Abstract
BackgroundHemocyanin is the oxygen transporter of most molluscs. Since the oxygen affinity of hemocyanin is strongly temperature-dependent, this essential protein needs to be well-adapted to the environment. In Tectipleura, a very diverse group of gastropods with > 27,000 species living in all kinds of habitats, several hemocyanin genes have already been analyzed. Multiple independent duplications of this gene have been identified and may represent potential adaptations to different environments and lifestyles. The aim of this study is to further explore the evolution of these genes by analyzing their exon–intron architectures.ResultsWe have reconstructed the gene architectures of ten hemocyanin genes from four Tectipleura species: Aplysia californica, Lymnaea stagnalis, Cornu aspersum and Helix pomatia. Their hemocyanin genes each contain 53 introns, significantly more than in the hemocyanin genes of Cephalopoda (9–11), Vetigastropoda (15) and Caenogastropoda (28–33). The gene structures of Tectipleura hemocyanins are identical in terms of intron number and location, with the exception of one out of two hemocyanin genes of L. stagnalis that comprises one additional intron. We found that gene structures that differ between molluscan lineages most probably evolved more recently through independent intron gains.ConclusionsThe strict conservation of the large number of introns in Tectipleura hemocyanin genes over 200 million years suggests the influence of a selective pressure on this gene structure. While we could not identify conserved sequence motifs within these introns, it may be simply the great number of introns that offers increased possibilities of gene regulation relative to hemocyanin genes with less introns and thus may have facilitated habitat shifts and speciation events. This hypothesis is supported by the relatively high number of introns within the hemocyanin genes of Pomacea canaliculata that has evolved independently of the Tectipleura. Pomacea canaliculata belongs to the Caenogastropoda, the sister group of Heterobranchia (that encompass Tectipleura) which is also very diverse and comprises species living in different habitats. Our findings provide a hint to some of the molecular mechanisms that may have supported the spectacular radiation of one of Metazoa’s most species rich groups.
Highlights
Hemocyanin is the oxygen transporter of most molluscs
The revised exon–intron architecture of Biomphalaria glabrata Hemocya‐ nin-like (BgHcl)-2 is highly similar to the gene structure of other Tectipleura hemocyanins (Fig. 3). Differences of this exon–intron structure to those of full-length hemocyanins of Tectipleura are only present in sequence sections that were poorly resolved within the published genome of B. glabrata: In Functional unit (FU)-c and in FU-f we have found sequence motifs which are usually conserved in hemocyanins but could not be detected in the BgHcl-2 gene
High conservation of intron positions as found for hemocyanin genes of Tectipleura is a frequently occurring phenomenon in orthologous genes of animals [30,31,32] but it is striking for hemocyanin genes of Tectipleura, since they feature 46 conserved internal introns instead of three (Nautilus pompilius), four (Octopodoidea) or seven (Lepetellida) and all of them stayed at the exact same position for more than 200 million years. These results are surprising as they do not correspond with the hemocyanin gene structures of Caenogastropoda elucidated by Chiumiento et al [21]. Their results indicate that accumulation of introns as we have detected in Tectipleura is a common feature of hemocyanin genes of Apogastropoda, but on the other hand, the four hemocyanin genes of P. canaliculata vary in number and positions of introns and do not show such a strong conservation as we have identified for Tectipleura
Summary
Hemocyanin is the oxygen transporter of most molluscs. Since the oxygen affinity of hemocyanin is strongly temperature-dependent, this essential protein needs to be well-adapted to the environment. The Mollusca is the second largest animal phylum and comprises diverse species with an enormous array of different body forms, physiologies, habitats and behaviors. They are divided into eight major classes (e.g. Schäfer et al BMC Ecol Evo (2021) 21:36. Gastropoda encompass the five major groups Patellogastropoda, Vetigastropoda, Neritimorpha, Caenogastropoda and Heterobranchia of which especially the latter two are highly diverse Together they form the clade Apogastropoda [1] and include about 68,800 different species [2]. The oxygen transporter of molluscs, namely hemocyanin, must have been adapted to new environments because the oxygen affinity of this protein is known to be temperature-dependent [3,4,5,6].
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