Alanine, proline and urea are major organic osmolytes in the snail<i>Theodoxus fluviatilis</i>under hyperosmotic stress

Wiesenthal, Amanda A.; Müller, Christian; Harder, Katrin; Hildebrandt, Jan‐Peter

doi:10.1242/jeb.193557

Cited by 26 publications

(34 citation statements)

References 54 publications

(78 reference statements)

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“…Presumably, in this study, the hyperosmotic treatment of gill filament culture induced the expression of klf4 to increase chloride cell densities. The miR-200b-3p target-gene, slc17a5 belongs to the solute carrier family of transporters to transport amino acids [50], which can serve as organic osmolytes to regulate cellular osmolality, against hyperosmotic stress [51]. The implication of the data are consistent with the physiological responses of fish gills.…”

Section: Discussionsupporting

confidence: 62%

Genome-wide analysis of MicroRNA-messenger RNA interactome in ex-vivo gill filaments, Anguilla japonica

Nong

et al. 2020

BMC Genomics

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Background: Gills of euryhaline fishes possess great physiological and structural plasticity to adapt to large changes in external osmolality and to participate in ion uptake/excretion, which is essential for the re-establishment of fluid and electrolyte homeostasis. The osmoregulatory plasticity of gills provides an excellent model to study the role of microRNAs (miRs) in adaptive osmotic responses. The present study is to characterize an ex-vivo gill filament culture and using omics approach, to decipher the interaction between tonicity-responsive miRs and gene targets, in orchestrating the osmotic stress-induced responses. Results: Ex-vivo gill filament culture was exposed to Leibovitz's L-15 medium (300 mOsmol l − 1 ) or the medium with an adjusted osmolality of 600 mOsmol l − 1 for 4, 8 and 24 h. Hypertonic responsive genes, including osmotic stress transcriptional factor, Na + /Cl − -taurine transporter, Na + /H + exchange regulatory cofactor, cystic fibrosis transmembrane regulator, inward rectifying K + channel, Na + /K + -ATPase, and calcium-transporting ATPase were significantly upregulated, while the hypo-osmotic gene, V-type proton ATPase was downregulated. The data illustrated that the ex-vivo gill filament culture exhibited distinctive responses to hyperosmotic challenge. In the hyperosmotic treatment, four key factors (i.e. drosha RNase III endonuclease, exportin-5, dicer ribonuclease III and argonaute-2) involved in miR biogenesis were dysregulated (P < 0.05). Transcriptome and miR-sequencing of gill filament samples at 4 and 8 h were conducted and two downregulated miRs, miR-29b-3p and miR-200b-3p were identified. An inhibition of miR-29b-3p and miR-200b-3p in primary gill cell culture led to an upregulation of 100 and 93 gene transcripts, respectively. Commonly upregulated gene transcripts from the hyperosmotic experiments and miR-inhibition studies, were overlaid, in which two miR-29b-3p target-genes [Krueppel-like factor 4 (klf4), Homeobox protein Meis2] and one miR-200b-3p target-gene (slc17a5) were identified. Integrated miR-mRNA-omics analysis revealed the specific binding of miR-29b-3p on Klf4 and miR-200b-3p on slc17a5. The target-genes are known to regulate differentiation of gill ionocytes and cellular osmolality.(Continued on next page) Conclusions: In this study, we have characterized the hypo-osmoregulatory responses and unraveled the modulation of miR-biogenesis factors/the dysregulation of miRs, using ex-vivo gill filament culture. MicroRNAmessenger RNA interactome analysis of miR-29b-3p and miR-200b-3p revealed the gene targets are essential for osmotic stress responses.

