Influence of Temperature, Hypercapnia, and Development on the Relative Expression of Different Hemocyanin Isoforms in the Common Cuttlefish Sepia officinalis

Abstract

The cuttlefish Sepia officinalis expresses several hemocyanin isoforms with potentially different pH optima, indicating their reliance on efficient pH regulation in the blood. Ongoing ocean warming and acidification could influence the oxygen-binding properties of respiratory pigments in ectothermic marine invertebrates. This study examined whether S. officinalis differentially expresses individual hemocyanin isoforms to maintain optimal oxygen transport during development and acclimation to elevated seawater pCO 2 and temperature. Using quantitative PCR, we measured relative mRNA expression levels of three different hemocyanin isoforms in several ontogenetic stages (embryos, hatchlings, juveniles, and adults), under different temperatures and elevated seawater pCO 2 . Our results indicate moderately altered hemocyanin expression in all embryonic stages acclimated to higher pCO 2 , while hemocyanin expression in hatchlings and juveniles remained unaffected. During the course of development, total hemocyanin expression increased independently of pCO 2 or thermal acclimation status. Expression of isoform 3 is reported for the first time in a cephalopod in this study and was found to be generally low but highest in the embryonic stages (0.2% of total expression). Despite variable hemocyanin expression, hemolymph total protein concentrations remained constant in the experimental groups. Our data provide first evidence that ontogeny has a stronger influence on hemocyanin isoform expression than the environmental conditions chosen, and they suggest that hemocyanin protein abundance in response to thermal acclimation is regulated by post-transcriptional/translational rather than by transcriptional modifications.

Transcriptome Sequencing and De Novo Assembly of Golden Cuttlefish Sepia esculenta Hoyle

“…Many studies have focused on investigating the physiological characters, environmental adaptations and cultivation improvements in Sepia [8,16,17,18]. However, though several sequencing data records deposited in NCBI database, there’re no systematic dissection on the genome and transcriptome information of Sepia published [19].…”

Environmental pH, O2 and Capsular Effects on the Geochemical Composition of Statoliths of Embryonic Squid Doryteuthis opalescens

“…The structures of the capsule can connect the external chemical environment to the embryo via the capsular membranes, interstitial jelly and the chorion membrane (hereafter, these effects are collectively referred to as "capsular effects"). The pH/pCO 2 and [O 2 ] of the perivitelline fluid that surrounds the embryo are impacted additively by the environment and by the physiological processes of the embryo itself [17][18][19][42][43][44][45][46][47]. Elemental incorporation within statoliths can be influenced by the environment [30,33,34,48], but physiological process impacts on statolith geochemistry, including processes within the statocyst [41], embryo [18,19,45,46], as well as within outer-embryo structures [49,50], are not well understood.…”

A new haemocyanin in cuttlefish (Sepia officinalis) eggs: sequence analysis and relevance during ontogeny

“…So far, the complete mRNA sequences of haemocyanin isoform 1 (SoH1 [GenBank:DQ388569]) and isoform 2 (SoH2 [GenBank:DQ388570]) have been identified in Sepia officinalis . Next to these two known isoforms there is great evidence for a third one in the cuttlefish (SoH3; [21,22]), whereof one fragment of ~1,000 bp has already been sequenced [GenBank:JN392726]. The existence of these isoforms raises questions about their evolution referring to origin and structural changes as well as to their physiological relevance.…”

“…However, all isoforms are expressed, and SoH1 and SoH2 even display different theoretical isoelectric points ( in silico : SoH1: pI = 5.79, SoH2: pI = 5.85), which in turn could affect the oxygen affinity [21,22]. The existence of different isoforms might therefore serve a physiological purpose.…”