Duplication of a single myhz1.1 gene facilitated the ability of goldfish (Carassius auratus) to alter fast muscle contractile properties with seasonal temperature change

Abstract

Seasonal temperature changes markedly effect the swimming performance of some cyprinid fish acutely tested at different temperatures, involving a restructuring of skeletal muscle phenotype including changes in contractile properties and myosin heavy chain expression. We analyzed the transcriptome of fast myotomal muscle from goldfish (Carassius auratus L.) acclimated to either 8 or 25∘C for 4 weeks (12 h light: 12 h dark) and identified 10 myosin heavy chains (myh) and 13 myosin light chain (myl) transcripts. Goldfish orthologs were classified based on zebrafish nomenclature as myhz1.1α, myhz1.1β, myhz1.1γ, myha, myhb, embryo_myh1, myh9b, smyh2, symh3, and myh11 (myosin heavy chains) and myl1a, myl1b, myl2, myl9a, myl9b, myl3, myl13, myl6, myl12.1a, myl12.1b, myl12.2a, myl12.2b, and myl10 (myosin light chains). The most abundantly expressed transcripts myhz1.1α, myhz1.1β, myhz1.1γ, myha, myl1a, myl1b, myl2, and myl3) were further investigated in fast skeletal muscle of goldfish acclimated to either 4, 8, 15, or 30∘C for 12 weeks (12 h light:12 h dark). Total copy number for the myosin heavy chains showed a distinct optimum at 15∘C (P < 0.01). Together myhz1.1α and myhz1.1β comprised 90 to 97% of myhc transcripts below 15∘C, but only 62% at 30∘C. Whereas myhz1.1α and myhz1.1β were equally abundant at 4 and 8∘C, myhz1.1β transcripts were 17 and 12 times higher than myhz1.1α at 15 and 30∘C, respectively, (P < 0.01). Myhz1.1γ expression was at least nine-fold higher at 30∘C than at cooler temperatures (P < 0.01). In contrast, the expression of myha and myosin light chains showed no consistent pattern with acclimation temperature. A phylogenetic analysis indicated that the previously reported ability of goldfish and common carp to alter contractile properties and myofibrillar ATPase activity with temperature acclimation was related to the duplication of a single myhz1.1 fast muscle myosin heavy chain found in basal cyprinids such as the zebrafish (Danio rerio).