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Open Access Research article

Gill transcriptome response to changes in environmental calcium in the green spotted puffer fish

Patrícia IS Pinto1, Hideo Matsumura2, Michael AS Thorne3, Deborah M Power1, Ryohei Terauchi4, Richard Reinhardt5 and Adelino VM Canário1*

Author affiliations

1 Centro de Ciências do Mar (CCMAR), CIMAR-Laboratório Associado, University of Algarve, Campus de Gambelas, 8005-139 Faro, Portugal

2 Gene Research Center, Shinshu University, Nagano, 390-8621, Japan

3 British Antarctic Survey (BAS), High Cross, Madingley Road, Cambridge, CB3 0ET, UK

4 Iwate Biotechnology Research Center (IBRC), 22-174-4 Narita, Kitakami, Iwate 024-0003, Japan

5 Max Planck Institute for Molecular Genetics (MPIMG), Ihnestraße 63-73 - 14195 Berlin, Germany

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Citation and License

BMC Genomics 2010, 11:476  doi:10.1186/1471-2164-11-476

Published: 17 August 2010

Abstract

Background

Calcium ion is tightly regulated in body fluids and for euryhaline fish, which are exposed to rapid changes in environmental [Ca2+], homeostasis is especially challenging. The gill is the main organ of active calcium uptake and therefore plays a crucial role in the maintenance of calcium ion homeostasis. To study the molecular basis of the short-term responses to changing calcium availability, the whole gill transcriptome obtained by Super Serial Analysis of Gene Expression (SuperSAGE) of the euryhaline teleost green spotted puffer fish, Tetraodon nigroviridis, exposed to water with altered [Ca2+] was analysed.

Results

Transfer of T. nigroviridis from 10 ppt water salinity containing 2.9 mM Ca2+ to high (10 mM Ca2+ ) and low (0.01 mM Ca2+) calcium water of similar salinity for 2-12 h resulted in 1,339 differentially expressed SuperSAGE tags (26-bp transcript identifiers) in gills. Of these 869 tags (65%) were mapped to T. nigroviridis cDNAs or genomic DNA and 497 (57%) were assigned to known proteins. Thirteen percent of the genes matched multiple tags indicating alternative RNA transcripts. The main enriched gene ontology groups belong to Ca2+ signaling/homeostasis but also muscle contraction, cytoskeleton, energy production/homeostasis and tissue remodeling. K-means clustering identified co-expressed transcripts with distinct patterns in response to water [Ca2+] and exposure time.

Conclusions

The generated transcript expression patterns provide a framework of novel water calcium-responsive genes in the gill during the initial response after transfer to different [Ca2+]. This molecular response entails initial perception of alterations, activation of signaling networks and effectors and suggests active remodeling of cytoskeletal proteins during the initial acclimation process. Genes related to energy production and energy homeostasis are also up-regulated, probably reflecting the increased energetic needs of the acclimation response. This study is the first genome-wide transcriptome analysis of fish gills and is an important resource for future research on the short-term mechanisms involved in the gill acclimation responses to environmental Ca2+ changes and osmoregulation.