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Section: Discussionsupporting

confidence: 62%

Genome-wide analysis of MicroRNA-messenger RNA interactome in ex-vivo gill filaments, Anguilla japonica

Nong

et al. 2020

BMC Genomics

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“…Euryhaline mollusks mainly accumulate amino acids as organic osmolytes in their cells under hyperosmotic stress (Shumway et al, 1977;Pierce and Amende, 1981). T. fluviatilis from both freshwater and mesohaline conditions showed the ability to accumulate organic osmolytes in response to hyperosmotic stress equally well; however, they differ in the pathways of acquiring these organic osmolytes (Wiesenthal et al, 2019). The main constituents of the increased amounts of organic osmolytes are alanine and proline that seem to be most important for an initial coping with high environmental salinity conditions and were also among the most important amino acid pathways that responded in the microbiome.…”

Section: Discussionmentioning

confidence: 99%

Impact of Salinity on the Gastrointestinal Bacterial Community of Theodoxus fluviatilis

et al. 2020

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Differences in salinity are boundaries that act as barriers for the dispersal of most aquatic organisms. This creates distinctive biota in freshwater and brackish water (mesohaline) environments. To test how saline boundaries influence the diversity and composition of host-associated microbiota, we analyzed the microbiome within the digestive tract of Theodoxus fluviatilis, an organism able to cross the freshwater and mesohaline boundary. Alpha-diversity measures of the microbiome in freshwater and brackish water were not significantly different. However, the composition of the bacterial community within freshwater T. fluviatilis differed significantly compared with mesohaline T. fluviatilis and typical bacteria could be determined for the freshwater and the mesohaline digestive tract microbiome. An artificial increase in salinity surrounding these freshwater snails resulted in a strong change in the bacterial community and typical marine bacteria became more pronounced in the digestive tract microbiome of freshwater T. fluviatilis. However, the composition of the digestive tract microbiome in freshwater snails did not converge to that found within mesohaline snails. Within mesohaline snails, no cardinal change was found after either an increase or decrease in salinity. In all samples, Pseudomonas, Pirellula, Flavobacterium, Limnohabitans, and Acinetobacter were among the most abundant bacteria. These bacterial genera were largely unaffected by changes in environmental conditions. As permanent residents in T. fluviatilis, they may support the digestion of the algal food in the digestive tract. Our results show that freshwater and mesohaline water host-associated microbiomes respond differently to changes in salinity. Therefore, the salinization of coastal freshwater environments due to a rise in sea level can influence the gut microbiome and its functions with currently unknown consequences for, e.g., nutritional physiology of the host.

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“…DEGs in the brackish water population were enriched not only in chitin metabolism but also in urea transport. Urea functions as an osmolyte, and holds special importance for cell volume preservation in an aquatic snail under hyperosmotic stress 35 . However, it is not clear why genes associated with urea were enriched only in the brackish water population and those associated with nitrogen-containing compounds only in the freshwater population; although both of them are osmolytes which act to prevent water loss in hyperosmotic environments.…”

Section: Discussionmentioning

confidence: 99%

Changes in transcriptomic response to salinity stress induce the brackish water adaptation in a freshwater snail

Yokomizo

Takahashi

2020

Sci Rep

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Studying the mechanisms of the establishment of a population in a novel environment allows us to examine the process of local adaptations and subsequent range expansion. In a river system, detecting genetic or phenotypic differences between a freshwater and brackish water population could contribute to our understanding of the initial process of brackish water adaptation. Here, we investigated behavioural and gene expression responses to salt water in a freshwater and brackish water population of the freshwater snail, Semisulcospira reiniana. Although the individuals in brackish water exhibited significantly higher activity in saltwater than freshwater individuals just after sampling, the activity of freshwater individuals had increased in the second observation after rearing, suggesting that their salinity tolerance was plastic rather than genetic. We found 476 and 1002 differentially expressed genes across salinity conditions in the freshwater and brackish water populations, respectively. The major biological process involved in the salinity response of the freshwater population was the biosynthesis and metabolic processing of nitrogen-containing compounds, but that of the brackish water population was influenced by the chitin metabolic process. These results suggest that phenotypic plasticity induces adaptation to brackish water in the freshwater snail by modifying its physiological response to salinity.

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Alanine, proline and urea are major organic osmolytes in the snailTheodoxus fluviatilisunder hyperosmotic stress

Cited by 26 publications

References 54 publications

Genome-wide analysis of MicroRNA-messenger RNA interactome in ex-vivo gill filaments, Anguilla japonica

Genome-wide analysis of MicroRNA-messenger RNA interactome in ex-vivo gill filaments, Anguilla japonica

Impact of Salinity on the Gastrointestinal Bacterial Community of Theodoxus fluviatilis

Changes in transcriptomic response to salinity stress induce the brackish water adaptation in a freshwater snail

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