications

Exploring the molecular basis of adaptive evolution in hydrothermal vent crab Austinograea alayseae by transcriptome analysis.

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