Transcriptional modulation patterns of abalone Haliotis discus hannai hypoxia inducible factor-1α (HIF-1α) in interdependent crosstalk between hypoxia, infection, and environmental stresses

Abstract

Hypoxia-inducible factor-1α (HIF-1α) is a key transcription factor for regulating oxygen-dependent homeostasis. Here, we characterized HIF-1α in Pacific abalone (Haliotis discus hannai), an aquaculture-relevant mollusk species, and its transcriptional regulation patterns in response to oxygen-dependent and oxygen-independent stimuli were investigated. The molecular cloning and sequence analysis revealed that the abalone HIF-1α shared conversed features in its domain organization such as basic helix–loop–helix (bHLH) domain, Per-Arnt-Sim (PAS) domain, oxygen-dependent degradation domains (ODDDs), and C-terminal transactivation domain (C-TAD) with metazoan orthologs. The abalone HIF-1α was proven to be transcriptionally active in multiple tissues according to dissolved oxygen contents, with the most sensitive responsiveness in the gill. Under non-hypoxic conditions, the tissue-dependent transcriptional regulation patterns of the abalone HIF-1α were closely correlated and intertwined with those of HSP90 and MT in response to thermal challenge and heavy metal exposure, respectively. The abalone HIF-1α expression was significantly modulated under normoxic conditions in response to immune challenges with lipopolysaccharide and Vibrio harveyi with the highest upregulation in the hemocytes. However, the combined treatment of hypoxia and immune stimulation exhibited no synergistic activation for the induction of HIF-1α mRNA. Collectively, dynamic transcriptional regulation of the abalone HIF-1α with the tissue specificity in response to oxygen-dependent and oxygen-independent stimulatory challenges suggests that HIF-1α plays crucial roles in interdependent crosstalk between hypoxia, innate immunity, and environmental stresses, which can be a useful basis to investigate cellular and physiological responses of farmed abalones to oxygen depletion and other-related stress factors.