Reproductive adaptations of the hydrothermal vent crab Xenograpus testudinatus: An isotopic approach.
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ABSTRACT:
SUBMITTER: Hung JJ
PROVIDER: S-EPMC6366749 | biostudies-literature |
REPOSITORIES: biostudies-literature
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Project description:Shallow-water hydrothermal vents off Kueishan Island (northeastern Taiwan) provide a unique, sulfur-rich, highly acidic (pH 1.75-4.6) and variable-temperature environment. In this species-poor habitat, the crab Xenograpsus testudinatus is dominant, as it mainly feeds on zooplankton killed by sulfurous plumes. In this study, 16S ribosomal RNA gene amplicon pyrosequencing was used to investigate diversity and composition of bacteria residing in digestive gland, gill, stomach, heart, and mid-gut of X. testudinatus, as well as in surrounding seawater. Dominant bacteria were Gamma- and Epsilonproteobacteria that might be capable of autotrophic growth by oxidizing reduced sulfur compounds and are usually resident in deep-sea hydrothermal systems. Dominant bacterial OTUs in X. testudinatus had both host and potential organ specificities, consistent with a potential trophic symbiotic relationship (nutrient transfer between host and bacteria). We inferred that versatile ways to obtain nutrients may provide an adaptive advantage for X. testudinatus in this demanding environment. To our knowledge, this is the first study of bacterial communities in various organs/tissues of a crustacean in a shallow-water hydrothermal system, and as such, may be a convenient animal model for studying these systems.
| S-EPMC4774926 | biostudies-literature
Project description:The sulphur-rich and acidic vent waters of a shallow hydrothermal vent field next to Kueishan Island in Taiwan provide a specific and generally toxic environment. Among only a few aquatic organisms able to survive there, the grapsoid crab Xenograpsus testudinatus is the dominant species with a high population density in the vent area. Here we study the gender-specific distribution, morphological traits, and relationship of wet weight vs. carapace width of this crab. A total of 1120 individuals including 831 male and 289 female (included 15 ovigerous) were examined during August and September in 2011 and May and September in 2012. Except in August 2011, there are no significant differences in the distribution of X. testudinatus in the hydrothermal vent area from the vent spout during most months. Among crabs, the weight of male (6.87 ± 2.90 g) was significantly heavier than that of females (4.17 ± 1.25 g) (p < 0.001, Student's t-test). As for the wet weight of crabs, significant differences were noted in both the length of chela and the width of carapace between males and females. Sexual dimorphism of X. testudinatus is evident in three morphological traits. Pearson's correlation showed a significant and positive correlation (p < 0.001) of wet weight, width of carapace and length of chela of the two sexes. Ovigerous crabs (shortest carapace width: 1.93 cm) were present in the specimen collected from August 2011 and May 2012. The ovigerous crabs were not found in the samples collected from September in both years 2011 and 2012, indicating that reproduction may have ceased during the period of sampling. The present results suggested that the reproductive period of X. testudinatus was before September. The distribution pattern and sexual dimorphism of X. testudinatus provided a better understanding of the idiobiology of this dominant metazoan in the hydrothermal vent area.
| S-EPMC7098652 | biostudies-literature
Project description:Shallow hydrothermal vent environments are typically very warm and acidic due to the mixing of ambient seawater with volcanic gasses (> 92% CO2) released through the seafloor making them potential 'natural laboratories' to study long-term adaptations to extreme hypercapnic conditions. Xenograpsus testudinatus, the shallow hydrothermal vent crab, is the sole metazoan inhabitant endemic to vents surrounding Kueishantao Island, Taiwan, where it inhabits waters that are generally pH 6.50 with maximum acidities reported as pH 5.50. This study assessed the acid-base regulatory capacity and the compensatory response of X. testudinatus to investigate its remarkable physiological adaptations. Hemolymph parameters (pH, [HCO3-], [Formula: see text], [NH4+], and major ion compositions) and the whole animal's rates of oxygen consumption and ammonia excretion were measured throughout a 14-day acclimation to pH 6.5 and 5.5. Data revealed that vent crabs are exceptionally strong acid-base regulators capable of maintaining homeostatic pH against extreme hypercapnia (pH 5.50, 24.6 kPa [Formula: see text]) via HCO3-/Cl- exchange, retention and utilization of extracellular ammonia. Intact crabs as well as their isolated perfused gills maintained [Formula: see text]tensions below environmental levels suggesting the gills can excrete CO2 against a hemolymph-directed [Formula: see text] gradient. These specialized physiological mechanisms may be amongst the adaptations required by vent-endemic animals surviving in extreme conditions.
