Molecular characterization and evolution of haemocyanin from the two freshwater shrimps Caridina multidentata (Stimpson,
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ORIGINAL PAPER
Molecular characterization and evolution of haemocyanin from the two freshwater shrimps Caridina multidentata (Stimpson, 1860) and Atyopsis moluccensis (De Haan, 1849) Julia C. Marxen • Christian Pick • Marcel Kwiatkowski Thorsten Burmester
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Received: 19 April 2012 / Revised: 22 November 2012 / Accepted: 29 December 2012 / Published online: 22 January 2013 Ó Springer-Verlag Berlin Heidelberg 2013
Abstract Haemocyanin (Hc) is a copper-containing respiratory protein, floating freely dissolved in the hemolymph of many arthropod species. A typical haemocyanin is a hexamer or oligohexamer of six identical or similar subunits, with a molecular mass around 75 kDa each. In the crustaceans, the haemocyanins appear to be restricted to the remipedes and the malacostracans. We have investigated the haemocyanins of two freshwater shrimps, the Amano shrimp Caridina multidentata and the bamboo shrimp Atyopsis moluccensis. We obtained three full-length and one partial cDNA sequences of haemocyanin subunits from the Amano shrimp, which were assigned to the a- and c-types of decapod haemocyanin subunits. Three complete and two partial haemocyanin cDNA sequences were obtained from the bamboo shrimp, which represent subunit types a, b and c. This is the first time that sequences of all three subunit types of the decapod haemocyanins were obtained from a single species. However, mass spectrometry analyses identified only a- and c-type subunits, suggesting that a b-subunit is not a major component of the
native haemocyanin of the bamboo shrimp. Phylogenetic and molecular clock analyses showed that malacostracan haemocyanins commenced to diversify into distinct subunit types already *515 million years ago. b-subunits diverged first, followed by a- and c-type subunits *396 million years ago. The haemocyanins of phyllocarids and peracarids form distinct clades within the a/c-cluster. Within the Caridea, an early divergence of distinct a-type subunits occurred *200 MYA. The tree of the c-subunits suggests a common clade of the Caridea (shrimps) and Penaeidae (prawns). Keywords Crustacea Decapoda Respiratory protein Haemocyanin Phylogeny Subunit
Communicated by G. Heldmaier.
Abbreviations Hc Haemocyanin MYA Million years ago PCR Polymerase chain reaction SDS-PAGE Sodium dodecyl sulfate-polyacrylamide gel electrophoresis Cmu Caridina multidentata Amo Atyopsis moluccensis
Electronic supplementary material The online version of this article (doi:10.1007/s00360-013-0740-9) contains supplementary material, which is available to authorized users.
Introduction
J. C. Marxen (&) C. Pick T. Burmester Institute of Zoology and Zoological Museum, University of Hamburg, Martin-Luther-King-Platz 3, 20146 Hamburg, Germany e-mail: [email protected] M. Kwiatkowski Department of Clinical Chemistry, University Medical Center Hamburg-Eppendorf, Campus Forschung, Martinistr. 52, 20246 Hamburg, Germany
Oxygen supply in many arthropod species is mediated by haemocyanin, which is floating freely dissolved in the he
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