| S-EPMC7367285 | biostudies-literature
Project description:Hydrothermal vent organisms have evolved physiological adaptations to cope with extreme abiotic conditions including temperature and pH. To date, acid-base regulatory abilities of vent organisms are poorly investigated, although this physiological feature is essential for survival in low pH environments. We report the acid-base regulatory mechanisms of a hydrothermal vent crab, Xenograpsus testudinatus, endemic to highly acidic shallow-water vent habitats with average environment pH-values ranging between 5.4 and 6.6. Within a few hours, X. testudinatus restores extracellular pH (pHe) in response to environmental acidification of pH 6.5 (1.78 kPa pCO2) accompanied by an increase in blood [Formula: see text] levels from 8.8 ± 0.3 to 31 ± 6 mM. Branchial Na(+)/K(+)-ATPase (NKA) and V-type H(+)-ATPase (VHA), the major ion pumps involved in branchial acid-base regulation, showed dynamic increases in response to acidified conditions on the mRNA, protein and activity level. Immunohistochemical analyses demonstrate the presence of NKA in basolateral membranes, whereas the VHA is predominantly localized in cytoplasmic vesicles of branchial epithelial- and pillar-cells. X. testudinatus is closely related to other strong osmo-regulating brachyurans, which is also reflected in the phylogeny of the NKA. Accordingly, our results suggest that the evolution of strong ion regulatory abilities in brachyuran crabs that allowed the occupation of ecological niches in euryhaline, freshwater, and terrestrial habitats are probably also linked to substantial acid-base regulatory abilities. This physiological trait allowed X. testudinatus to successfully inhabit one of the world's most acidic marine environments.
| S-EPMC4734175 | biostudies-literature
Project description:Hydrothermal vents in the Southern Ocean are the physiologically most isolated chemosynthetic environments known. Here, we describe Kiwa tyleri sp. nov., the first species of yeti crab known from the Southern Ocean. Kiwa tyleri belongs to the family Kiwaidae and is the visually dominant macrofauna of two known vent sites situated on the northern and southern segments of the East Scotia Ridge (ESR). The species is known to depend on primary productivity by chemosynthetic bacteria and resides at the warm-eurythermal vent environment for most of its life; its short-range distribution away from vents (few metres) is physiologically constrained by the stable, cold waters of the surrounding Southern Ocean. Kiwa tylerihas been shown to present differential life history adaptations in response to this contrasting thermal environment. Morphological adaptations specific to life in warm-eurythermal waters, as found on - or in close proximity of - vent chimneys, are discussed in comparison with adaptations seen in the other two known members of the family (K. hirsuta, K. puravida), which show a preference for low temperature chemosynthetic environments.
| S-EPMC4480985 | biostudies-literature
Project description:Animals living in extreme environments, such as hydrothermal vents, would be expected to have evolved protective shells or exoskeletons to maintain homeostasis. The outer part of the exoskeleton of vent crabs (Austinograea sp.) in the Indian Ocean hydrothermal vent was one of the hardest (approximately 7 GPa) biological materials ever reported. To explore the exoskeletal characteristics of vent crabs which enable them to adapt to severe environments, a comparative analysis was conducted with the Asian paddle crab (Charybdis japonica) living in coastal areas. Nanoindentation, thermogravimetric analysis, scanning electron microscopy, energy dispersive x-ray analysis, and Raman spectroscopy were used to analyze the mechanical properties, thermal stability, structure, surface components, and the composition of compounds, respectively. Though both species have four-layered exoskeletons, the outermost layer of the vent crab, a nano-granular structure, was much thicker than that of the coastal crab. The proportions of aluminum and sulfur that constitute the epicuticle of the exoskeleton were higher in the vent crab than in the coastal crab. There was a lack of water or volatile substances, lots of CaCO3, and no carotenoid-based compounds in the exoskeleton of the vent crab. These might have improved the mechanical properties and thermal stability of the hydrothermal species.
| S-EPMC9276715 | biostudies-literature
Project description: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.
| S-EPMC5446156 | biostudies-literature
Project description:To understand the origin, migration, and distribution of organisms across disjunct deep-sea vent habitats, previous studies have documented the population genetic structures of widely distributed fauna, such as gastropods, bivalves, barnacles, and squat lobsters. However, a limited number of investigations has been conducted in the Southwest Pacific Ocean, and many questions remain. In this study, we determined the population structure of the bythograeid crab Austinograea alayseae from three adjacent vent systems (Manus Basin, North Fiji Basin, and Tonga Arc) in the Southwest Pacific Ocean using the sequences of two mitochondrial genes (COI and 16S rDNA) and one nuclear gene (28S rDNA). Populations were divided into a Manus clade and a North Fiji-Tonga clade, with sequence divergence values in the middle of the barcoding gap for bythograeids. We inferred that hydrographic and/or physical barriers act on the gene flow of A. alayseae between the Manus and North Fiji basins. Austinograea alayseae individuals interact freely between the North Fiji Basin and the Lau Basin (Tonga Arc). Although further studies of genetic differentiation over a geological time scale, life-history attributes, and genome-based population genetics are needed to improve our understanding of the evolutionary history of A. alayseae, our results contribute to elucidating the phylogeny, evolution, and biogeography of bythograeids.
| S-EPMC6481846 | biostudies-literature
Project description:Two novel cyclodepsipeptides containing an unusual anthranilic acid dimer and a D-phenyllactic acid residues, clavatustides A and B, were identified from cultured mycelia and broth of Aspergillus clavatus C2WU isolated from Xenograpsus testudinatus, which lives at extreme, toxic habitat around the sulphur-rich hydrothermal vents in Taiwan Kueishantao. This is the first example of cyclopeptides containing an anthranilic acid dimer in natural products, and the first report of microbial secondary metabolites from the hydrothermal vent crab. Clavatustides A and B suppressed the proliferation of hepatocellular carcinoma (HCC) cell lines (HepG2, SMMC-7721 and Bel-7402) in a dose-dependent manner, and induced an accumulation of HepG2 cells in G1 phase and reduction of cells in S phase.
| S-EPMC3877885 | biostudies-other
Project description:Hydrogenovibrio bacteria are ubiquitous in global deep-sea hydrothermal vents. However, their adaptations enabling survival in these harsh environments are not well understood. In this study, we characterized the physiology and metabolic mechanisms of Hydrogenovibrio thermophilus strain S5, which was first isolated from an active hydrothermal vent chimney on the Southwest Indian Ridge. Physiological characterizations showed that it is a microaerobic chemolithomixotroph that can utilize sulfide, thiosulfate, elemental sulfur, tetrathionate, thiocyanate or hydrogen as energy sources and molecular oxygen as the sole electron acceptor. During thiosulfate oxidation, the strain produced extracellular sulfur globules 0.7-6.0 ?m in diameter that were mainly composed of elemental sulfur and carbon. Some organic substrates including amino acids, tryptone, yeast extract, casamino acids, casein, acetate, formate, citrate, propionate, tartrate, succinate, glucose and fructose can also serve as carbon sources, but growth is weaker than under CO2 conditions, indicating that strain S5 prefers to be chemolithoautotrophic. None of the tested organic carbons could function as energy sources. Growth tests under various conditions confirmed its adaption to a mesophilic mixing zone of hydrothermal vents in which vent fluid was mixed with cold seawater, preferring moderate temperatures (optimal 37°C), alkaline pH (optimal pH 8.0), microaerobic conditions (optimal 4% O2), and reduced sulfur compounds (e.g., sulfide, optimal 100 ?M). Comparative genomics showed that strain S5 possesses more complex sulfur metabolism systems than other members of genus Hydrogenovibrio. The genes encoding the intracellular sulfur oxidation protein (DsrEF) and assimilatory sulfate reduction were first reported in the genus Hydrogenovibrio. In summary, the versatility in energy and carbon sources, and unique physiological properties of this bacterium have facilitated its adaptation to deep-sea hydrothermal vent environments.
| S-EPMC5733100 | biostudies-literature